Dinosaurs: How We Know What We Know [1 ed.] 1138608165, 9781138608160

Citation preview

Dinosaurs

Dinosaurs How We Know What We Know Mary Higby Schweitzer Elena Rita Schroeter Charles Doug Czajka

First edition published 2021 by CRC Press 6000 Broken Sound Parkway NW, Suite 300, Boca Raton, FL 33487-2742 and by CRC Press 2 Park Square, Milton Park, Abingdon, Oxon, OX14 4RN © 2021 Taylor & Francis Group, LLC CRC Press is an imprint of Taylor & Francis Group, LLC Reasonable efforts have been made to publish reliable data and information, but the author and publisher cannot assume responsibility for the validity of all materials or the consequences of their use. The authors and publishers have attempted to trace the copyright holders of all material reproduced in this publication and apologize to copyright holders if permission to publish in this form has not been obtained. If any copyright material has not been acknowledged please write and let us know so we may rectify in any future reprint. Except as permitted under U.S. Copyright Law, no part of this book may be reprinted, reproduced, transmitted, or utilized in any form by any electronic, mechanical, or other means, now known or hereafter invented, including photocopying, microfilming, and recording, or in any information storage or retrieval system, without written permission from the publishers. For permission to photocopy or use material electronically from this work, access www.copyright.com or contact the Copyright Clearance Center, Inc. (CCC), 222 Rosewood Drive, Danvers, MA 01923, 978-750-8400. For works that are not available on CCC please contact [email protected] Trademark notice: Product or corporate names may be trademarks or registered trademarks and are used only for identification and explanation without intent to infringe. ISBN: 978-1-138-60816-0 (hbk) ISBN: 978-0-367-56381-3 (pbk) ISBN: 978-0-429-46671-7 (ebk) Typeset in ITC Leawood by Deanta Global Publishing Services, Chennai, India

MHS: I would like to dedicate this book to my dad, who taught me to see and to love nature; to my brother, who taught me to always question and who first instilled in me my love of dinosaurs; to Nathan, Melissa, Matt, and LeAnne, who are my very heartbeat; to Noah, I hope you grow up to love all living things and to have a never-ending curiosity about them; to Avery, whose curious spirit and giant smile are always with me; and to my students, past, present, and future, who push me to be just a little bit better every year. ERS: I would like to dedicate this book to my mother (Carolann) and my father (William), whose support and encouragement of my curiosity was unfailing (though surely exhausting!).

CONTENTS

Preface ix Acknowledgments xiii

CHAPTER 1: How Do We Understand the Natural World? The Nature of Science and the Field of Paleontology

1

CHAPTER 2: How Do We Know When Dinosaurs Lived? Interpreting Earth’s History from Rocks

19

CHAPTER 3: How Do We Explain Variation among Past and Present Organisms? Evolution and Evolutionary Mechanisms 53 CHAPTER 4: How Do We Know Who Is Related to Whom? Systematics and Phylogenetic Relationships

77

CHAPTER 5: How Do We Know When and How Life Began and Evolved? The Origin of Life and Evolution through Time 97 CHAPTER 6: How Do We Use Anatomy of Living Animals to Understand Dinosaurs? Bones and Anatomy 125 CHAPTER 7: How Do We Know What a Dinosaur Is? Diagnosing and Defining Dinosauria 137 CHAPTER 8: How Do We Name and Group Dinosaurs? Part I: Ornithischian Dinosaurs 155 CHAPTER 9: How Do We Name and Group Dinosaurs? Part II: Saurischian Dinosaurs 189

viii

Contents

CHAPTER 10: How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs? Pterosaurs, Marine Reptiles, Mammals, and Others

225

CHAPTER 11: How Do We Know How Dinosaurs Became Part of the Fossil Record? Taphonomy and Fossilization

255

CHAPTER 12: How Do We Interpret the Ecology of Dinosaurs? The Relationship of Dinosaurs to Their Physical and Biological Environments

277

CHAPTER 13: How Do We Know How Dinosaurs Moved? Dinosaur Functional Morphology 301 CHAPTER 14: How Do We Know What Dinosaurs Looked Like? Dinosaur Appearance 325 CHAPTER 15: How Do We Know What Dinosaurs Ate? Direct and Indirect Evidence for Dinosaur Diets 349 CHAPTER 16: How Do We Interpret Dinosaur Behavior? Dinosaur Trackways, Herding, and Pathologies

375

CHAPTER 17: How Do We Know about Dinosaur Reproduction? Mating and Parental Care among Dinosaurs 407 CHAPTER 18: How Do We Know If Dinosaurs Were Warm-Blooded, Cold-Blooded, Or Something in Between? Dinosaur Physiology and Metabolism 439 CHAPTER 19: How Do We Know Birds Are Dinosaurs? The Phylogeny of Maniraptoriformes and the Origin of Flight

469

CHAPTER 20: How Do We Know about Extinctions? The End of the Dinosaur Reign and Other Mass Extinctions 505 Index 535

PREFACE

I

n writing this book, we sought to use student fascination with dinosaurs to illustrate, and practice, the process of science. Thus, this textbook grew out of our love for student learning and curiosity as much as our passion for Earth history and dinosaurs. It had its germination during our complete overhaul of an introductory college class on dinosaurs. We wanted the course to better engage students by allowing them to explore bone and fossil specimens, analyze evidence and data, and work collaboratively with their peers to develop, and then test, new ideas. The revised course was designed to allow students to behave like scientists through making observations, testing ideas, and thinking critically about the things we know—and don’t—all the while working together, because as it is practiced in “real life”, science is a collective effort that doesn’t happen in isolation. Furthermore, we hoped that by studying these exotic, ancient, and extinct beasts, students would learn more about the world they have inherited. Our goals for this book were similar to our goals for the class. Too often in our collective teaching experiences, we observed that many students view science as a rather boring collection of facts that someone else has already figured out, with little opportunity for them to contribute to the body of knowledge in any meaningful way. In our minds, the most exciting parts about science are the things we don’t know, as this is what keeps science moving forward. The central theme (and title!) of the book is the demonstration of not just what we know, but how we know the things we know about dinosaurs. This is important, because most of what we know about extinct dinosaurs cannot come from observing them in life. Instead, it comes from the fossil record, an incomplete source that we must carefully interpret, using scientific principles and observations of different life forms today—different, but bound by the same constraints that operated on dinosaurs. For this reason, it can be unclear to those outside the field of paleontology of just how we arrive at the understanding we possess about the Earth and animals of the past. Through this approach, we hope to give readers an idea of how one can go about answering paleontological questions from a temporal separation of 65 million years (or more!). We also fear that many students leave science courses with the impression that there are no questions or discoveries left to be made in science. This could not be further from the truth! It is our goal for readers to come away from this book not only having learned something new, but also with the impression that there is still so much to learn. To help accomplish this, every chapter includes a section entitled “What We Don’t Know”. It is here that we discuss some of the bigger unanswered questions around each chapter’s topic and present a series of questions that one might consider in light of the unknowns. Science is driven by human curiosity, and we hope these sections encourage readers to develop their own curiosity about the things they are learning! Finally, students often ask us, “Do you have any advice for studying for this class?” In the below section, we provide information about how you might utilize this text and provide a few brief tips for reading and stud-

x

Preface

ying based on what education research has shown to be most effective for improving learning.

A NOTE TO STUDENTS: HOW TO USE THIS BOOK As you read through the book, you will notice that each section starts with a list of objectives, or things you should be able to do after reading that section. The purpose behind these objectives is to assist with active reading, a technique that employs study strategies that have been shown to make learning more effective. The objectives are designed to give you an idea of what you should get out of reading each section and help outline the main points of what you are reading. A great strategy for how you might use these objectives to improve learning and retention might include the following steps: 1. Write the objectives for the section down with some space after each one. 2. Read through the section with the objectives in mind and highlight or annotate if you find this helpful. 3. Attempt to recall and write out what the objective is asking without looking at the text. 4. Fill in any gaps by reviewing the relevant text section. 5. Relate what you have just read to previous information you have learned and add that to your notes. By using the above method of active reading, you are employing two effective, research-proven learning strategies. In Step 3, practice testing pushes you to try to actively recall information. Numerous research studies have shown that practice testing is one of the best strategies you can incorporate into your studying if you want to increase learning. We recommend using it anytime you study, not just when you read. Flashcards or generating your own practice test questions are great ways to incorporate practice testing. In Step 5, you are using self-explanation, a strategy where you explain how newly learned material is related to known information, another technique with evidence showing that it supports learning. If we could offer one final suggestion, it would be to make sure you are spreading your studying out. This is a strategy known as distributed practice, and the research supporting its effectiveness is very robust. Distributed practice is the strategy of using a set schedule to spread studying out over time. This is the opposite approach of the all too common strategy of “cramming” (massed studying), which manifests as a long period of study without break, often utilized the night before an exam. Distributed practice encourages multiple, short study sessions (20–45 minutes), that are spread out over multiple days. Reviews of hundreds of studies examining the effect of distributed practice show that, on average, 10% more material is recalled when using distributed practice versus massed study. Think of this as a full letter grade improvement on an exam, just by changing when you study! We hope that you will find these tips beneficial, but most importantly, we hope this book sparks your curiosity and leads you to ask new questions, all the while learning about some of the most iconic animals to have ever roamed the Earth!

A NOTE TO INSTRUCTORS Dinosaurs are a great way to get students excited about science, and teaching introductory courses about dinosaurs can serve as a gateway

Preface

for getting students interested in other STEM disciplines such as biology and geology. Beyond adopting this textbook, we want to provide other supports for instructors who teach, or are interested in teaching, introductory dinosaur courses. To do this, we have created the website teachingdinosaurs.com. It will allow you to access numerous teaching resources, such as in-class activities, learning objectives, question banks, mastery quizzes, information on using and obtaining teaching specimens, and more! We encourage you to check out the site, hopefully find some useful resources for your teaching, and leave us any feedback you might have so we can continue to improve the resources available to instructors!

xi

ACKNOWLEDGMENTS

We thank Kaitlyn Tiffany for her tireless efforts in photography and photo editing, which were integral in bringing the concepts we discuss in this book to life. This book would not be possible without her help. Additionally, we thank Gail Tiffany for giving us the benefit of her expertise in photo editing. We thank our many colleagues who were so patient with our endless questions and clarifications, and who gave freely of their time to review the content of each chapter. We can never know all the intricacies of each of your fields, but we hope we have represented them adequately. Our heartfelt gratitude goes out to the amazing paleoartists who generously allowed us to use their artwork in this text. We would especially like to recognize the extensive contributions of Karen Carr, Mark Hallet, Luis Rey, and Mark Witton. Additionally, we thank our colleagues who shared their data and images with us directly or on Creative Commons and other open-access venues. Your images allowed us to illustrate concepts words could never capture. Finally, we are grateful for all the Natural History Museums that provided us access to specimens for photography, which were invaluable to the completion of this work.

1 1

HOW DO WE UNDERSTAND THE NATURAL WORLD? THE NATURE OF SCIENCE AND THE FIELD OF PALEONTOLOGY

D

inosaur paleontology is a science, but have you ever thought about what exactly science is or how you would define it? Many people view science as simply a collection of facts we know about how the world and universe operate. But this is only part of the truth, because all the things that we don’t know about the world are equally important, and, as you can imagine, there are a lot of things we don’t know! Science is also a process—a process that builds upon itself, a challenge to solve those unknowns. There are so many things left to figure out and so much science to be done! With this book, we have tried to discuss both the known and unknown in our understanding of dinosaurs. We will of course deal with what is known about the topic of each chapter. We also hope to go beyond just telling what is known, but to be explicit in showing how that knowledge came to be; what hypotheses, observations, and experiments led to the generation of this knowledge. We will then end each chapter with a discussion of things we don’t know and questions to consider that will hopefully provoke further thought, discussion, and wonder. Science, as we will see later in this chapter, is ultimately driven by human curiosity. In that respect, we are all innately scientists. Even if you don’t think you are a science person or good at science, you practice the process of science all the time! At some point in your life you have probably been curious about how something works, or why something happens, and regardless of how trivial this curiosity may have been, you probably engaged in some type of scientific thinking while pondering such questions (Figure 1.1). And most likely you are taking a course on dinosaurs and/or reading this book because you are interested (and curious) about dinosaur science. As you study, learn, and practice science, try to harness your curiosity by asking questions and formulating testable hypotheses beyond the basic concepts. Try to come up with your own ideas of what we don’t know in addition to those at the end of each chapter. Invoking your curiosity can make learning science easier and more enjoyable. Arguably, the most important part of learning (and sci-

IN THIS CHAPTER . . . 1.1 DEFINING SCIENCE 1.2 THE ANATOMY OF SCIENTIFIC INVESTIGATION 1.3 WHAT IS PALEONTOLOGY? 1.4 HOW DOES PALEONTOLOGY FIT INTO SCIENCE? 1.5 A BRIEF HISTORY OF DINOSAUR PALEONTOLOGY 1.6 WHY STUDY PALEONTOLOGY?

2

CHAPTER 1    How Do We Understand the Natural World? Figure 1.1  A collection of preserved specimens and literature at the Naturalist Center in the North Carolina Museum of Natural Science, Raleigh, NC. Looking at this image,

what is one thing you are curious about? What would you like to see closer? What is one question you have? (Courtesy of E. Schroeter.)

ence!) is being able to ask new questions, more than being able to state new facts.

1.1 DEFINING SCIENCE After reading this section you should be able to… • Define “science” and describe the features of a scientific investigation. • Compare and contrast observations vs. interpretations. • Explain how experimental and historical science are different.

Science is a system of acquiring knowledge that uses observation, experimentation, and interpretation to describe natural phenomena. It rests on both “rules” and definitions. Any scientific endeavor must be systematic, testable, falsifiable, and must allow for predictions to be generated and then tested. Let’s unpack some of the information in the previous paragraph so that we can make better sense of what science is. Acquiring new knowledge most often begins by making observations. In science, observations include not only the general meaning of visually noting something, but also includes recording what is observed—and that recording is considered data. So if you used a ruler to measure the length of a dinosaur tooth, that would be considered an observation in the scientific sense. Data, then, can be defined as a collection of measured observations. In science, data are all we have, and all science rests on data—not opinion, not hearsay, not “what makes sense”. Just data. Data can be qualitative or quantitative: • Qualitative data are observations that are not expressed in numbers (e.g., blue, salty, loud). • Quantitative data are observations that consist of numerical measurements (e.g., 12 m, 40°C, 5 mL).

1.1  Defining Science

Note that most variables that we might measure can be expressed either qualitatively or quantitatively—a noise can be “loud” or it can be 100 decibels, a pair of pants can have a size of “extra large” or size 40-inch waist. The distinction between qualitative and quantitative is not in the variable we are measuring, but in how we as researchers are choosing to measure and record it. Thus, “The femur of this dinosaur is longer than its circumference” is qualitative, and “A full-grown Tyrannosaurus rex measures up to 12 m (~40 ft) from nose to tail”, is quantitative. Experimentation within the realm of science will be more thoroughly explained in Section 1.2, but observations are often used to conduct experiments in order to answer research questions of interest. Finally, it is important to distinguish between observations and interpretations. When observations are collected about a natural phenomenon or used to evaluate experiments, interpretations are then made based on the observations or results of experimentation. Distinguishing between the two can sometimes be tricky. Take for example the statement “this structure was made from a meteorite impact”. While this may sound like scientific data (especially if an expert tells you so), it is actually an interpretation. This interpretation may be based on measurements (data!) and comparison with other structures (data!), but unless there is a video of the impactor making the feature, we can only make informed interpretations about the origin of the structure. This doesn’t mean that interpretations aren’t useful or based on factual evidence, it just means they are not the result of direct observation. Section 1.2 will further elaborate on the scientific process and introduce more of the vocabulary used in scientific investigations. There are two main branches of science: • Natural sciences: These are the sciences that deal with the physical world and can be further broken down into two further subbranches. • Life sciences: Biology and all its subdisciplines (e.g., zoology, botany) that are concerned with the living, organic world are part of life sciences. • Physical sciences: Physics, chemistry, astronomy, and Earth sciences are all considered physical science and study the non-living world and universe. • Social sciences: These are the sciences that deal with aspects of human society and relationships. The social sciences include fields like philosophy, sociology, anthropology, archaeology, and social psychology. Additionally, there are two types of scientific studies: • Experimental science: Involve testing through experimentation, often in a laboratory, and rely on repeatability. So that way, if two people set up the same experiment, using the same materials and the same conditions, they should get the same results. • Historical science: Uses observations (i.e., data) to make conclusions about past events but does not involve direct experimentation. Historical science also relies on repeatability, but it is of a different kind; if I have the same data, I should be able to come to the same conclusions as other researchers before me. The following is an example. Structures like those in Figure 1.2 are interpreted to be the results of impacts by extra-terrestrial bodies upon a planetary surface. When a scientist can see and touch and measure all aspects of (A), which is located in Arizona, they can apply many of their interpretations to extremely

3

4

CHAPTER 1    How Do We Understand the Natural World? Figure 1.2  Impact craters. Direct

observations of the (A) Barringer crater in Arizona that can inform scientists about the (B) Korolev crater on Mars and lead to the interpretation that both structures were formed by a meteorite impact. (A courtesy of D. Roddy, US Geological Survey, https:// commons.wikimedia.org/wiki/File:Barringer_ Meteor_Crater,_Arizona.jpg; B courtesy of Björn Schreiner ESA/DLR/FU Berlin, https:// commons.wikimedia.org/wiki/File:Pers​pecti​ ve_vi​ew_of​_Koro​lev_c​rater​.jpg.​)

similar structures shown in (B), which is located on Mars. Whether a scientist is located in America, Spain, or China, those interpretations— that some structure with a certain mass hit Mars in the past—will be the same. Repeatability in historical science is different than in experimental science, but it is still extremely important. Only through the historical sciences can certain ideas be tested. For example, the impact that certain ecological processes may have on the eventual morphology (shape) of an organism, or the gradual acquisition of traits within organisms that are commonplace today can only be observed through the fossil record. Has our atmosphere always consisted of the same ratio of gasses that it has today? Have mountain ranges always existed where they are currently located? Have our oceans always divided the continents in the same way we observe today? How do populations change over time? What are the drivers of speciation? What events contribute to extinction, or recovery from extinctions? How do communities of organisms respond over time to disturbances? These are questions only the historical sciences can answer. By now you may be wondering just where paleontology and the study of dinosaurs fit into these science classifications (hint: it’s not a social science!). Before describing exactly how paleontology fits into the sciences in Section 1.3, it is important to cover some important details of scientific investigations.

1.2 THE ANATOMY OF SCIENTIFIC INVESTIGATION After reading this section you should be able to… • Explain the difference between hypotheses, theories, and laws. • Describe three ways to test hypotheses. • Argue for the importance of falsifiability in science.

Any scientific investigation, whether it be experimental or historical, follows a set of principles that are commonly referred to as the scientific method. Rather than a series of steps that must be followed, the scientific method is a set of principles that are utilized to ensure that scientific investigations are rigorous and sound. A hypothesis is a scientific statement that guides the approach of an investigation, and it must follow certain rules. It must be testable, able to be independently verified, formulated so that one may make predictions from it, and—perhaps most importantly—it must be capable of being proven false. A hypothesis must also be parsimonious, that is, the simplest statement that explains all of the data. All of these components must be present to make a valid scientific hypothesis, and a hypothesis may be accepted, rejected, or modified, based upon additional data.

1.2  The Anatomy of Scientific Investigation

What does it mean to say that a hypothesis must be falsifiable? We must recognize that whether a hypothesis is right or wrong has nothing to do with it being scientific. In fact, scientific statements are more often proved wrong than right. The hypothesis that the sun revolved around the Earth (geocentrism), and the Earth, therefore, was the center of the known universe, was held as the most logical explanation for the observations at the time, until Galileo gathered more data, in the form of careful measurements and detailed observation, which disproved that idea. Siding with data, rather than the popular ideas, cost Galileo greatly. The hypothesis (the sun revolved around the Earth) was eventually proven wrong, but it was still a scientific statement. An idea that is wrong may be just as scientific as one that is right. An example of an invalid scientific hypothesis is: Some dinosaurs were invisible and weightless. How could you possibly test that hypothesis? Moreover, how would you prove it wrong (falsify it)? Similarly, any statement that contains the words “I believe” is not a scientific hypothesis, because it is not capable of being tested or being falsified. If you “believe” that the Earth is flat, how can I prove your belief wrong? Many things that people assume are science do not follow these rules and are not actually scientific. So, always ask, “what data do you have to support this”? A hypothesis must be testable. How does one test a hypothesis? There are three basic approaches: • Prediction • Experimentation • Literature review (building on data produced by others) Testing by prediction basically means that if your hypothesis is correct, a prediction based upon it will be shown to be true, and therefore supported. The first step to all hypothesis testing is forming a prediction, so if you can’t generate a prediction from your hypothesis, it’s not a valid scientific hypothesis. Let’s look at an example hypothesis: Birds are dinosaurs. This hypothesis posits an evolutionary relationship between birds and dinosaurs like T. rex, in which they share an ancestor in common more recently than either do with any other organism. So if that were correct, what would you predict? Perhaps you would predict that birds and dinosaurs would share specific features that other animals don’t have. You’d then test your prediction by examining the bones of both birds and dinosaurs. Here’s what you find when you do: • Similarities in the way the bones of their “hands” and “wrists” are formed. • Similarities in their skulls and the way the bones of the skull relate to each other. • Unique structures not found in any other lineage but found in both dinosaurs and birds—feathers! Examination of the skeletons showed the features you predicted would be there if birds had evolved from dinosaurs, therefore, this hypothesis is supported by the observations of our test (i.e., data). Take note, however, that supporting a hypothesis is not the same as proving it correct. Hypotheses can either be supported, and thus have an increased likelihood

5

6

CHAPTER 1    How Do We Understand the Natural World?

of being correct, or they can be falsified, and thus be incorrect. Because there’s always the chance that they could someday be falsified when new data come to light, they can’t ever be considered to be proven. Another component of hypothesis testing is experimentation. Many, perhaps most, scientific hypotheses are tested this way. Experimentation represents a potential way to evaluate the accuracy of a prediction we’ve made. In an experiment, researchers design a procedure that manipulates conditions and evaluates the effect that manipulation has on a subject of interest (e.g., a specimen). The changes in features such as temperature, color, or size (i.e., variables) that are measured are the data we use to support or falsify our hypothesis. In the example above, we took observations from bones of living (birds) and fossil (dinosaur) specimens to gather data and determine if our predictions were correct. Although we may have taken measurements of bones and their features, we didn’t manipulate the conditions of these bones and evaluate their response, therefore, we did not experiment on them to test our hypothesis. Here’s an example of a hypothesis that can be tested with experimentation: Compound A is chemically similar to compound B. Here’s a prediction we might make based on our hypothesis: If these compounds are chemically similar, they will both boil at approximately the same temperature. What kind of experiment would you design to test this? Perhaps you would heat both compounds and measure the temperature at which they each reach their boiling point. The activity of heating these compounds and measuring the results is an experiment. The third way to test a hypothesis is through the accumulated literature (i.e., published scientific studies), which can also be considered an appeal to authority. For just about any dinosaur question out there, there is a body of literature we can turn to for data. Not all published literature is equal, however. In science, only peer-reviewed literature, published in recognizable scientific journals, can be used to test a hypothesis. This is because every paper in the peer-reviewed literature has (theoretically) run a gauntlet of reviewers (who are experts in a specific field) that are qualified to objectively evaluate the methods, data, and conclusions of the paper. There are two methods of testing hypotheses from a review of the literature. One is called a meta-analysis, which uses statistical procedures to analyze the results of multiple studies to further support a hypothesis. Let’s say you wanted to further investigate the hypothesis that compound A is chemically similar to compound B. You search and find ten published studies that all tested the boiling points of compounds A and B. Based on these ten studies, you can conduct a statistical analysis on the reported boiling points reported in all ten studies to further support your hypothesis. The other type of hypothesis testing using the literature is called a systematic review. Whereas a meta-analysis relies on a statistical analysis of data from multiple studies, a systematic review synthesizes the results from multiple studies. So for our compound A and B problem, perhaps you search the literature and find ten studies, but not all of them are testing the boiling points. Perhaps these studies tested various other properties such as the melting point, flammability, and elemental composition. Your systematic review would synthesize all the

1.2  The Anatomy of Scientific Investigation

results from these studies to further support or reject the hypothesis that compounds A and B are chemically similar. Now that we know what a hypothesis is, and how we test it, how does it relate to a theory? In science, a theory is one of the strongest statements that can be made. A theory grows out of a hypothesis; when a hypothesis has been tested over and over and over again, in many different ways and aspects, and never been proven false, the likelihood becomes very high that it is correct. A theory then, is a really, really, REALLY well-tested, and incredibly well-supported, hypothesis. No hypothesis is ever proven, but a theory is as close to a proven hypothesis as we can come. A theory, then, can be defined as a thoroughly tested explanation for how or why something occurs in the natural world. As we will see later, the “how” or “why” part of this definition is extremely important. For example, let’s take the theory of evolution put forth by Darwin. Despite almost 200 years of continual testing, the theory of evolution has never been falsified. Further, it is the simplest explanation that also fully accounts for ALL aspects of the diversity of life we observe on this planet (thus parsimonious), including the biological transitions we find in the fossil record, and the shared features we see among phylogenetic groups. Darwin’s theory of evolution by natural selection provides an explanation for how life has continually changed over time. So when a scientist talks about “the theory of evolution”, it means that it has passed all of the tests that have been devised, and has been refined and tested again and again. There is a lot of confusion among the general public about how we use the term “theory”, because in science, it means something different than how we sometimes use it casually in everyday conversation. You may have heard it said, “Evolution is just a theory”. Statements like this imply that a scientific theory is just as valid as any other hypotheses for the origin of life, or the origin of our species. This is simply not correct, because it equates an extremely well-tested and well-supported hypothesis with unsupported, untested, and even invalid hypotheses. The idea that something “is just a theory” implies that there is something more well established beyond a theory. But in science, there is no explanation that is more reliable or rigorous than a scientific theory. Now, perhaps you are thinking “but what about a law!” This is another common misconception—that scientific theories can get further promoted to the status of scientific law. However, theories and laws represent different types of scientific knowledge. Remember that theories are explanations for how or why. Scientific laws answer a completely different question, and that is “what”. Scientific laws are general rules that tell us what will happen under specific conditions. Like theories, they are derived from a hypothesis, established with repeated observation and experimentation, and have never been falsified. An example is Boyle’s law, which tells us that the pressure exerted by a gas is proportional to the volume it occupies. It has an established equation that we can use to predict what the pressure of a gas will be if we change the volume of its container. But it doesn’t tell us why the pressure goes up. As we have seen, hypotheses form the basis for all scientific investigations. Through the process of prediction and experimentation, we can build support for hypotheses, and given enough established evidence they can become theories. But it is important to remember that all hypotheses, and even all scientific knowledge, must be falsifiable. The job of a scientist, then, should be to disprove, not to prove. If we fail to disprove, the hypothesis or theory or law is strengthened. In science, nothing is ever completely proven, and all scientific knowledge

7

8

CHAPTER 1    How Do We Understand the Natural World?

is considered provisional; proving should not be the primary goal of science. Rather, science should also continually seek to disprove, especially to disprove one’s pet ideas. That removes an element of bias. So, if you hear that scientists have “proven” something, think about what it would take to disprove it, and whether or not that is possible to do.

1.3 WHAT IS PALEONTOLOGY? After reading this section you should be able to… • Define paleontology.

Paleontology is the study of ancient life. Although you might think that all paleontologists study dinosaurs, most of them don’t. In fact, they study a range of topics, from the origin of life itself, to fossil plants, to microorganisms, to humans, and all aspects of life in between. Here are a few of the subdisciplines within paleontology: • Microbial paleontologists study the preservation and extent of microbial life in the rock record. • Invertebrate paleontologists study the origin, evolution, and distribution of invertebrates, from worm traces and insects to clams and squid. • Paleobotanists study the origin, evolution, morphology (shape), and distribution of fossil plants, and how they relate to plants living today. • Palynologists study the fossil record of pollens. • Paleoecologists study the interactions between different groups of organisms within a single environment and how they relate to each other. • Paleoclimatologists study the chemistry of ancient atmospheres and ancient climates. They study periods where the Earth was colder or warmer than today, and try to understand ancient influences and trends, and use these data to predict future climates. Many also study how ancient life impacted Earth’s global climate, such as when the expansion of terrestrial plant life some 400 million years ago removed vast amounts of carbon dioxide from the atmosphere, leading to an ice age. • Vertebrate paleontologists study the origin, evolution, distribution, and extinction of vertebrate organisms—those with true bone, and a bony vertebral column. Even among vertebrate paleontologists, there is a wide variety of research subdisciplines. Some study fish and their ancestors; some study amphibians; some study lizards and snakes; some study turtles; some study mammals and their ancestors, the “mammal-like reptiles”; some study humans and their near ancestors; some study crocodiles and their relatives, and some study birds and dinosaurs. Some researchers don’t focus on specific animal groups, but rather biological aspects of extinct creatures across groups. For example, those who specialize in biomechanics study movement and locomotion of ancient organisms, while molecular paleontologists study the preservation and alteration of biomolecules in fossil remains.

1.4  How Does Paleontology Fit into Science?

1.4 HOW DOES PALEONTOLOGY FIT INTO SCIENCE? After reading this section you should be able to… • Classify paleontology as a science and justify this classification.

So, with our new-found terminology, where does paleontology fall as a scientific field of study? Seemingly, paleontology is a life science (biology) as it is concerned with the study of ancient life. But ultimately, paleontology is fundamentally cross-disciplinary. All of the life that paleontologists study is now part of the rock record and geologic time, and using geological principles and understanding the Earth sciences are as critical for paleontologists as knowing biology. Paleontologists must also borrow from and avail themselves of the tools, technologies, methods, and backgrounds of a host of other scientific disciplines. Paleontologists borrow from biology, physics, astronomy, geology, sedimentology, chemistry, computer science, and mathematics, just to name a few. Paleontology is primarily a historical science. Although slightly different from disciplines using experimental methods, historical sciences must still follow the scientific method. Thus, they begin with an observation, which is the basis on which to form a hypothesis. Hypotheses are then tested in historical sciences just as surely as they are in experimental ones, meaning data must be generated. Based on the data, then, a hypothesis is supported, rejected, or modified. Ultimately, predictions are made based upon the hypothesis, and these are then tested. A good example of using prediction to test a hypothesis in the historical science of paleontology is the story of Tiktaalik (Figure 1.3). Scientists who study the origin of tetrapods (tetra = four; pod = foot) from fish-like ancestors made a prediction of what features an animal intermediate between these two states would possess, and, based upon the data from other fossils, predicted when it might have lived. Then, these scientists looked at geological maps to see where rocks of this age were currently exposed on the planet and predicted that this would be the place they might find this key “intermediate”. Then, they organized an expedition to Ellesmere Island in Canada, where the right aged rocks were exposed— rocks that also represented the shallow streams capable of holding such a transitory animal. There, they found a well-preserved, articulated fossil (Figure 1.3A) that exhibited a blend of fish-like features (gill-supporting neck bones, scales, bony fins) and tetrapod-like features (lungs, adaptations of the skull and neck, and a strong pelvic girdle), exactly as had been predicted. As you might guess, paleontological hypotheses about the biology and behavior of dinosaurs are often tested without experimentation, as this is a little more difficult to do given that dinosaurs are, well, dead. If you Figure 1.3  (A) Cast (replica) of Tiktaalik fossil specimen discovered on Ellesmere Island in Nunavut, Canada. (B) Paleoartist reconstruction of what Tiktaalik might have looked like in life. (Courtesy of K. Tiffany. Images

taken at the Field Museum.)

9

10

CHAPTER 1    How Do We Understand the Natural World?

want to determine how fast dinosaurs ran, you can’t line them up and time them with a stopwatch. However, that doesn’t mean experiments aren’t possible in paleontology. For example, a researcher focusing on a particular dinosaurian aspect of biology, such as locomotion, might begin by measuring things like how far a muscle attachment scar is from a joint in a particular species, or the ratio of upper leg bone length to lower leg bone length. Then, she can measure the same feature in living animals, and conduct racing experiments on the animals that are still around to see how these variables affect their speed.

1.5 A BRIEF HISTORY OF DINOSAUR PALEONTOLOGY After reading this section you should be able to… • Briefly outline the history of dinosaur paleontology.

There are far too many investigators who have played, and continue to play, pivotal roles in establishing the science of dinosaur paleontology to cover exhaustively in this text (see the Literature section at the end of this chapter for some great books dealing with the history of dinosaur paleontology). Here we try to introduce some of the primary influencers of the field, both at its beginning and currently. Dinosaur paleontology is expanding rapidly, fueled by curiosity and cultural phenomenon, such as the Jurassic Park franchise. But dinosaurs have captured the attention of society at many points in our history. Dinosaurs have been known from their bones for about as long as there has been human culture to record them, and they form the basis for folklore from ancient China (dragons) to native Americans. But the pull of dinosaurs really began with their first ”official” discovery, in the early 1800s, when William Buckland, a geology professor at Oxford University, realized that the bones, teeth, and limbs he had been asked to describe belonged to its own, “new” creature, and he named it Megalosaurus. Two women in this Victorian age contributed greatly to the early foundations of vertebrate paleontology. Mary Ann Mantell, wife of geologist Gideon Mantell, stumbled upon some bones while walking on a beach in England, and named this creature Iguanodon, because its teeth resembled those of the familiar lizard. Mary Anning who, with her brother, is credited with finding and describing the first ichthyosaur fossils, not far from their home in southern England (Figure 1.4). The Annings were impoverished, and made their living selling their fossil finds. Mary is thought to be the inspiration for the nursery rhyme, “she sells seashells by the seashore”. These women point to something else rather unusual for paleontology, and that is from its first inception, women have been strong contributors to this science, even in Victorian England, and they continue to be. The name “dinosaur” was coined by Sir Richard Owen, a well-known naturalist and comparative anatomist, who later went on to found London’s Natural History Museum. He realized that the fossils belonged to animals that rightly deserved their own category. They were “reptiles”, based upon comparative anatomical details, but they certainly did not closely align with any known at that time. The name dinosaur (deino, a Greek word meaning terrible, powerful, or fearful, and saur, the term for lizard) was certainly appropriate for the group that spanned ~150 million years, encompassing virtually every ecological niche, and filling well over 700 species.

1.5  A Brief History of Dinosaur Paleontology

11

Figure 1.4  Portrait of Mary Anning with her dog at the Golden Cap outcrop, a cliff on the English Channel coast that is rich in ammonite and belemnite fossils. (Unknown artist, public

domain.)

These dinosaur finds coincided with, and gave support to, the then-new theory of evolution proposed by Darwin. In fact, it was a dinosaur (because birds are dinosaurs) that all but cemented this idea in biological thought. The discovery of a small, long-tailed, toothy skeleton in the lithographic limestone quarries of Solnhofen, Germany, was first attributed to this new group, the Dinosauria. It was only with the discovery of a spectacular specimen that was preserved with a full covering of what could only be feathers, that the first “missing link” predicted by Darwin’s theory, was described. It had many “reptilian” features, but the undeniable presence of feathers contributed to its classification as the first bird. By the middle of the 1800s, dinosaur bones had been found and described from all over Europe, but the first presence of dinosaurs in North America were footprints. These “giant bird” tracks were actually the tracks of a small dinosaur. In 1855, however, bones were found by geological surveyors working in Montana, and described by Joseph Leidy, an anatomy professor at the University of Pennsylvania (Figure 1.5). But these isolated bones did not compare with another find of Leidy’s, an almost complete skeleton found in New Jersey, and described in 1858. Although this skeleton had many features in common with the Iguanodon described from England, it was from much younger sediments, and had many features setting it apart. Leidy christened his new find Hadrosaurus. Dinosaur fever was fully exemplified by the Great Bone Wars in the 1870s. The competitors were Edward Drinker Cope (Figure 1.6), a student of Leidy’s in Pennsylvania, and his arch-enemy, Othniel Charles

12

CHAPTER 1    How Do We Understand the Natural World?

Figure 1.5  Portrait of Joseph Leidy.

(Courtesy of Gilbert Studios, public domain.)

Figure 1.6  Portrait of Edward Drinker Cope. (Courtesy of Frederick Gutekunst,

public domain.)

1.5  A Brief History of Dinosaur Paleontology

Marsh (Figure 1.7), a Yale-educated naturalist whose uncle, George Peabody, contributed money to establish the venerable Peabody Museum, which Marsh was dedicated to filling with specimens. Cope is credited with naming over a thousand new species of living and extinct reptiles, including many dinosaurs. These two bitter rivals are responsible for the discovery and descriptions of many of the best known, and best-loved dinosaurs today—the massive Diplodocus, the spiny Stegosaurus, and of course, Triceratops. A new generation of paleontologists followed, many trained by Cope or Marsh, and these explored the vast American West, unearthing a continual stream of massive and unexpected ancient beasts. Barnum Brown, sent out by the then-new American Museum of Natural History in New York City, explored the Late Cretaceous deposits in Canada and Montana (Figure 1.8). He is known for discovering the first documented remains of tyrannosaurus. Charles Sternberg was hired by the Royal Ontario Museum, and charged with finding additional dinosaur skeletons that would stay in Canada (Figure 1.9). Unlike Cope and Marsh, Brown and Sternberg overlapped without animosity, and often worked together to collect and study the dinosaurs they recovered.

Figure 1.7  Portrait of Othniel Charles Marsh, center of the back row, and his field crew. (Photographer unknown,

public domain.)

Figure 1.8  Barnum Brown at a field site in Montana. Brown was often

photographed wearing a fur coat at fossil field sites. (Courtesy of Preston, public domain.)

13

14

CHAPTER 1    How Do We Understand the Natural World? Figure 1.9  Charles Sternberg prepping fossils in a sandstone slab.

(Courtesy of the US National Archives and Records Administration, public domain.)

In the 1920s, dinosaur hunting expanded to parts of Asia. Scientists from Sweden, the United States, and France collected from these new areas, but it was Roy Chapman Andrews, a debonair paleontologist sent out by the American Museum, whose finds captured the imagination of the American public and placed dinosaurs front and center in the collective consciousness of the nation. He went on expeditions hoping to find the origin of humans, but instead found the first dinosaur eggs and nests as well as abundant bones. Andrews, who formed a role model for the character Indiana Jones, reported the first complete nests of dinosaurs, and described the small ceratopsian relative of Triceratops, called, appropriately, Protoceratops. They also found bones from many predatory dinosaurs, including the smaller Saurornithoides, Oviraptor, and the larger Tarbosaurus, a relative of the great Tyrannosaurus. By the 1920s then, dinosaur paleontology was cemented as a discipline, and great finds continued. John Ostrom, also from Yale, became curator of the Peabody Museum well-stocked by Marsh, followed Barnum Brown’s trail to Montana, finding and describing Deinonychus, and suggesting the possibility that birds evolved from this group of small dinosaurs because of many shared features. The 1970s saw a rekindling of interest in dinosaurs, fed by discoveries of a new generation of paleontologists, as well as contributions across disciplines that brought new rigor to this descriptive science. Bob Bakker, a student of Ostrom’s, whose proposal that dinosaurs were not sluggish and slow, but rather active, exhibiting pack hunting and herding behavior—and proposed and popularized the idea that dinosaurs may have been warm-blooded. Jack Horner, a paleontologist from Montana who also spent time working at Princeton before returning home as curator of the Museum of the Rockies, found the first evidence of dinosaur nests in North America, and only the second site (after Roy Chapman Andrew’s sites in Mongolia) to produce dinosaur nests. Jack provided the first evidence that dinosaurs were “good mothers” and named a new dinosaur species (Maiasaura peeblesorum, the “good mother lizard”) based upon this idea. Jack was the scientific advisor for the Jurassic Park movies, and was the role model for its lead character, Alan Grant. Together with Kevin Padian (now at Berkeley) and Armand de Ricqlès (Collège de France, ret), Jack established the field of dinosaur paleohistology, incorporating microscopic studies of dinosaur bone to propose that dinosaurs employed growth rates and physiological strategies approximating those of living mammals and birds.

1.5  A Brief History of Dinosaur Paleontology

Philip Currie also contributed to the great dinosaur renaissance in which we find ourselves. He established the Royal Tyrrell Museum of Paleontology in Drumheller, Canada, and developed Dinosaur Provincial Park, to capitalize on highly productive Late Cretaceous bonebeds, and participated in expanding vertebrate paleontology in China, through the China–Canadian Dinosaur Project, and describing some of the first feathered dinosaurs to be recovered from the famous Liaoning lagerstätten. Mark Norrell, current chair of vertebrate paleontology at the American Museum of Natural History in New York, has been influential in many areas of dinosaur study. In joint expeditions with scientists in Mongolia, Mark has discovered and described many crucial specimens and named many new dinosaur groups. He was part of the team to recover and describe an exquisite oviraptorid brooding its eggs on nest, arms outstretched to protect them. Kay Behrensmeyer, a curator at the National Museum of Natural History (Smithsonian), has conducted a multi-decade study to understand how animals may transition from living animals to fossils, establishing the field of taphonomy. Although her study was focused on mammals, there is no doubt that dinosaurs underwent the same processes as all other animals, and her work contributed greatly to our understanding of how fossils become fossils. Zhou Zhonghe is affiliated with Nanjing University, Institute of Vertebrate Paleontology and Paleoanthropology (IVPP), the Chinese Academy of Science, and the National Academy of Science in the United States. Even though he grew up in a country with some of the most significant and prolific deposits of dinosaurs in the world, he had never seen a fossil until college. He focuses on ancient birds and the evolution of flight but has participated in the discovery and description of some of the most amazing fossils ever found, including Confuciusornis, and the feathered dinosaur Anchiornis. Karen Chin is a paleobotanist, taphonomist, and paleoecologist, who has contributed to our understanding of dinosaur habits and habitats through study of their fossil feces, or coprolites. Kristi Curry Rogers specializes in the study of sauropod dinosaurs, using histology to estimate rapid growth rates in these massive creatures. Cathy Forster has conducted multi-year studies of Mesozoic dinosaurs and birds from Madagascar, and has described many new dinosaurs, including iguanodonts and other ornithopods from China and South Africa, and studies ceratopsian evolution. Too many others to mention continue to contribute to our understanding of dinosaurs. John Hutchinson brings dinosaurs to life through biomechanical studies and modeling; Luis Chiappe primarily studies bird evolution—until he found himself in the middle of the largest sauropod nesting ground ever discovered. Tom Holtz specializes in theropod research but it also a well- known dinosaur communicator, bringing the dinosaurs he loves to non-specialists. Greg Erickson pioneered the study of how dinosaurs grew and produced the first growth curve for T. rex! Paul Sereno has led expeditions into Argentina and Africa in search of the earliest dinosaurs, and described Eoraptor, one of the earliest dinosaurs known, as well as Afrovenator, Nigersaurus, Suchomimus, and many others. The dinosaur revolution continues with a new generation of men and women who dedicate their energies to better understanding our past, so we can prepare for our future. We hope you join them, or at least continue to remain interested in their exciting research!

15

16

CHAPTER 1    How Do We Understand the Natural World?

1.6 WHY STUDY PALEONTOLOGY? After reading this section you should be able to… • Argue for the importance of studying paleontology.

This book is about dinosaurs and how we can study animals no human has ever seen. But, beyond the fact that they make great movie fodder, are they really worth the time, effort, energy, and money we put into them? Many argue that it is a time-consuming and expensive effort that has minimal impact on our present lives. Aren’t there a lot of other research ideas to support that are more important? And since much research is funded through federal research agencies, couldn’t one argue it is a waste of taxpayer dollars? In fact, why study the distant past at all? Why is it important to know about the history of our planet before there were humans? Consider this: as you now know from reading about scientific inquiry, all predictions for the future are based upon the past. If one wants to predict economic trends, one must know those from the past. If one wants to predict climate change, one must understand climate patterns in the past, and what influenced them. We live on a changing planet. From its beginning to the present, all aspects of it are in flux. Temperatures rise and fall. Atmospheric composition changes. Water levels change. Icy glaciers form and retreat; mountains rise up to spectacular heights and erode away. How do we know? The rocks, and the fossils they contain, tell us. If you want to predict the future, you MUST study the past. The very short time span of recorded human history, about 5,000 years, is just not sufficient relative to the 4.5-billion-year history of Earth to make adequate predictions, and more, formulate policy, for the future. The rocks are all we have. If we want to know if the Earth is currently experiencing a human-driven mass extinction event, we have to compare to extinction rates of the geologic past. Evolution and the mechanisms that drive it, climate patterns and adaptation within a lineage to changing environments, are all written in the rocks. In fact, organismal or lineage change is only visible in the rock record—the human life and lineage span is simply too short to observe really long trends. So, to detect the effect humans have on processes and systems that have been occurring since life began, one must study these processes as recorded before there were humans to affect it. Human overprint is only detectable using the rock record. Similarly, trends that affect the human species, such as migratory patterns, environmental or other factors that favor the acquisition of novel traits, or co-evolution of humans and diseases are only capable of being understood in the context of the past. If we want to understand patterns of extinction, either local or global, and how an ecosystem recovers from extinction, we must understand the rocks. This is important, because well over 99% of all species that have ever occupied space on our planet are extinct. Being able to understand the extinction of species in the past, patterns of extinction (i.e., who or what went extinct? Many species or a single one? Slowly, or in a geological “instant”?), and contributing factors will help us anticipate, and perhaps mitigate, these patterns in the future. But, why should we study dinosaurs in particular? Some would argue that paleontological studies are “too expensive” for research on life that’s no longer around, and can it really be all that relevant to our lives and problems today?

1.6  Why Study Paleontology?

Dinosaurs represent the extremes of what is possible for terrestrial vertebrates. We have recovered long-necked sauropod dinosaurs that are estimated to have been the size, and mass, of 14 elephants stacked together when they were alive! That is not much smaller than the massive blue whales, the largest animal on earth. But, without water to contribute buoyancy, how did sauropods move their massive bulk? On the other end of the spectrum, birds are dinosaurs, and thus they also represent some of the smallest of vertebrates, with certain hummingbirds reaching to only about two inches at adulthood. That is a far greater range of variation than is seen in mammals. The fastest dinosaurs, estimated from skeletal, biomechanical, and footprint data, were a group of saurischians theropods called ornithomimids. It is estimated that these dinosaurs could run as fast as 40 miles (60 km) per hour. That isn’t as fast as a cheetah, the world’s fastest animal, who can run about 70 miles per hour. But many dinosaurs could have outrun most mammals. As we will see later, dinosaurs had some amazing adaptations for food processing. No mammal has possessed the extremely efficient dental batteries—rows of teeth stacked upon each other—that contributed to dinosaurs being able to occupy so many niches. Dinosaurs could replace their teeth throughout their lifetimes, making dino dentists unnecessary. Dinosaurs possessed unique, one-way airflow in their lungs, making them extremely efficient at extracting oxygen from their atmosphere, which, as stated above, contained far more CO2 than our does. Many data suggest that oxygen was also much lower than today’s levels, particularly early in the Mesozoic when dinosaurs were rising to ascendancy. Could these efficient oxygen-extracting lungs explain how they got to be so successful and diverse? So, dinosaurs were an amazing group of animals, dominating the terrestrial earth for ~150 million years, or longer, if you count the birds in your backyard. But there are additional reasons to study dinosaurs. One major reason is that because people of all ages are fascinated with these big beasts, they can provide a pathway into science and encourage students to consider STEM disciplines. Learning how to employ the scientific method to study them extends to all other disciplines, and all other disciplines can shed light on some aspects of dinosaur lives. Comparative anatomy sheds light on how dinosaurs are related to today’s life forms—and means that to fully understand dinosaurs we must understand the anatomy and physiology of living vertebrates. To simulate dinosaur movements requires physics, biomechanics, and yes, computers! Computer modeling brings dinosaurs to life! Geology reveals much about where and when they lived, and geochemistry can shed light on aspects of their environment. Histology allows us to compare the microstructure of dinosaur bones with those of living animals and their nearest relatives, allowing us to approximate how fast they grew. Dinosaurs have captured the imagination of old and young, rich and poor, in just about every country. Dinosaurs are the ideal and universal vehicle (a scientific “gateway drug”) for teaching and applying the scientific method, illustrating how science is done, and teaching the value of inference and critical thinking. Dinosaurs reigned the Earth for over 140 million years, and the human lineage, through its earliest human-like ancestors to today, have only been present for about 4 million years—and in our “modern” form, only about 300,000! Therefore, we can study trends and patterns that go well beyond a human life span, or a human “species-span”, by looking at dinosaur evolution. Furthermore, the relationships between dinosaurs and their environments and ecological interactions shed light on patterns between humans and their

17

18

CHAPTER 1    How Do We Understand the Natural World?

environments. Finally, the intense study of dinosaurs involves applying new or developing methodologies in all the tangential disciplines to better understand the life of these big beasts—and in the process, benefiting and expanding all sciences. Besides…dinosaurs are just cool. And sometimes, that is reason enough.

INSTITUTIONAL RESOURCES Understanding Science 101 from the UC Museum of Paleontology of the University of California at Berkeley: https​://un​dsci.​berke​ley.e​du/ar​ticle​/0_0_​0/int​ro_01​

LITERATURE Brinkman, P. D. (2010). The Second Jurassic Dinosaur Rush: Museums and Paleontology in America at the Turn of the Twentieth Century. University of Chicago Press, Chicago.

Rieppel, L. (2019). Assembling the Dinosaur: Fossil Hunters, Tycoons, and the Making of a Spectacle. Harvard University Press, Cambridge, Massachusetts.

Cadbury, D. (2012). The Dinosaur Hunters: A True Story of Scientific Rivalry and the Discovery of the Prehistoric World (Text Only Edition). HarperCollins UK, London.

Shubin, Neil (2008). Your Inner Fish. Vintage Books, New York, NY, p. 237.

2 2

HOW DO WE KNOW WHEN DINOSAURS LIVED? INTERPRETING EARTH’S HISTORY FROM ROCKS

Y

ou are probably familiar with the general structure of our solar system. The sun is the center, and the planets, of varying sizes and compositions, follow well-defined paths around it (Figure 2.1). But the solar system was not always such a nice, friendly, well-organized place. The sun began to form about 4.5 billion years ago, from an interstellar cloud composed of mostly hydrogen and helium that began to collapse upon itself because of gravity. This collapse may have been triggered by the shockwave of a nearby supernova (star explosion). Gravitational interactions between these particles caused them to slowly gain speed until the whole cloud began to rotate. The faster it spun, the more the particles began to collide, sometimes sticking together, or accreting. As some particles gained mass through accretion, their gravitational pull became greater, which in turn pulled more particles to them, forming bodies that gradually increased in size. A majority of the particles (again mostly hydrogen) collected at the center, and eventually, the pressure and density of this body became so great that atoms began to fuse, in the process producing incredible energy. This body would become our sun. The various-sized planets around the early sun (which, in the early days after its formation, probably only reached about 70% of today’s solar temperatures) formed in much the same way, accreting from the leftover dust not swept up by the sun. The condensation of matter out of the interstellar cloud continued under the influence of both the sun’s increasing gravity and the increasing spin of the cloud. To visualize this, think of videos you have seen of figure skaters spinning on the ice. If they want to go faster, they pull their arms and legs inward, forming a tight column. If they want to slow down, they throw their arms out wide, and sometimes lift one leg in a right angle to the one still on the ground. The early solar system was filled with colliding bodies, high heat, and instability—not a friendly place for life to begin! But, as the mass of these accreted particles increased, they acted like vacuums, sucking up all the debris between these new planetoids and keeping the areas between

IN THIS CHAPTER . . . 2.1 A BRAVE NEW WORLD: THE FORMATION OF THE EARTH 2.2 OUR MOVING EARTH: PLANETARY STRUCTURE AND PLATE TECTONICS 2.3 BUILDING BLOCKS OF THE EARTH: ROCK TYPES AND CLASSIFICATION 2.4 SEDIMENTARY ENVIRONMENTS 2.5 ROCK CLOCKS: STRATIGRAPHY 2.6 ROCK CLOCKS: RADIOACTIVE ISOTOPES AND ABSOLUTE DATING 2.7 OUR ROADMAP THROUGH TIME: THE GEOLOGIC TIMESCALE 2.8 WHAT WE DON’T KNOW

20

CHAPTER 2    How Do We Know When Dinosaurs Lived?

Figure 2.1  Image of our solar system with the sun in the center. The

terrestrial planets of Mercury, Venus, Earth, and Mars are in the foreground relative to the sun, while the gas giants Jupiter and Saturn along with the ice giants Uranus and Neptune are in the background. (Courtesy of Harman Smith and Laura Generosa, public domain.)

Figure 2.2  Artist’s rendering of a new solar system forming. This image was

based on a swirling disk spotted by NASA’s Spitzer Space Telescope. It is thought that this disk could produce a few Earth-sized rocky planets. (Courtesy of NASA, https​:// ww​w.nas​a.gov​/mult​imedi​a/ima​gegal​lery/​ image​_feat​ure_3​11.ht​ml.)

them free from debris (Figure 2.2). This process, which resulted in our planetary solar system, occurred over 10 to 100 million years following the sun’s formation.

2.1 A BRAVE NEW WORLD: THE FORMATION OF THE EARTH After reading this section you should be able to… • State the age of the Earth and cite the evidence used to determine its age. • List the two hypothesized sources of Earth’s water and identify the evidence used to support them.

Evidence for how long ago the Earth formed is not easily obtained from Earth itself. The problem is the early period of bombardment resulted in the continual melting and reforming of the surface. Between that and the constant rock cycling that continues today (caused by tectonic activity of the Earth’s crust after it cooled; see Sections 2.2 and 2.3), direct evidence of the very earliest history of our planet has been obliterated. Therefore, we must rely on the study and dating of asteroids in the solar system (which are older than terrestrial rocks), data from moon rocks formed at

2.1  A Brave New World: The Formation of the Earth

the same time as the Earth, but not recycled (because the moon doesn’t undergo tectonic activity like the Earth does), measurements of the sun, and observations of other, distant galaxies that are currently forming to piece together the picture of Earth’s birth. The early Earth was hot, with a lot of areas covered with molten lava, and other areas that had solidified became covered with pockmarks from the near-continual asteroid bombardment. If water would have been present, it would have been instantly vaporized. Life, at least life as we know it, could not have existed in such environments. In fact, the geological period representing this time is called the Hadean, after Hades, Greek for “the land of the dead”. This time period was, quite literally, Hell on Earth (Figure 2.3). However, as the bombardment from outer space slowed, the surface of the planet rapidly cooled. Evidence from the dating of rare zircon crystals suggests that the Earth was cool enough to form continental rocks as early as 4.4 billion years ago, just 100 million years after the gigantic collision that led to the formation of our Moon. For life to get started, the surface of the planet had to cool enough to allow water to exist in liquid form, because liquid water is absolutely necessary for the chemical reactions of life to occur. If there was no water on Earth after its initial formation, where did the first liquid water come from? Scientists hypothesize that there were two sources of water for the earliest oceans: (1) water vapor arising from outgassing of volcanoes from the very active planetary core and (2) from occasional collisions with carbon-rich meteorites or icy comets that contained water. But how can we possibly know any of this? There are several lines of evidence that show us this is how our solar system and Earth came to be. • We can observe this process happening elsewhere: With powerful telescopes capable of reaching far into space, we can see other solar systems “being born” right before our eyes (see Figure 2.2). These all follow a pattern that is dependent upon, in part, the mass of the “sun” around which the forming planets orbit. It is reasonable to conclude, until data show otherwise, that our own system arose in a similar manner.

Figure 2.3  Artist’s rendering of what the early Earth may have looked like shortly after formation, a period known as the Hadean Period. (Public

domain.)

21

22

CHAPTER 2    How Do We Know When Dinosaurs Lived?

• There are pieces of the dust cloud still around for us to observe: We can study the remnants of the original interstellar dust cloud, which persist as asteroids and other small bodies not big enough to form planets. We have analyzed the chemical composition of such rocky meteors and asteroids and compared them with rocks both on the moon (brought back by astronauts on the Apollo missions) and on Earth. These bodies provide evidence about both the age and early formation of Earth. • We can examine the rocks on our planet: The Earth’s estimated age is 4.54 billion years (only 400–500 million years after the beginning of the cloud’s collapse). The oldest rocks on Earth date to about 3.8 billion years while the oldest minerals are 4.4 billion years old (minerals are the building blocks of rocks, see Section 2.3). The chemical make-up of these ancient rocks and minerals tells us about Earth’s early atmosphere and geology. We can also use radiometric isotopes to calculate the absolute age of the earth (see Section 2.6). • We can observe interstellar collisions occurring and the markings of past ones: We can see collisions between interstellar bodies going on within and beyond our solar system. Additionally, because the moon has no tectonic activity to recycle its rocks, nor an atmosphere to weather away the surface rocks with wind and rain, we can still observe the scars left from these collisions on the surface of the moon. In some cases, we can even study evidence of more recent collisions on our own planet; impact craters, including ones in South Africa, Mexico, Canada, and the United States, provide geological evidence of these events. Such events have also happened within recorded history. For example, we know that earth sustained an impact with an extraterrestrial body in Siberia in the early 20th century (called the Tunguska event). This leveled trees for miles, and was heard, seen, and photographed by many (Figure 2.4). • We can study current volcanoes and meteorites found on Earth: Volcanic eruptions still happen today, though not as frequently as on the early Earth, and modern eruption events have been shown to release large amounts of water vapor in addition to other gasses. Additionally, meteorites found on Earth that are 4.6 billion years old have been shown to contain water with a similar isotopic composition to Earth. These observations provide evidence for how water may have originated on the early Earth. • We can use computer modeling to simulate these events: Using laws of physics that relate mass and gravity, computers can calculate Figure 2.4  Archival photograph showing downed trees resulting from the Tunguska impact. (Courtesy of CYD,

public domain.)

2.2  Our Moving Earth: Planetary Structure and Plate Tectonics

how particles within an interstellar cloud would behave, further supporting the theory of our solar system’s formation.

2.2 OUR MOVING EARTH: PLANETARY STRUCTURE AND PLATE TECTONICS After reading this section you should be able to… • Make a labeled sketch to show the relationship of the Earth’s crust, mantle, and core. • Describe the relative motions of tectonic plates at the three major types of plate boundary. • Summarize the evidence that was critical to building the theory of plate tectonics from the continental drift hypothesis. • Propose two reasons why understanding plate tectonics is relevant to the study of dinosaurs.

It isn’t just the first formation of the planet that shapes what we see today—it is the chemical and physical structure of the planet itself. As the planet grew larger during its formation, the interior began to heat up and melt, resulting in clear chemical differentiation throughout the planet’s interior, in both density and chemical makeup. The heaviest materials, primarily metallic iron and nickel, sank all the way to the center, forming Earth’s core. As the Earth began its slow cooling process after formation, the metallic core began to solidify, creating a solid inner core and liquid outer core. The lightest materials, largely oxygen and silicon, rose toward the surface, eventually forming a rocky crust. In between the dense metallic core and outer crust is an “intermediate zone”, composed primarily of oxygen, magnesium, and silicon bearing rock, known as the mantle. This layer is the thickest and accounts for 84% of Earth’s volume. Although the pressure of the Earth keeps the mantle solid, over geologic time it behaves like a liquid or “gooey” rock (Figure 2.5). We can’t bore a hole straight through the Earth, so how do we know about its interior layers? Our knowledge of the Earth’s interior comes from measuring the travel time of seismic waves generated by earthquakes. Just as light will refract through a prism or reflect off a mirror, seismic waves traveling through the Earth refract and reflect as they encounter materials with different properties, for example, solid versus liquid (Figure 2.6). The time it takes different waves to reach various

Figure 2.5  Diagram illustrating the internal layers of the Earth. (Courtesy

of USGS, public domain.)

23

24

CHAPTER 2    How Do We Know When Dinosaurs Lived?

Figure 2.6  Image showing how earthquake waves travel through the Earth. The travel times of these waves

give scientists clues as to the properties of the layers that make up the Earth. (Courtesy of USGS and Vanessa Ezekowitz, https://commons.wikimedia.org/wiki/ File:Earthquake_wave_shadow_zone.svg.)

points gives us insight into the properties of the layers they are passing through and allows scientists to reconstruct an accurate model of the Earth’s interior. The Earth has cooled considerably since its formation, but it still has plenty of internal heat today. This heat comes from two primary sources, residual heat from its formation and heat generated by the decay of radioactive elements in its mantle and crust (for more on radioactivity, see Section 2.6). This heat is dissipated via convection in both the solid mantle and the liquid outer core. Convection within the metallic, liquid outer core, coupled with Earth’s rotation, is responsible for creating the Earth’s magnetic field. This magnetic field protects the Earth from charged solar winds that would otherwise strip away our atmosphere, making Earth uninhabitable. Heat from the core is also transferred to the mantle, where solid rock behaves plastically or like a gooey fluid and this has a profound effect on Earth’s geology. Because the core is hot, the deepest part of the mantle, closest to the core, is also hot. Because heated fluids are (usually) less dense than identical fluids at colder temperatures, the heated part of the mantle rises toward the surface, and cooler parts of the mantle sink to take its place. However, once the hot rocks reach the upper part of the mantle where it is cooler, they begin to cool as well, until they are dense enough to sink back down and make way for rising rocks that were more recently heated by the core. Think of the Earth’s mantle as a giant lava lamp (Figure 2.7)! This cyclical, conveyor belt of plastic rocks between the core and just below the crust is called a convection current, and they have been active since the planet formed. These convection currents (and gravity, see below) are responsible for the Earth’s continually changing surface. They rearrange the oceans and move the continents in a process called plate tectonics.

2.2  Our Moving Earth: Planetary Structure and Plate Tectonics Figure 2.7  A lava lamp is a good analog for convection in the Earth’s mantle. (Courtesy of Novemberchild,

https://commons.wikimedia.org/wiki/ File:1990s_Mathmos_Astro.jpg.)

Plate tectonics causes mountains to form, seas to open, and volcanoes to rise. These events, in turn, have had major effects on global temperatures, ocean currents, and atmospheric composition. Those things, in turn, affect the course, distribution, and direction of life. Thus, understanding plate tectonics is crucial for understanding the history of life on this planet. But what is plate tectonics? The Earth’s crust is not a whole, unbroken shell like you’d find on an M&M candy. Rather, it is like the M&M at the bottom of the bag, with a shell that’s broken into pieces. Each piece we call a tectonic plate. The convection currents described above, coupled with gravity, move these plates around on the surface of the Earth, crashing them together, pulling them apart, and sliding them past each other. Figure 2.8 is a map of Earth’s tectonic plates. Tectonic plates are composed of the crust as well as the uppermost part of the mantle, which is rigid like the crust. This combination of crust and mantle is known as the lithosphere. Tectonic plates can be made up of continental crust, oceanic crust, or a combination of both. Overall, the rocks that make up continental crust are of a lower density than those of oceanic crust. This density difference between the two crustal types has implications for how tectonic plates interact, as we will see below. Tectonic plates interact with each other in three ways, at what are known as tectonic boundaries: • Convergent boundary: Where two plates move toward each other or collide

25

26

CHAPTER 2    How Do We Know When Dinosaurs Lived? Figure 2.8  Map showing the tectonic plates of Earth as well as relative motions at some of the plate boundaries. (Courtesy of USGS and Scott

Nash, public domain.)

• Divergent boundary: Where two plates move away from each other • Transform boundary: Created by plates sliding laterally past one another To complicate matters further, there are three different types of convergence depending on the type of crust composing each plate at the converging edge: • Oceanic–Oceanic: Two oceanic plates converge • Continental–Continental: Two continental plates converge • Continental–Oceanic: A continental plate converges with an oceanic plate Each type of tectonic boundary results in different, recognizable features. Here is a description of each boundary type and associated features: • Divergent boundary (Figure 2.9): When two plates of oceanic crust move apart, mantle rock from below moves upward to fill the gap, making elevated ridges on the ocean floor, called a mid-ocean ridge. As the mantle rock moves upward toward the surface, it experiences decreasing pressure which causes it to melt and form

Figure 2.9  Cross-section showing major boundary types and their associated features. (Courtesy of Jose F.

Virgil, USGS, https://commons.wikimedia. org/wiki/File:Tectonic_plate_boundaries. png.)

2.2  Our Moving Earth: Planetary Structure and Plate Tectonics

magma. As the magma continues to move upward, it eventually cools near or at the surface to form new oceanic crust. This occurs in the center of the ridge at a rift; a narrow trough that represents where the rifting is occurring. Gravitational forces “pulling down” the ridges on either side of the divergent boundary, a process known as ridge push, contributes to pushing the plates apart. Underwater volcanoes and earthquakes are abundant at oceanic divergent boundaries. • Continental rifting: Sometimes convective forces in the mantle can stretch and eventually rift continental crust apart. This process leads to the formation of a continental rift valley, and eventually a new plate boundary and an ocean basin form. This process is currently occurring in the East African Rift valley and the Red Sea which represents the beginnings of a new ocean (Figure 2.10)! • Oceanic–Oceanic convergent boundary (Figure 2.11): When two plates of oceanic crust collide, one plate subducts, or moves underneath the other one. The subducting plate sinks into the mantle for great depths, and the gravitational forces known as slab pull that drag these subducting plates into the mantle are the primary driving force behind plate tectonics. Think of a rug sliding off the edge of the table, where the part hanging off the table pulls the rest of the rug with it. Subducting plates around Earth’s surface are continually pulling plates behind them as new plate material is being formed at divergent boundaries. Additionally, as

Figure 2.10  Image depicting the present-day location of rifting in eastern Africa. The Red Sea is the

beginnings of a new ocean, and the African Plate will eventually rift into the Nubian and Somalian plates which will be separated by an ocean. (Courtesy of USGS, public domain, https://commons.wikimedia.org/ wiki/File:EAfrica.png

Figure 2.11  Oceanic–Oceanic convergent boundary. (Courtesy

of Tectonics is Cool, https://commons. wikimedia.org/wiki/File:Simplified_ convergent_boundaries.jpg.)

27

28

CHAPTER 2    How Do We Know When Dinosaurs Lived?

the subducting plate moves down into the mantle, friction and pressure cause water incorporated in the minerals of the rocks to be superheated and released. This superheated water causes the surrounding rock to melt, creating magma (liquid rock) that rises through the overriding plate because of its lower density. When this rising magma reaches the surface, it forms volcanoes on the overriding oceanic plate and can eventually form island arcs. The Aleutian Islands in Alaska and the islands of Japan are examples of island arcs that formed at an oceanic–oceanic convergent boundary. Subduction also produces one feature never seen at divergent boundaries: a deep oceanic trench. The Mariana trench is formed by such convergence and is the deepest spot in the Earth’s oceans. • Continental–Oceanic convergent boundary (Figure 2.12): When an oceanic plate collides with a continental plate, the oceanic plate always subducts under the continental crust. This is because continental crust is composed of less dense rock than the oceanic crust. As with oceanic–oceanic convergent boundaries, a trench also forms at the zone of subduction, and rising magma from the release of superheated water causes the formation of volcanoes on the overriding continental plate. Volcanoes in the pacific northwest of the United States, such as Mt. Saint Helens and Mt. Rainier, are the result of an ocean plate subducting under the continental United States. • Continental–Continental convergent boundary (Figure 2.13): When the oceanic crust of a plate is completely subducted, it may lead to the collision of two continental plates. When two continental plates collide, think of it like two identical cars crashing together in a head-on collision—the continental plates, like the hoods of the cars, buckle and push up. Because both continental plates are made up of rocks of similar density, neither plate subducts. Rather, the collision causes both plates to be pushed up, and results in extensive folding and faulting (breaking) of the crust. Because there is no longer a subducting plate releasing water and causing melting, volcanic activity in these collisions zones ceases— but strong earthquakes result. Continental collisions result in the suturing of tectonic plates. Spectacular mountain ranges result from this type of collision; some of the highest mountains on the planet formed this way. The Himalayas and Mount Everest arose from the slow collision of continental plates, and the Appalachian Mountains are the result of the North American continent colliding with the African continent over 260 million years ago.

Figure 2.12  Oceanic–Continental convergent boundary. (Courtesy

of Tectonics is Cool, https://commons. wikimedia.org/wiki/File:Simplified_ convergent_boundaries.jpg.)

2.2  Our Moving Earth: Planetary Structure and Plate Tectonics Figure 2.13  Continental–Continental convergent boundary. (Courtesy of

Nefronus, https://commons.wikimedia.org/ wiki/File:Cont​inent​al-co​ntine​ntal_​conve​ rgenc​e_en.​svg.)​

• Transform boundary (Figure 2.9): Convergent and divergent plate boundaries are linked by transform boundaries. These are areas where the edges of two tectonic plates are moving laterally past one another. Since there is no pulling apart or subduction occurring, transform boundaries do not have volcanic activity. However, the sliding of one plate past another causes a great deal of friction, which results in lots of earthquakes. The San Andreas Fault in southern California is a famous example of a transform boundary, where the Pacific plate is sliding past the North American plate (Figure 2.14). So how do we know the continents move if it happens too slowly to see it? What is the evidence for this constant geographic flux? Our understanding of plate motions and the theory of plate tectonics relies on multiple independent lines of evidence. Tracing the evidence for plate tectonics provides a nice example of how a hypothesis can be slowly revised as new evidence and testing leads to a robust theory that explains the workings of the natural world.

2.2.1 Coastline Matching In 1912, a German scientist named Alfred Wegener proposed a hypothesis that he called “continental drift”, in which the Earth’s continents were slowly moving across the surface of the Earth. One line of evidence he used to support his hypothesis was the uncannily complementary

Figure 2.14  Aerial photograph of the San Andreas Fault. The river in the

photograph has been laterally offset by movement along the fault. (Courtesy of Doc Searls, https​://ww​w.fli​ckr.c​om/ph​otos/​docse​ arls/​15392​616.)

29

30

CHAPTER 2    How Do We Know When Dinosaurs Lived?

coastlines on either side of the Atlantic. The shape of the continents is reminiscent of puzzle pieces; the east coast of North and South America would fit together very well with the west coast of Europe and Africa, if we could just push them across the oceans that separate them.

2.2.2 Distribution of Rock Types and Ancient Life Recorded in the Fossil Record Isolation of populations drives evolutionary change and differentiation. Continents today are separated by oceans, making interchange between populations from one continent to another almost impossible. But Wegener realized that some fossils of organisms from the eastern coasts of North and South America during the Triassic (~200–250 million years ago) are very similar, if not identical to fossils found on the western coasts of Africa from deposits of the same time period. This indicates these populations were not isolated from each other but were able to interbreed as one population. These patterns only make sense if the continents were joined in the past. Otherwise, these two populations would have had to swim the entirety of the Atlantic regularly. Wegener also noted the presence of rocks and sediments indicative of glaciation on parts of continents that are today very near the equator, evidence that the continents must have been in different locations in the geologic past.

2.2.3 Mid-Ocean Ridges Wegener’s hypothesis was not well accepted by the scientific community, largely because he could not provide a mechanism for how the continents moved through the oceanic crust. However, in the 1950s, scientists began extensively mapping the ocean floor, and in the process discovered the Mid-Atlantic Ridge, a long underwater feature that runs the entire length of the Atlantic Ocean (Figure 2.15). It was proposed that this ridge was the site of seafloor spreading, where new oceanic crust was being made, and that the ocean crust was moving along the surface of the Earth as well. Similar ridges were mapped in all of the world’s ocean basins

Figure 2.15  Elevation map showing the Mid-Atlantic Ridge, which is the light blue feature that runs down the center of the dark blue Atlantic Ocean. (Courtesy of NOAA, public domain,

https://commons.wikimedia.org/wiki/ File:Atlantic_bathymetry.jpg.)

2.2  Our Moving Earth: Planetary Structure and Plate Tectonics

2.2.4 Paleomagnetism Some rocks incorporate magnetic minerals whose crystals align with the direction of the Earth’s magnetic field at the time the rocks solidified, much like many tiny arrows on a compass, all pointing the same direction. So, even though the east coast of the United States is, today, far removed from the west coasts of Africa and Europe, the little magnetic compasses frozen in these rocks show the same direction of the magnetic field that they would if they were part of the same rock. Furthermore, these magnetic minerals align with the magnetic north pole at the time the rocks solidified. The data show that either the magnetic north moved, or the continents moved, and because the magnetic field is determined by the movement of the Earth’s metallic liquid core, it is far more likely that the continental plates moved, relative to one another. Additionally, Earth’s magnetic north and south poles switch (north becomes south and south becomes north) at random time intervals ranging from about 0.1 to 1 million years over Earth’s history. These reversals of magnetism are recorded in the rocks as magnetic anomalies, and such data helped to spur the idea of seafloor spreading. By using a magnetometer, scientists could detect the magnetic anomalies locked into the rocks of the Atlantic Ocean, which created a pattern of magnetic stripes when mapped. They noticed that these stripes occurred symmetrically on either side of the Mid-Atlantic Ridge between the continents (Figure 2.16), evidence that new seafloor was being created and moving away from the ridge on both sides.

2.2.5 Seismic and Volcanic Activity Is Concentrated along “Plate Boundaries” It is not a coincidence that you’re much more likely to feel an earthquake in California than Illinois. When the origin of earthquakes we detect are mapped to their geographical source, we see that they do not occur randomly, but are concentrated along the boundaries where plates are moving toward, apart, or against one another (Figure 2.17). It was also the mapping of earthquakes that led to the discovery of subduction zones. In certain earthquake-prone areas, the point of origin of these earthquakes was seen to increase in depth along a slanting profile that points down into the mantle (Figure 2.18). These zones provided the evidence for subduction and the recycling of crustal material that was needed to balance the creation of new crust at the mid-ocean ridges. Like earthquakes, mapping of volcanic activity worldwide produces a similar pattern concentrated at the tectonic boundaries.

Figure 2.16  As new seafloor is created at mid-ocean ridges, minerals in seafloor rocks record the Earth’s current polarity at the time of cooling. Reversals in polarity over geologic

time are recorded as magnetic anomaly stripes in the seafloor that can be detected with a magnetometer. (Courtesy of CHMEE2, public domain, https://commons. wikimedia.org/wiki/File:Ocea​nic.S​tripe​.Magn​ etic.​Anoma​lies.​Schem​e.svg​.)

31

32

CHAPTER 2    How Do We Know When Dinosaurs Lived? Figure 2.17  Map of earthquake epicenters from 1963–1998. Tectonic

plate boundaries can be inferred based on earthquake activity. (Courtesy of NASA, DTAM project team, public domain.)

Figure 2.18  The plot of earthquakes in a Wadati–Benioff zone follows the path of a subducting tectonic plate.

(courtesy of USGS, public domain)

2.2.6 Global Positioning System Today, scientists can use the Global Positioning System (GPS), which uses signals from satellites orbiting the Earth to accurately measure the direction and rate of plate movements. With these data, the direction and rates of plate motions are more precise, and we can measure the movement of plates which ranges anywhere from 2 centimeters per year, all the way up to 15 centimeters per year at the East Pacific Rise, the Pacific Ocean’s divergent spreading center. On average, plates move at about the same rate that human fingernails grow! All of this evidence was used to build the theory of plate tectonics in the mid-1960s, at last producing a mechanism to support the hypothesis of continental drift. The theory of plate tectonics would revolutionize the field of geology in the decades to follow. It is predictive and explains most of the geologic processes and features that we observe on Earth today. But why do we need to know these things about the Earth to fully understand the lives of the great beasts that are the focus of our studies? Dinosaurs originated when all of Earth’s continents were just beginning to break apart from a giant supercontinent called Pangea. Indeed, this break-up may have favored their emergence as the dominant terrestrial vertebrates. When there was only one giant landmass, it would have greatly influenced global climate by directing ocean currents, wind patterns, and precipitation. The very dry interior of this giant superconti-

2.2  Our Moving Earth: Planetary Structure and Plate Tectonics

nent (think current Australian climate, only larger scale) may have given the earliest dinosaurs, who laid hard-shelled eggs and were free from dependence on water for reproduction, an advantage over the amphibians with which they shared the planet. The first cracks in the supercontinent came in the Late Triassic (205 million years ago), when Laurasia (the northern part of the landmass) began to split from the southern region, Gondwana (Figure 2.19. At first, the only observable effect of this split would have been the beginnings of a small, shallow sea. This would allow the massive long-necked sauropods, whose fossils we find in rocks from this time period, to move freely between Asia and North America, but would have isolated them from populations of other large sauropods living in Gondwana. Later, as the Atlantic Ocean grew and deepened, even this small passageway was closed. The ancestors of the tank-like Ceratopsians or the duck-billed Hadrosaurs were more restricted in their movements, and their fossils reflect this. In Jurassic sediments, there isn’t much difference in the appearance of groups of dinosaurs. But in the later Cretaceous, when the separation between landmasses was virtually complete (Figure 2.20), Russian dinosaurs look very different from those in Montana and Wyoming, which look different still from those found in Cretaceous Argentina. Dinosaurs saw more global change as a lineage, by far, than any changes we humans will ever experience. The changing continents shaped dinosaur evolution and understanding the distribution of the continents gives us insight into how and why dinosaurs emerged and were so successful. This, in turn, can help us to better predict the effects of these changing dynamics on our own future.

Figure 2.19  Paleomap showing the arrangement of continents during the Late Triassic Period 201.6 million years ago. You can see Pangea beginning to rift

apart and the very early Atlantic Ocean forming between North America and Africa and Europe. (Reprinted with permission from Chris Scotese.)

Figure 2.20  Paleomap showing the arrangement of continents during the Late Cretaceous Period 73.8 million years ago. (Reprinted with permission

from Chris Scotese.)

33

34

CHAPTER 2    How Do We Know When Dinosaurs Lived?

2.3 BUILDING BLOCKS OF THE EARTH: ROCK TYPES AND CLASSIFICATION After reading this section you should be able to… • Describe the relationship between rocks and minerals. • Define the three major rock types and sketch a diagram to summarize their relationship (i.e., the rock cycle).

Although dinosaurs were once alive, and thus part of the biosphere (the zone of life on earth), they are now part of the geosphere, or rock record. Because their skeletons are found in specific rock formations, to answer the question of when dinosaurs lived (and where to look for them), a basic understanding of geology and sedimentology is needed. The Earth’s crust, where the remains of all extinct dinosaurs now reside, is made up of rocks. These rocks are made up of a variety of minerals. Therefore, to understand the story of a rock, a basic understanding of its mineral composition is required. Minerals have five essential characteristics: 1. Minerals are naturally occurring. That is, they are formed from natural geological processes. 2. Minerals are inorganic. They do not derive from living matter. Substances like coal, which is made from compressed/carbonized plant matter, cannot be a mineral. 3. Minerals are solid. There are no liquid minerals. Once a mineral melts, it is no longer considered a mineral, but magma or lava. 4. Minerals have a crystalline structure. All atoms in a mineral are internally ordered in a structured, repeating pattern. This pattern confers certain properties to the mineral and is diagnostic. 5. Minerals have a definite chemical composition. The chemical composition of a given mineral is consistent across all samples. For example, all quartz have atoms that are composed of one silica atom and two oxygen atoms (SiO2). Although there can be some very small variations (usually inclusions that give minerals a variety of colors, like amethyst, rose quartz, and smoky quartz), the main composition is consistent. Sapphires and rubies, for example, are the same mineral (corundum), with the same structure, but are colored differently because of the metal each incorporates. Minerals combine to form the rocks that make up our planet. All rocks fall into one of three categories: 1. Igneous rocks, which are formed from the cooling and solidification of magma or lava. 2. Metamorphic rocks, which have undergone physical or chemical changes due to experiencing high heat and pressure. 3. Sedimentary rocks, which are rocks formed by deposition and cementation of minerals or rock particles. Igneous rock forms from liquid magma or lava that has cooled and solidified, and we categorize igneous rock by the rate at which it cooled, which is related to where it cooled. Magma is liquid rock that is beneath the surface of the Earth. If it solidifies while it is still underground, where temperatures and pressures are higher, it cools slowly, and the minerals

2.3  Building Blocks of the Earth: Rock Types and Classification

that compose it form solid crystals that are visible to the naked eye, as in granite (Figure 2.21). This solidification process can take thousands to millions of years, and the longer the rock takes to cool, the more time these crystals have to form and the larger they are. Thus, the crystal size of igneous rocks is directly related to their speed of formation. Conversely, lava is liquid rock that has extruded onto Earth’s surface. Because the surface of the Earth is much cooler than its interior, lava cools and solidifies much more rapidly than magma, and the crystals it forms are tiny (Figure 2.21). In fact, some of the lava that is ejected from a volcanic explosion cools so quickly, it forms a glass rock (obsidian) that has no crystal growth (Figure 2.22). Generally, when you find an igneous rock, crystal size is a good indicator of the speed of solidification, and therefore where the cooling took place. We call rocks that cooled slowly from magma inside the Earth intrusive (or plutonic) igneous rocks, and those that cooled quickly from lava on the Earth’s exterior extrusive (or volcanic) igneous rocks (Figure 2.23). • Big crystals = slow cooling = solidified inside the Earth = intrusive igneous rock • Small crystals (or none visible) = rapid cooling = solidified at the Earth’s surface = extrusive igneous rock As you have probably guessed, fossils are not found in either type of igneous rock. If a dinosaur were to fall into a river of lava, or get trapped in a volcanic eruption, its remains would be destroyed by the high heat, leaving no trace. Metamorphic rocks form through the application of intense heat and/ or pressure on pre-existing rock. As you read previously, continental Figure 2.21  Granite on the left is a coarse-grained, intrusive igneous rock, and rhyolite on the right is a fine-grained, extrusive igneous rock.

(Courtesy of D. Czajka.)

Figure 2.22  Obsidian, or volcanic glass, is an extrusive igneous rock that cools so quickly it has no crystal growth. (Courtesy of D. Czajka.)

35

36

CHAPTER 2    How Do We Know When Dinosaurs Lived? Figure 2.23  Diagram illustrating the difference between extrusive (volcanic) and intrusive (plutonic) igneous rocks. (Courtesy of Jim

Houghton, https​://up​load.​wikim​edia.​org/ w​ikipe​dia/c​ommon​s/9/9​c/Int​rusiv​e-Ext​rusiv​ e_Ign​eous_​Featu​res.p​df.)

plate interactions cause parts of the Earth’s crust to be subducted. As this rock is pushed deep underground, where temperatures and pressures are higher, this increased heat and pressure can cause the rock to change its texture and composition. The heat is not great enough to make the rocks fully melt and become magma again, but they instead become more or less plastic, and the grains within the rocks become stretched and folded into various patterns. For example, when a piece of granite undergoes metamorphosis, the grains are still visible and largely made up of the same minerals, but they are re-organized, often aligning perpendicular to the direction of pressure resulting in a feature called foliation (Figure 2.24). Fossils can be found in weakly metamorphosed rock, but they are stretched and distorted, discolored, and changed so that much of the original information is usually lost. Sedimentary rock is rock that has been formed from the deposition of pre-existing rock, which has been broken down into sediment, and then compacted and cemented into new rock. Clastic sedimentary rocks are rocks that were formed by mechanical (physical) weathering and deposition. At the Earth’s surface, pre-existing rocks (of any of the three kinds), undergo abrasion by wind or flowing water, freeze/thaw cycles, and other processes that break the rock down (much like using an emery board on your fingernail) into smaller particles called clasts. Although the rock is broken into smaller pieces, the chemical composition of these clasts doesn’t change. For comparison, think about sanding a piece of wood; the sawdust you create is still wood, chemically and in every other way, just smaller. The clasts resulting from these weathering processes are then moved (eroded) by some erosional force (e.g., wind, water, gravity) and deposited elsewhere as sediment. Over time, as the layers of weathered rock particles accumulate on top of each other, increasing the pressure

Figure 2.24  Gneiss, on the left, is formed from the metamorphism of rocks like granite, pictured on the right. You can see the foliation, or

alignment, of the mineral grains in the gneiss compared with the granite. (Courtesy of D. Czajka.)

2.3  Building Blocks of the Earth: Rock Types and Classification

on the sediments at the bottom, the clasts are compacted. Compaction squeezes water out of the sediments that was trapped during deposition and leaves behind minerals that cement the clasts together (in a process called lithification). The end result is a clastic sedimentary rock. We classify clastic sedimentary rock by the size of the clasts composing them. Table 2.1 lists the various size clasts and the associated sedimentary rocks that they make up. As you can imagine, the larger the particles surrounding the bones of dinosaurs, the more likely it is that the bones will be crushed. Additionally, the larger the particles, the more energy it takes to move (erode) them, making it even more likely that bones will be pulverized. A dinosaur carcass that is being transported with or buried by a river carrying large gravel and boulders will be quite battered and destroyed. So, if recognizable pieces of dinosaur bones are what you hope to find, you will start your search in deposits of fine sandstone, siltstone, or mudstone (clays). The second type of sedimentary rock is chemical sedimentary rock. These sedimentary rocks are formed when mineral elements are precipitated (chemically deposited) out of a solution to form the sedimentary rock. Halite, or rock salt, is a chemical sedimentary rock that forms when salty seas or lakes evaporate, leaving behind sodium chloride crystals that make up halite. Because they are chemically precipitated, unlike clastic sedimentary rocks, there are no visible clasts/particles/grains in chemical sedimentary rocks. If living organisms were involved in the precipitation of these compounds, we call these biochemical sedimentary rocks. Many marine organisms (including microscopic ones) precipitate calcium carbonate out of the seawater to make their shells. As these organisms die and their shells or skeletal fragments accumulate on the ocean floor, they can form limestone, a biochemical sedimentary rock (Figure 2.25). As you can probably tell from the above discussion, rocks aren’t static. They can be formed, they can be changed from one kind to another, and

TABLE 2.1 CLAST SIZES AND COMMON ASSOCIATED SEDIMENTARY ROCKS Clast Name

Clast Size

Sedimentary Rock Name

Clay

Smaller than 3.9 µm

Mudstone or shale

Silt

3.9 to 62.5 µm

Siltstone

Sand

0.0625 to 1 mm

Sandstone

Gravel to boulders

1 mm or larger

Conglomerate or breccia

A micrometer (µm) is one-thousandth of a millimeter (mm).

Figure 2.25  Fossiliferous limestone.

(Courtesy of D. Czajka.)

37

38

CHAPTER 2    How Do We Know When Dinosaurs Lived?

Figure 2.26  Diagram illustrating the rock cycle. (Courtesy of Rachel Atkins.)

they can be destroyed. This rock cycle (Figure 2.26) can have a big effect on the history of life on this planet and can tell us a lot about the history of our planet. Volcanoes (igneous rock) affect climate and atmospheres, and even the pH of local waters; sedimentary rock tells us about local environments—mudstones indicate low energy environments, while conglomerates show very high-energy waters; and metamorphic rocks tell us about mountain building events, or tectonic movements, all of which affect life. What affects the rock affects the fossils entombed within them. To understand life, we must understand what has happened to the rock. As different animals today live and die in various sedimentary environments, different kinds of fossils are found in different kinds of sedimentary rocks. Most of the interior of the Earth’s crust is made of intrusive igneous rock, but most (~75%) of the earth’s surface is sedimentary rock. This is good for dinosaur hunters, as sedimentary rock is where we find dinosaur bones!

2.4 SEDIMENTARY ENVIRONMENTS After reading this section you should be able to… • Give examples of different types of sedimentary environments.

2.4  Sedimentary Environments

Understanding sedimentary rocks is important because they can tell us about the environment in which they were deposited (their depositional environment). For example, the further grains of sediment are transported from their source, the smaller and more rounded they become. That is why you see more jagged, bigger rocks in high mountains streams, but only muddy, silty bottoms on low-lying lakes and deltas. The closer rocks are to where they eroded from, the larger and more angular they stay. Thus, by looking at the size and angularity of the grains surrounding dinosaur bone, we can tell a lot about where the animal was living— or at least, where it was buried. Sedimentary rocks can form in marine (ocean) environments, and we can identify three different types of environments that represent ancient oceans. Ocean shores are high energy, and the waves can move big grains, represented by coarse sands and gravels. Shallow ocean areas like continental shelves, where marine life is abundant, are represented by limestones formed from the remains of marine organisms. Further out in the ocean, away from the waves in areas with less marine life, sediment falls slowly to the ocean bottom, so these rocks are well sorted, forming siltstones and shales. However, dinosaurs didn’t live in the oceans, and if we ever find their skeletons in ocean sediments, they probably died somewhere where the currents could carry their bloated bodies out to sea, like a river delta. We should focus our searches, therefore, in terrestrial sediments—and there are a lot of different terrestrial environments where sedimentary rocks form. Some of the main terrestrial depositional environments include: • Eolian: Sediments are deposited by strong winds and usually represent dry desert environments where there aren’t plants and trees to interfere with wind action. Eolian rocks are often sandstones with large preserved dunes. • Lacustrine: Sediments are deposited by lakes. Lakes tend to be low energy systems and so lacustrine rocks are very fine-grained, such as mudstones and shale. • Fluvial: Sediments are deposited by river or stream channels, where the waters carry different size grains, depending on the energy of the system. Fluvial deposits can preserve ripples and layers that can be indicative of flow direction. • Floodplain: When rivers rise up over their banks, flooding adjacent environments, fine-grained muds and sands are deposited. These floodplain deposits can contain evidence of roots and plant material buried by the flood waters. • Estuarine: Sediments deposited in estuaries, which are bodies of water near the ocean and represent a transitional area between river environments and the ocean. As such, sediment deposition is influenced by both river input and tides. • Deltaic: Environments formed where rivers meet the sea. As fast-moving rivers meet the still ocean, they abruptly lose energy and drop most of their sediment load, forming a shallow fan shape moving out from the river. • Alluvial: These are superficially similar to deltaic deposits, but form when rivers exit a steep mountainous or canyon area and enter a flatter area like a valley. The rapid change of gradient causes the river to drop much of the coarse-grained sediment it was carrying, forming an alluvial fan.

39

40

CHAPTER 2    How Do We Know When Dinosaurs Lived?

We also know that, based upon observations of living animals, certain animals are much more likely to be found in some environments than others. While camels might inhabit eolian environments, crocodiles are not usually found there. The same holds true for dinosaurs. The bones of some types of dinosaurs are found most often in sediments that contain plant material and pollen, indicating forests, while others are consistently found in Aeolian sediments indicative of desert environments.

2.5 ROCK CLOCKS: STRATIGRAPHY After reading this section you should be able to… • Apply the principles of stratigraphy to determine the order in which strata were formed. • Explain what an unconformity indicates and identify the three types. • Explain how index fossils and faunal succession can be used to correlate and order geologic units.

If we want to know how old fossils are, we must understand how old the rocks containing them are. But how do we tell the age of rocks? There are two ways we get at the age of rocks: • Stratigraphic dating, which determines the age of rock layers relative to one another • Radiometric dating, which quantifies the numeric age of rock layers in years (Section 2.6) Stratigraphy is a subdiscipline of geology that deals with the study of rock layers, primarily sedimentary rock, which tends to be deposited in layers called strata. One of the founders of stratigraphy was Nicolaus Steno, who lived from 1638 to 1686. Steno proposed four laws that help us determine the relative age of rock layers. The first law, the Law of Superposition, states that if strata are undisturbed, the oldest rocks are on the bottom, and the youngest rocks are on top (Figure 2.27). This law dictates that if Allosaurus fragilis and Tyrannosaurus rex lived together, their skeletons should be in the same, or equivalent layers of rock. As it turns out, we never find bones from Allosaurus in the same layers as T. rex, but rather T. rex always comes from rock layers significantly higher (and therefore younger) than Allosaurus bones. Thus, by studying the rocks and using the Law of Superposition, we can say that Allosaurus lived before T. rex in time. Similarly, we never Figure 2.27  The Law of Superposition states that the brown and gray strata at the bottom were deposited first and are thus older than the tan and orange layers at the top of this stratigraphic section in Montana.

(Courtesy of D. Czajka.)

2.5  Rock Clocks: Stratigraphy

see dinosaur bones and human bones-or even pre-human bones in the same layers, so we know that humans and dinosaurs never lived at the same time. The second law, the Law of Original Horizontality, states that, at the time of deposition, sediment deposited in a basin is laid down in horizontal layers (that is, horizontal relative to gravity at the time they’re formed). So if you find a rock layer that is tilted at a 45-degree angle, the law tells you that it was deposited horizontally first, and must have been tilted by tectonic forces after deposition. The third of Steno’s laws is the Law of Lateral Continuity. This states that at the time they were deposited, a single layer of rock was contiguous (i.e., connected with no gaps). Because of uplift, erosion, and other processes, these contiguous layers might be interrupted—missing in some areas where the rock has been eroded away by these forces (Figure  2.28). Think of a blanket of snow covering either side of a highway. Two snowstorms did not independently create the snow on the left and right sides of the road. It was one storm that deposited it, and a plow (hopefully!) removed the section of snow across the road that would have connected the two regions. Lateral continuity allows us to correlate fossils found in layers separated by weathering and erosion. It also helps us determine where to look for our favorite dinosaurs. For example, suppose when I am hunting dinosaurs, I find evidence of a T. rex in one particular layer of rock. But there is only a little bit of him, and I’d like to find a more complete skeleton. I can see that the same layer is exposed across the valley and continues all around the side of the outcrop. Because of lateral continuity, I know that these layers were once connected, and therefore dinosaur bones found in the layer on one side are the same age as the ones in the layer on the other, whether or not that layer is still connected. This implies that more of the T. rex skeleton might be found in that layer, exposed elsewhere. Finally, Steno proposed the Principle of Crosscutting Relationships. Suppose you have a series of strata that were laid down from oldest (at the bottom) to youngest (at the top), and then imagine that a river of molten rock cuts through those layers (Figure 2.29). Would the resulting intrusive igneous rock be older or younger than the sedimentary rocks? If you said the igneous rock was younger you would be correct, as the sedimentary rocks had to have been laid down first for the igneous intrusion to cut across them, much like a sandwich has to be made before you can cut it in half. This is the principle of crosscutting relationships; the feature (e.g., igneous intrusion, fault line) that does the cutting is always younger than the rock layers that it cuts. Another founder of historical geology was James Hutton. Hutton was a Scottish farmer and was the first to describe the rock cycle (Section 2.3,

Figure 2.28  Illustration of the Law of Lateral continuity. While now separated

by an erosional feature, the layers pictured were originally continuous at the time of deposition. (Courtesy of woudloper; https:// commons.wikimedia.org/wiki/File:Prin​ciple​ _of_h​orizo​ntal_​conti​nuity​.svg.​)

41

42

CHAPTER 2    How Do We Know When Dinosaurs Lived?

Figure 2.29  The Principle of Crosscutting Relationships states that these strata are older than the faults that are cutting through them.

(Courtesy of Roy Luck, https://flic.kr/p/ asqAq7.)

Figure 2.26). But, for the purposes of relative dating, Hutton proposed two key principles. The first was the concept of Uniformitarianism, which simply states that the processes we observe operating today also operated in the past, which geologist Charles Lyell (see below) described with the simple phrase “the present is the key to the past”. Essentially, all of the features that we observe in the geologic rock record are the result of processes that we can observe in action today. Hutton’s second principle was that of unconformities, geological formations which represent enormous time gaps in the rock record (see below). At a time when the world’s age was estimated at only a few thousand years, the idea that it could have taken millions of years to form the landscapes we see was new…and quite controversial. Charles Lyell, also Scottish, lived in England during the 1800s, and built upon the foundation laid by Steno, but also popularized Hutton’s ideas in his famous work “Principles of Geology”. Lyell also added another principle to our understanding of geologic time, the Principle of Inclusions. This is similar to the principle of crosscutting above. When a finger of magma cuts into the surrounding rock, it dislodges some pieces of the rock it invades (the host rock). These little pieces then become incorporated into the still-liquid magma and are solidified inside it as an inclusion. The end result is a composite of sedimentary and igneous rock, and when we find this in the field, the principle of inclusions tells us the relative age of the composition; inclusions are always older than the rock into which they are incorporated (Figure 2.30). The floating pieces of rock that become part of the invading igneous body had to have been there first to become incorporated in the first place, therefore they are older. Figure 2.30  Based on The Principle of Inclusions, the white limestone block must be older than the volcanic igneous rock that includes it. (Courtesy

of https://upload.wikimedia.org/wikipedia/ commons/f/f2/Xenolith.JPG.)

2.5  Rock Clocks: Stratigraphy

Applying Steno, Hutton, and Lyell’s principles allows us to put things into a relative time construct. They don’t allow us to state that a rock is 65 million years old, but by using them, we can say with confidence which rock layers are older or younger than others. To look a little more closely at the concept of “time-telling” by geology, let us consider Hutton’s unconformities. These deal with loss of time in the geological record. Unconformities are significant time gaps in a series of rock strata that represent an interruption in the deposition of sediment, either because deposition never occurred or because erosion removed it. There are three types of unconformities. The first is a nonconformity. This happens when igneous or metamorphic rock, formed deep under the surface of the earth, is uplifted to shallower levels (usually by mountain building forces). Then, these rocks are exposed and subjected to weathering. At some later time, sedimentary rocks are laid down on the surface of the exposed igneous rocks. Thus, a nonconformity (Figure 2.31) involves two different rock types, sedimentary rock over igneous or metamorphic. This type of unconformity represents events taking place over a significant amount of time: the igneous rock cooling and solidifying, then being uplifted toward the surface, then the topmost portion being eroded, then sediments depositing on this exposed surface, eventually undergoing lithification. A nonconformity, therefore, usually represents hundreds of millions of years of “missing” data. A disconformity (Figure 2.32) happens when the deposition of sedimentary rock is interrupted and then restarts at a later time. They are represented by two parallel sedimentary layers separated by an erosional surface, which is indicative of missing time. Think about limestone being formed in a shallow ocean near the coast. If sea level drops, the limestone becomes exposed at the surface and undergoes erosion. If sea level rises back to the level it was at, new limestone will be formed on top of the previously exposed and eroded limestone. The erosional surface between the limestone layers represents a gap in time when no deposition was occurring. The amount of time represented by a disconformity can be relatively small, or it can represent tens of thousands to millions of years. The important point is that disconformities involve two parallel sedimentary layers separated by an erosional surface. The easiest type of unconformity to recognize is an angular unconformity, and again, it represents a very long time between depositional events. In an angular unconformity, strata laid down in originally horizontal layers have been uplifted and tilted through tectonic events into layers that are angled—sometimes into very steep and dramatic angles.

Figure 2.31  Photo of the Great Unconformity in the Grand Canyon, showing a nonconformity. Here

the Vishnu schist, a metamorphic rock, underlies the Tapeats Sandstone, representing over a billion years of missing time! (Courtesy of Rachel Atkins.)

43

44

CHAPTER 2    How Do We Know When Dinosaurs Lived? Figure 2.32  Photo of a disconformity.

The layers are parallel to each other, but the upper dark shales are Devonian in age while the lower dolostones are Ordovician in age. There are about 55 million years of missing time, including the entire Silurian Period. (Adapted from James St. John, https://flic. kr/p/KogKZW.)

The exposed, angled rock layers undergo erosion for a time, and when deposition restarts, new rock layers are again laid down horizontally. The end result is a rock outcropping that has angled strata on the bottom, overlain by newer horizontal strata (Figure 2.33 and Table 2.2). Armed with these concepts of how the rocks record time, and the ways we can read that time, let’s move on to the concept of biostratigraphy. This requires using fossils (“bio”) to correlate layers, or strata, of rock (“stratigraphy”), or in other words, using fossils to help determine the relative ages of rock. English geologist William Smith was among the first geologists to recognize that strata could be divided into eras of time and correlated across space based on the fossils they contained. This can be accomplished in several ways. The type of fossils, or certain features in fossils of a similar type, change as you go from lower (older) to higher (younger) sections of a stratigraphic column. For example, they change in size, or fossils of sea-dwelling creatures may be replaced with land-dwelling types. A dinosaur that looks pretty much the same below the neck may have bigger horns, shields, or crests as you go from lower to higher, or an entirely new organism may be represented, like mammals, when there was no hint of them in lower sections. This trend was first observed by Smith, and he described it as the Principle of Faunal Succession, where organisms change in a very systematic way over time.

Figure 2.33  Photo of an angular unconformity in the Grand Canyon, representing around 600–700 million years of missing time. The angled layers

were originally deposited horizontally, then tilted and eroded, and eventually, new horizontal layers were deposited on top of the angled layers. (Courtesy of James St. John; https://flic.kr/p/dMehuH.)

2.5  Rock Clocks: Stratigraphy

45

TABLE 2.2 SUMMARY OF “TIME-TELLING” PRINCIPLES Principal/Law

Key Features

Superposition

Older strata below younger

Horizontality

Strata that are tilted were originally deposited horizontally

Lateral continuity

Separated strata can be correlated even if not contiguous

Crosscutting

Strata being cut across are older than the feature doing the cutting

Inclusions

Rock inclusions are older than the layer they are in

Nonconformity

Sedimentary strata deposited on igneous or metamorphic rock separated by erosion

Disconformity

Sedimentary strata separated by an erosional surface

Angular unconformity

Strata laid down horizontally, tilted, and eroded, then more strata deposited on top of the erosional surface

In addition, there are some types of fossils that are very short-lived, geologically speaking, but are also unique, so if those types of fossils are observed, the time when the fossil-containing rocks were laid down can be highly constrained. (These characteristic fossils are called index fossils). Other fossil organisms lived a very long time and are quite widespread. Where these long-lived fossils overlap with others, both can be used to determine the relative ages of the rocks. In the example in Figure 2.34, you can see the orange shells persist for a significant amount of time, as indicated by the two bottom layers of limestone. The red gastropod

Figure 2.34  Two stratigraphic columns demonstrating the use of fossils to correlate and attain the relative ages of sedimentary layers.

46

CHAPTER 2    How Do We Know When Dinosaurs Lived?

and green trilobite fossils are only found in the oldest (lowest) rocks. The purple ammonite and brown clam fossils are found only in the middle and top layers. Therefore, finding the orange shell, purple ammonite, and brown clam fossils together in location B allows you to constrain the age to the same layer they are found together in location A, even though assemblage 1 and 3 are not found at all in the second location, because the only time you see this group of fossils together falls within a constrained age, younger than layer 1 and older than layer 3.

2.6 ROCK CLOCKS: RADIOACTIVE ISOTOPES AND ABSOLUTE DATING After reading this section you should be able to… • Explain what happens during radioactive decay using the terms parent isotope, daughter isotope, and half-life. • Use the relative proportions of parent and daughter isotopes to determine the numerical ages of rocks. • Assess why certain isotopes (e.g., carbon-14) cannot be used to date older rocks from the time of the dinosaurs.

So far, all of Steno and Lyell’s principles, and the concepts of index fossils and faunal succession, only allow us to say “this rock layer is older than this one” or “these fossils predate dinosaurs and others postdate them”—they can only give us a qualitative sense of time relative to something else. So how can we say that dinosaurs emerged about 230 million years ago or that they went extinct 65 million years ago? How do we obtain hard or absolute dates for rocks and the fossils they contain (i.e., quantitative data)? Absolute geochronology adds numbers to the relationships we have resolved through the various relative dating strategies. These numbers are based upon principles of isotope decay. To understand how this works requires a chemistry refresher. Let’s start with elements. What is an element? What defines an element to the exclusion of others? Or, what makes carbon carbon, and not nitrogen? First, remember that atoms are made up of three types of subatomic particles: • Protons: Particles with mass that have a positive charge • Neutrons: Particles with mass that have no charge (i.e., neutral) • Electrons: Particles with (effectively) no mass and a negative charge An element is defined by the number of protons in its nucleus, which is unique to each element. This number is its atomic number. This is frequently also the number of electrons associated with an atom of a given element, because in a neutral atom, the number of protons and electrons present are the same and their charges cancel each other out. In shorthand, it looks like this: # protons = # electrons = atomic number. However, we can also characterize an element in another way—by comparing the number of protons and the number of neutrons in the nucleus. Because the number of protons is defining and unique for each element, for a given atom of an element, the number of protons is always the same—an atom of carbon always has six protons. If that changed, it would become an atom of a different element. However, the number

2.6  Rock Clocks: Radioactive Isotopes and Absolute Dating

of neutrons can vary, and because neutrons have mass, that means that the mass of two atoms of carbon can be different, even if the number of protons is the same. The combined mass of the protons and neutrons in a nucleus make up the atomic mass of an atom. Atoms with the same atomic number but different atomic masses are called isotopes of one another. For example, in Figure 2.35, all of these atoms are the same element, hydrogen, and we know this because they all have the same number of protons. But protium, deuterium, and tritium are all isotopes of hydrogen, because their number of neutrons, and therefore their mass, differs. The vast majority of hydrogen that is found on our planet is 1H, the simplest element, with only one proton and one electron. When denoting an isotope, the atomic mass (# of protons + neutrons) is written to the top left of the letter symbolizing the element, as was done above with the protium isotope of hydrogen (1H). The stable isotope of carbon (atomic number 6) with six neutrons would be denoted 12C. Over 99% of the carbon in our atmosphere is 12C, with 13C and 14C occurring at less than 1% and in trace amounts, respectively. How many protons are found in the nucleus of 14C? Isotopes can be stable or unstable. An imbalance in the number of protons and neutrons in the nucleus can cause an isotope to be unstable, which causes them to give off energy through a process known as radioactive decay. There are three common types of radioactive decay, called alpha (α), beta (β), and gamma (γ) decay, but for our purposes, only alpha and beta decay are useful in absolute dating, so we will limit our discussion to those two types. During alpha decay, an unstable nucleus kicks out two protons and two neutrons, which is in essence, a helium atom. The loss of an α particle reduces both the atomic mass and the atomic number of the parent element by that amount. When an isotope undergoes alpha decay, it becomes a completely new element because it has lost two protons. For example, 238Ur (uranium, atomic number 92) undergoes alpha decay, becoming 234Th (thorium). How many protons does thorium have? It is also important to note, that not all decay products are stable. The 234Th that results from the decay of 238Ur is also unstable, and the decay of 238Ur leads to the formation of eight different elements until the stable lead-206 (206Pb) is reached! When an isotope undergoes beta decay, one of two things happens. Either a proton is spontaneously converted into a neutron (called beta plus decay), or a neutron is converted into a proton (beta minus decay). When this occurs, the isotope also releases energy in the form of a beta particle which is either an electron or a positron (another type of subatomic particle). Although beta decay does not change the atomic mass of an

Figure 2.35  Image showing the three naturally occurring isotopes of hydrogen. All have one proton, but

varying numbers of neutrons. (Courtesy of BruceBlaus; https://commons.wikimedia.org/ wiki/File:Blausen_0530_HydrogenIsotopes. png.)

47

48

CHAPTER 2    How Do We Know When Dinosaurs Lived?

isotope, it does alter the atomic number, and like alpha decay, results in a new element, but one with the same mass. Carbon-14 (14C) undergoes beta minus decay, meaning a neutron becomes a proton, and becomes nitrogen-14 (14N). If carbon has six protons, how many protons does 14N have? So how do we use this information to determine the absolute age of rocks? While radioactive decay is a truly random process, using large sample sizes can allow us to determine the average time it will take for half of a sample of a specific isotope to decay. We use the concept of a “half-life”, defined as the time it takes for half of the starting, or parent, material to decay into the end, or daughter, product. This half-life number varies and is unique to each radioactive isotope. When an igneous rock first forms, or solidifies, there is no daughter material present. As time passes, part of the parent material that has solidified in the rock, through the processes of radioactive decay, will convert to the daughter product—the amount of parent isotope gradually decreases, and the amount of daughter isotope increases. This occurs at a known and constant rate; therefore, measuring the ratio of parent to daughter material in a rock sample can reveal the age of the rock. This process is known as absolute, radiometric, or numerical age dating. Some common elements used for radiometric dating are shown in Table 2.3. Let’s work through an example to give you a better idea of how this works. Suppose you find a rock and you’re curious how old it is. You send a small sample off to an analytical lab, and they tell you it has 25% 235Ur and 75% 207Lead. First you need to figure out how many half-lives the uranium has been through. By definition, after one half-life there is 50% parent and 50% daughter. Since your sample has only 25% of the parent (235Ur) it must have gone through an additional half-life (after two halflives there is 25% parent remaining). So your sample has gone through two half-lives, and you know that the time it takes for half a sample of 235Ur to decay into 207Pb is 704 million years, multiplying by two will give you the age of your sample, 1,408 million or 1.4 billion years old! So, what does all this chemistry and physics have to do with dinosaurs? Keeping in mind that our central question in this chapter is “how do we know when dinosaurs lived?”, this concept of radiometric decay is critical to putting numbers on our geological timeline. As stated above, these types of decay from one element to another occur at determined rates, rates that are unique to each element, and so act like small atomic clocks in the rock. When we measure the isotopes of elements making up a rock, and then measure the ratio of parent to daughter decay products, we can accurately determine how old the rock is. However, there is one catch. Radioactive decay can only be used to obtain the ages of igneous and some low-grade metamorphic rocks (those that haven’t been cooked too hotly, which resets the atomic clocks). Because sedimentary rock forms from pre-existing rock, applying radiometric dating will only tell us when the pre-existing rock was formed, not when the sedimentary

TABLE 2.3 HALF-LIFE OF COMMONLY USED GEOCHRONOLOGICAL ISOTOPES Parent Isotope

Daughter Isotope

238

Uranium

206

235

4.5 billion years

Uranium

207

Potassium

40

Carbon

14

40 14

Half-Life

Lead Lead

704 million years

Argon

1.25 billion years

Nitrogen

5,730 years

2.7  Our Roadmap Through Time: The Geologic Timescale Figure 2.36  Two stratigraphic columns demonstrating (1) the use of fossils to correlate and attain the relative ages of sedimentary layers and (2) the use of radiometric dating to assign a numeric date range to the fossils in the layer.

rock itself was formed. But…we said that almost all fossils are found in sedimentary rock, so how does this help us? We can date volcanic rocks that are interbedded with rocks containing the fossils. So if we go back to our illustration in Figure 2.34 (reproduced as Figure 2.36), imagine that in location B, there were two volcanic ash layers (igneous rock, represented by the red lines), above and below the bed containing the fossils we are interested in. We can measure the absolute age of these ash layers, bracketing the age of assemblage 2 to no older than ~300 million years, and no younger than ~250 million years. And, because of biostratigraphy, we can say that in Location A, where there are no igneous rocks, assemblage 2 is also between 250 and 300 million years old. All of the concepts described for both relative and absolute dating are used in tandem; both are vital to being able to place major events in life history on a timeline. This is also crucial to figuring out dinosaur relationships, because having a “descendant” (derived) dinosaur living before its ancestral (basal) relatives would be rather problematic. Each of the concepts we have discussed contributes different information to our understanding of time in the rock record, but when all are used together, the data are very robust. Thus, we can say when dinosaurs lived with a high degree of confidence. We can also identify the temporal range of the dinosaurs—how long each group lived, and when they died. From these data, we have learned that some dinosaurs lived longer in some parts of the world than in others. For example, the large, long-necked sauropods went extinct in the Jurassic and Early Cretaceous in most parts of the world, but based upon relative and absolute dating principles, we know there were still small populations of sauropods living at the very end of the “Age of Dinosaurs”!

2.7 OUR ROADMAP THROUGH TIME: THE GEOLOGIC TIMESCALE After reading this section you should be able to… • List the four main divisions of the geologic timescale in the correct hierarchical order. • Identify the Era and Periods in which dinosaurs lived and supply the general age (in millions of years) for each.

49

50

CHAPTER 2    How Do We Know When Dinosaurs Lived?

At this point, and likely prior to reading this book, you have heard terms like Jurassic or Cretaceous. You most likely are familiar with a blockbuster movie franchise that uses the term Jurassic. What is probably less familiar is exactly to what the term “Jurassic” refers, or more importantly, to when the Jurassic is referring. The Jurassic Period is one of many periods in the geologic timescale. As early geologists like Charles Lyell and William Smith began to correlate strata and fossils in different areas, they began to create divisions in Earth’s history. These divisions were largely based on changes in the fossil or rock record, and these changes often signified global environmental or geologic changes or large faunal turnovers (e.g., mass extinctions, see Chapter 20). With the advent of radiometric dating in the early 1900s, not only could the age of the Earth be estimated more precisely, but more accurate dates could now be assigned to the divisions created by geologists. Together, the use of relative and absolute dating allowed scientists to create a geologic timescale that serves as a temporal roadmap through Earth’s 4.5-billion year history (Figure 2.37). The timescale is divided into smaller and smaller divisions and these are defined as follows: • Eons: These are the broadest divisions on the geologic timescale. There are four major eons, the Hadean, Archean, Proterozoic, and Phanerozoic. All dinosaurs lived during the Phanerozoic Eon. • Eras: Each eon is divided into eras. We are going to primarily be concerned with the eras of the Phanerozoic Eon, because this is when dinosaurs lived. The three eras of the Phanerozoic are the Paleozoic, Mesozoic, and Cenozoic. (Greek for “early”, “middle”, and “late” life respectively). All extinct dinosaurs lived during the Mesozoic Era between 252 and 65 million years ago (Mya). • Periods: Eras are divided into periods and the three most important periods for the study of dinosaurs are those of the Mesozoic Era, the Triassic (252–201 Mya), Jurassic (201–145 Mya), and Cretaceous (145–65 Mya). • Epochs: Further subdivide the periods. The epochs of the Mesozoic periods don’t have fancy names, instead they are referred to as Early, Middle, and Late. For example, T. rex lived during the Late Cretaceous. Just as your address can be used to locate you spatially, the geologic timescale allows us to locate events and organisms in time. For example, you live in a certain country, and within that country a specific state, within that state a city, within that city on a street, and on that street a specific house. Temporally (time), you live in the Phanerozoic Eon, the Figure 2.37  The geologic time scale.

2.8  What We Don’t Know

Cenozoic Era, the Quaternary Period, and the Holocene Epoch. Can you figure out T. rex’s temporal address? One thing you might notice about the geologic timescale is that it contains a lot more divisions near the present day, in the most recent 500 million years (Figure 2.37). The reason for this is that there was a massive radiation of life around 542 Mya, known as the Cambrian Explosion. This “explosion” may have occurred as the result of the first “hard parts” like shells and skeletons showing up for the first time in multicellular organisms, and these are more readily preserved in the fossil record. Prior to this, life was mostly microbial or soft-bodied, and much less likely to preserve in the fossil record. The abundance of preserved fossils after 542 Mya has allowed scientists to create a more divided and detailed geologic timescale for the more recent Phanerozoic Eon. The concept of geologic, or deep, time is one that is difficult for humans to grasp because we experience life on the scale of minutes, hours, and days. It can be hard to comprehend just how long a million years is, nevertheless 200 million or even a billion! We think of dinosaurs as having existed a long time in the past, but in Earth’s vast history, they are a relatively recent phenomenon. Dinosaurs evolved around 230 Mya, meaning they only occurred in the last 5% of Earth’s 4.5-billion-year history! Our own species’ existence is far more fleeting. Homo sapiens evolved some 315,000 years ago, and this represents the last 0.007% of Earth’s history! The author John McPhee captures just how brief our own time on this planet is: “Consider the Earth's history as the old measure of the English yard, the distance from the King's nose to the tip of his outstretched hand. One stroke of a nail file on his middle finger erases human history”. When studying events in the Earth’s past, such as the evolution and reign of the dinosaurs, it is important to have fundamental knowledge of the geologic timescale. This way, when you hear the term Jurassic, you will have a general idea of when this was, both relatively (between the Triassic and Cretaceous) and absolutely (201–145 Mya). Familiarity with the timescale not only helps to map events in time, but it gives one an appreciation for the vastness of the Earth’s history and the remarkable events that comprise its past.

2.8 WHAT WE DON’T KNOW There is A LOT that we still don’t know about our own planet and its 4.5-billion-year history, enough that the unknowns would fill an entire book (or an entire series of books). But that is what makes the study of dinosaurs, geology, and science in general so exciting; there will always be questions to answer and knowledge to discover! The following are just two examples of the things we don’t know related to the topics in this chapter.

2.8.1 When Was the Surface of the Earth Able to Support Water in the Form of Oceans? This is one of many questions about the early Earth that is difficult to answer due to the lack of a rock record in the earliest parts of Earth’s history. The oldest rocks on Earth that are about 4.03 billion years old don’t tell us anything about surface conditions. It is not until 3.8 billion years ago that we have rock, known as Banded Iron Formations (BIFs), which are formed by deposition in seawater. So while there is evidence of water on Earth 3.8 billion years ago in the form of BIFs, was water present even earlier? Recent research on isotope values of 4.2-billionyear-old zircon crystals suggests that they formed from magma melts that interacted with water.

51

52

CHAPTER 2    How Do We Know When Dinosaurs Lived?

Questions to consider: • Was the Earth’s hot and hellish Hadean Eon shorter than previously thought, with surface water present after only 300 million years, or even sooner? • What implications does the timing of water on Earth have for the origin and evolution of life on Earth?

2.8.2 What Are the Mantle Mechanics that Explain the Formation of the Supercontinent Pangea? Lots of questions remain about how the Earth’s mantle behaves and how this behavior drives plate tectonics. Supercontinents have been a regular feature of Earth’s surface in the past, and the formation of supercontinents has vast impacts on the Earth’s hydrosphere, atmosphere, and biosphere. The formation and eventual dispersion of Pangea played a significant role in the origin and evolution of dinosaurs. The formation of Pangea is thought to have occurred by an unusual mechanism whereby younger oceanic crust was consumed to bring all the continents together. Generally, when supercontinents form it is due to the subduction of the oldest oceanic crust. What was happening in the mantle that would have caused Pangea to have formed via this introverted (closing of younger oceans) way? Questions to consider: • If Pangea had formed via extroversion (closing of older oceans) like previous supercontinents, how would the timing and arrangement of the supercontinent have been different? • What impact would an extroverted formation for Pangea have had on the origin and evolution of dinosaurs?

INSTITUTIONAL RESOURCES An Introduction to Geology. A free online textbook from Salt Lake Community College: https://opengeology.org/textbook/ Geoscience Videos: https​: //ww ​w.you​tube.​com/c​hanne​l/UCt​QfVk8​PDyHU​6e9q_​ 1cEY0​Q Where did Earth’s water come from? By TEDed: https​: //ww​w.you​tube.​com/w​atch?​ v=Rwt​O04EX​gUE Plate Tectonics Explained by MinuteEarth: https​: //ww​w.you​tube.​com/w​atch?​v=kwf​NGatx​UJI

LITERATURE Daly, R. T. , and Schultz, P. H. (2018). The delivery of water by impacts from planetary accretion to present. Science Advances, 4(4), eaar2632.

Rudge, J. F. , Kleine, T. , and Bourdon, B. (2010). Broad bounds on Earth’s accretion and core formation constrained by geochemical models. Nature Geoscience, 3(6), 439.

Murphy, J. B. , Nance, R. D. , and Cawood, P. A. (2009). Contrasting modes of supercontinent formation and the conundrum of Pangea. Gondwana Research, 15(3–4), 408–420.

Saal, A. E. , Hauri, E. H. , Van Orman, J. A. , and Rutherford, M. J. (2013). Hydrogen isotopes in lunar volcanic glasses and melt inclusions reveal a carbonaceous chondrite heritage. Science, 340(6138), 1317–1320.

3 3

HOW DO WE EXPLAIN VARIATION AMONG PAST AND PRESENT ORGANISMS? EVOLUTION AND EVOLUTIONARY MECHANISMS

IN THIS CHAPTER . . .

I

n 1859, Charles Darwin published his now-famous book, On the Origin of Species, which laid out one of the fundamental principles of evolution: natural selection. By describing processes of natural selection, he provided a mechanism for what we now call the “Theory of Evolution”. We already discussed (Chapter 1) that a theory is the strongest scientific explanation that can be made, and one supported with a lot of accumulated evidence. However, despite its abundant cross-disciplinary support, derived from geology and sedimentology (geological time), nuclear physics (absolute dating), molecular biology (genetic mutations and mutation rates), and morphology (common ancestry and biomechanical function), the concept of evolution has probably generated more controversy among the public than any other scientific theory. The predictions allowed by the theory of evolution have been validated, sometimes in surprisingly direct ways. Further, it has profound implications for any discipline related to biology at any level; evolution through natural selection underlies every aspect of biology, from medical treatments and drug design to designing landscapes for different climates. Some have even referred to evolution as the “grand unifying theory of biology”. So what exactly is the biological, scientific definition of “evolution”? What is the evidence for evolution and how do we use the principles of evolution to study dinosaurs?

3.1 DARWIN’S TENETS OF EVOLUTION 3.2 MODES OF NATURAL SELECTION 3.3 CHANGE IN POPULATIONS: EVOLUTION IN ACTION 3.4 DRIVERS OF EVOLUTION: VARIATION AND SELECTION 3.5 SPECIATION, MICROEVOLUTION, AND MACROEVOLUTION 3.6 THE PACE OF CHANGE: GRADUALISM VS. PUNCTUATED EQUILIBRIUM 3.7 EVOLUTION: FACT OR THEORY? 3.8 WHAT WE DON’T KNOW

54

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms?

3.1 DARWIN’S TENETS OF EVOLUTION After reading this section you should be able to… • State the tenets of Darwin’s theory of evolution. • Differentiate between phenotype and genotype. • Define evolution.

Over the centuries since Darwin published On the Origin of Species, there has been much discussion (and much confusion) among the general public as to what Darwin’s treatise on evolution actually says, and what those ideas actually mean. The theory of evolution by natural selection (as proposed by Darwin) rests on these main tenets: 1. Populations possess individuals with varying traits (i.e., characters). Populations consist of many individuals of the same species, and there can be a lot of variation between those individuals (Figure 3.1). Just look around, you can see that this is true—no one you meet looks exactly like yourself (unless you have an identical twin, and even then there are slight differences). This variation in character states goes beyond just an individual’s appearance; we vary from those around us in things like eyesight acuity, metabolic efficiency, growth rate, pigment expression, blood type, and our predisposition to be susceptible or resistant to certain diseases. The sum total of how all the varying traits are expressed within a given individual is called its phenotype, and the variation we observe between individuals is called phenotypic variation. 2. These characters are heritable and can be passed from parents to their offspring. You’ve probably heard people say things like “you’ve got your mother’s eyes” or “the baby has its father’s nose”. It has been well-recognized for centuries that parents produce offspring that share some of their features. In fact, this is the basis for the practice

Figure 3.1  Fifteen individuals of the bivalve species Donax variabilis showing a wide range of phenotypic variation in the color pattern of their shell. (Courtesy of Debivort, https://

commons.wikimedia.org/wiki/File:Coquina_ variation3.jpg.)

3.1  Darwin’s Tenets of Evolution

of selectively breeding animals to produce desired “breeds” of dogs, horses, and other livestock, a practice that has spanned many cultures over thousands of years (how else would you get a pug?). Although the concept that offspring share some features with each of their parents seems obvious, at the time that Darwin wrote On the Origin of Species in 1859, no one knew about the existence of DNA or that this complex molecule was the carrier of all information about an organism at the genetic level. Since Darwin’s time, we have discovered that traits outwardly expressed by an individual (its phenotype) are coded for in an organism’s genes (i.e., its genetic code or genotype). It is portions of an organism’s genotype, passed on to offspring, which dictate these shared features. An individual’s genotype is its literal genetic code, the As, Ts, Gs, and Cs (the nucleic acids in DNA) that carry the information needed for an organism to grow and function. Like letters combining to make a word, the specific order in which these nucleic acid bases align on the DNA strands determines the traits the organism will express. It is the genotype that is passed from one generation to the next (half from each parent), and it is from changes in the genotype—a reordering of the “letters”, from time to time—that all variation arises. However, it is in the phenotype that this variation is expressed and observed, and it is the phenotype upon which natural selection acts. An example of this genotype-phenotype relationship that affects humans is a disease called sickle cell anemia. A change in a single base in the DNA coding for hemoglobin (out of ~440 bases) results in an abnormal protein, causing the protein, and consequently the cell containing it, to change shape, from a rounded cell to a sickle shape (Figure 3.2). In people that inherit this genotype from both of their parents, the resulting phenotype of altered hemoglobin and blood cells decreases the amount of oxygen their blood can carry,

Figure 3.2  Individuals with sickle cell anemia inherit from their parents a genetic mutation in the section of their genome that codes for the protein hemoglobin. This mutation

results in red blood cells that are shaped like sickles instead of the typical round shape (inset), which can obstruct blood flow to tissues and organs. This illustrates the direct relationship between an individual’s genotype (their genetic code) and their phenotype (the morphology produced by that genetic code). (Courtesy of BruceBlaus, https://commons.wikimedia.org/wiki/ File:Sickle_Cell_Anemia.png.)

55

56

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms?

and can cause painful blockages in their blood vessels when their sickle-shaped cell gets “hung-up” on other cells. 3. Organisms produce more offspring than are needed to replace themselves, thus competing for limited resources. Female cats can birth litters of four to five kittens (on average) and have up to three litters per year. That means a cat that reproduces for ten years can produce 120–150 kittens—no wonder the internet has no shortage of cat memes (meme is a play on the word gene; memes are cultural ideas that are spread by individuals)! Obviously, this is many more cats than are needed to replace the two cats required to make them. And many other species have even higher reproduction rates. A female guinea pig can have litters of four to eight pups up to five times a year, for eight years, producing up to 320 pups (Figure 3.3). One female cockroach can produce up to 400 eggs in her lifetime, and one female fly can produce up to 900 eggs. 4. Some of these inherited characters can help individuals survive and reproduce, thus these helpful variations become more common in a population over time. Because animals produce more offspring than needed to replace themselves, this inevitably leads to competition for resources between individuals within a population, as well as between different populations. All resources are limited. Space, water, shelter, food, and light are just a few of the finite resources organisms must have to survive. Since individuals in a population aren’t exactly the same (tenet two), some will have traits that are better suited for success in this competition. Going back to the previous example of sickle cell anemia, it would seem that if this genetic mutation causes so many dangerous health issues, it would be selected against, and eventually removed from the human population, right? It turns out that there is more to the story. This mutation is prevalent in African populations, particularly those with roots to regions in Africa that are exposed to malaria, a mosquito-borne disease that is as lethal as sickle cell anemia. Although two copies of the sickle cell gene can be fatal, if a human has only one copy of the mutated gene, they have strong resistance to malaria! In that region of our planet, a genotype bearing one copy of the mutation results in a malaria-resistant phenotype that experiences great health advantages over individuals with either two copies of the mutation (sickle cell phenotype) or no mutation (malaria susceptible phenotype). Another example of selection acting on advantageous mutations comes from plants. Photosynthesis evolved very early in the history of life, within 0.5 billion years of life originating. The process is old, Figure 3.3  A female guinea pig with a litter of pups. A single guinea pig can

produce around 40 litters of pups in her lifetime, each with four to eight pups, producing far more offspring than is needed to replace herself. (Courtesy of Kaitlyn Tiffany.)

3.2  Modes of Natural Selection

and effective, and the proteins that are part of photosynthesis are very widespread in all plants. However, after millennia of an overall warm, wet global climate, in the Oligocene and Miocene (34–35 million years ago), the planet went through prolonged periods of drought. In the plants that arose during this prolonged dry spell, we see evidence for the development of a new type of photosynthesis—a type that uses different proteins in a different pathway and requires much less water. We call these C4 plants, and they include some grasses, a type of plant that changed the planet forever. At first, these plants were rare, but extended drought put selective pressure on the plant population—i.e., pressure that causes selective (non-random) survival of individuals, who will go on to reproduce and pass down the advantageous traits to their offspring (tenet two). This process is called natural selection. As a population undergoes natural selection over generations, individuals with certain advantageous traits proliferate, while individuals with detrimental, or less advantageous ones are lost over time, resulting in a slow and gradual change of the average phenotype of a population. From these tenets, we can arrive at a simple and direct definition for evolution: inherited change in a population over time. Other common ways this definition has been phrased include “descent with modification” or “change in the frequency of alleles (i.e., gene variants) in a population”. No matter how it is phrased, the inherent meaning is always the same: populations change over successive generations as changes accumulate in their inherited traits.

3.2 MODES OF NATURAL SELECTION After reading this section you should be able to… • Give an example of directional, stabilizing, diversifying, and sexual selection relating to dinosaurs. • Show each mode of selection graphically. • Describe the outcomes of each mode of selection over time. • Summarize how sexual selection can shape a population.

There are three basic modes of natural selection: • Directional selection • Diversifying selection • Stabilizing selection

3.2.1 Directional Selection In directional selection, an “extreme” phenotype for a trait (e.g., small size, long neck, dark color) is favored over others, causing that phenotype to be more commonly expressed in a population (Figure 3.4). For example, consider a population of mice that populate a forest after a forest fire. In the dark soot left behind, black mice would be the hardest to spot, while mice with white fur would stand out starkly and be easily picked out by predators. After several generations, a population that started with a wide variety of coloration will shift toward the greatest number of individuals in the population having very dark fur and few individuals having pale fur. Directional selection in dinosaurs: Imagine a small population of small (human-sized), carnivorous bipedal dinosaurs living in an ancient forest.

57

58

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms? Figure 3.4  Diagram representing the effect of directional selection on the expression of a trait in a population.

The movement of the population’s most common phenotype toward a more extreme expression of the trait (e.g., greater length, darker color) over time is indicated by the dotted lines. (Adapted from a diagram by Azcolvin429, https://commons.wikimedia. org/wiki/File:Directional_selection_after.svg.)

To avoid competition as the population expanded, suppose a subpopulation of these little guys moved away from the forest floor into a more open habitat. This would make them more vulnerable to predation, so over time, slightly bigger sizes might be favored. Can you see how, if this trend continued, we might get an enormous T. rex?

3.2.2 Diversifying Selection (or Disruptive Selection) In diversifying selection, multiple extreme phenotypes for a trait (e.g., small and large, dark and light) are favored, while intermediate forms are selected against, causing a split in the dominant expression of the trait in the population (Figure 3.5). Consider that same population of mice that live in an area that contains both patches of very dark underbrush and very light soil. Mice with light fur would be hard to spot on the soil, while mice with dark fur would be hard to see in the underbrush. Mice with coloration between these two endpoints, however, would be easily spotted by predators on both the soil and the underbrush, giving them a disadvantage on either terrain. This would lead to a population of mostly light or dark mice, with few individuals with intermediate coloration.

Figure 3.5  Diagram representing the effect of diversifying (or disruptive) selection on the expression of a trait in a population. The intermediate

expression of a trait (gray dotted line) is selected against, causing it to become less frequent in the population over time. Conversely, extreme expressions of the trait on both ends of the spectrum (e.g., dark and light) become more frequent (black dotted lines). (Adapted from a diagram by Azcolvin429, (https://commons.wikimedia. org/wiki/File:Disruptive_selection_after.svg.)

3.2  Modes of Natural Selection

Diversifying selection in dinosaurs: In the example above, a small population of bipedal dinosaurs moved out of the forest floor into a more open habitat, favoring large size. But the population remaining in the forest would still face competition. Smaller dinosaurs might require less food, be able to negotiate quick changes of direction while running between trees, and be able to reproduce more rapidly and more often. Given these pressures, can you see how diversifying selection might produce tiny compsognathids and large tyrannosaurids from the same starting population of theropods?

3.2.3 Stabilizing Selection In stabilizing selection, the intermediate phenotype for a trait (e.g., medium height, neither tall nor short) is favored, causing the extreme phenotypes (e.g., tall and short) to be less common, resulting in an overall reduction in variation in the population (Figure 3.6). For example, in those same mice that live on the forest floor, brown, mottled fur would allow them to blend into the sun and shadows of the underbrush, but black or white fur would stand out starkly, allowing predators to spot them easily. While the original population of mice may have been quite variable, after several generations, almost all of the mice will be brown and mottled. Stabilizing selection in dinosaurs: Horned dinosaurs, like Triceratops, are known for their highly variable head ornaments. Huge frills with spikes and projections or large holes, long and curved nasal horns, or elongated “eyebrow horns” make them stand out among other dinosaurs. Yet, their bodies, from the neck down, are virtually indistinguishable. Many reasons have been put forth to explain variation in their heads, including sexual selection (below) or sympatry, where they must distinguish themselves from similar dinosaurs when ranges overlap. But the very lack of variation from the neck down may be an example of stabilizing selection, because, after all, how much variation is allowed when an animal has to carry around a head that is about a third the length of the body! There wouldn’t be much room for variation in body dimensions!

3.2.4 Sexual Selection Natural selection produces adaptive traits—traits that confer an advantage to organisms that possess them. However, not all evolutionary change helps an animal adapt to its environment. In fact, sometimes it

Figure 3.6  Diagram representing the effect of stabilizing selection on the expression of a trait in a population.

In this example, the intermediate expression of a trait (black dotted line), which was already the most frequent in the population, is favored. It remains the most frequent, and over time, the extreme expressions of the trait (e.g., tall and short) become less frequent. (Adapted from a diagram by Azcolvin429, https://commons.wikimedia. org/wiki/File:Stabilizing_selection_after.svg.)

59

60

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms?

can be quite the opposite! Sexual selection happens, not when driven by competition for resources, rather, it is driven by competition for mates! Sexual selection explains the persistence of a lot of traits that don’t seem to be advantageous otherwise. Bright colors in birds, big antlers in deer, and heavy manes in lions don’t necessarily give the bearers of these traits direct adaptive advantage—after all, bright colors are easily spotted by predators, big antlers are heavy and can get caught in trees, and long manes cost metabolic energy to maintain with little benefit (starving lions lose their manes). Take, for example, peafowl (Figure 3.7). The iconic color and pattern of the tail of the male peafowl (peacock) is, perhaps, the most well-known example of sexual display in the animal kingdom. Males with the biggest, most colorful feathers are the most likely to secure mates, because these features are preferred by the females (peahens) of the population. However, these long tails make flight very difficult for the males of the species—almost impossible for full-grown males—and they make it easier for predators to catch them. Their big tails don’t have a practical adaptive advantage beyond preference by the opposite sex. The presence of sexually selected traits can be correlated with sexual dimorphism. Sexual dimorphism is a scientific way to say that animals possess differing characters because they are male or female. We will cover this more in Chapter 17. Briefly, you can tell male and female young apart by observing their primary sex characteristics—the ones they are born with—the genitals. But sexually dimorphic traits are secondary— that is, they go beyond differences in their genitals (primary traits) and develop later. Sexually dimorphic traits, then, don’t show up in an individual until they will be practical—individuals express these traits only as they begin to approach sexual maturity. After all, there is no point in expending metabolic energy to develop or maintain these features (a mane, antlers, enormous tail feathers) if the individual is not ready to use them to compete for mates. For example, consider humans. Chances are you will not be able to tell whether your new baby cousin is a male or female until you are charged with changing their diapers. However, when your cousin is about ready Figure 3.7  Male (left) and female (right) peafowl. The peacock’s tail is a

classic example of sexual selection in action. Although there is no practical adaptive advantage to the peacock’s large and colorful tail—in fact, it impairs their ability to fly and evade predators—this trait is preferred by females during mate selection. (Courtesy of K. Tiffany, taken at the Field Museum.)

3.3  Change in Populations: Evolution in Action

to attend junior high school, things start to change—puberty can produce deeper voices, facial hair, and a repositioning of fatty deposits. When these traits appear, they indicate that the individual is getting ready for reproduction, but the traits themselves do not directly contribute to reproduction. The same is true with animals. Baby deer look pretty much alike, until they approach sexual maturity. Then, the males sprout their first little nubs of antlers. Sexual selection in dinosaurs: The fact that sexually selected traits don’t usually confer an obvious adaptive advantage, like sharper teeth or longer legs, do both explain certain features we observe in dinosaurs, and complicate our interpretations of other features. Dinosaurs have some pretty weird traits—like bowling‐ball shaped domes on the head of pachycephalosaurs or enormous (and heavy) head shields in ceratopsians. If these traits are the result of sexual selection, we would predict only adults would have them. Furthermore, we would predict that roughly half the adult population would possess them. But, if we find small dinosaurs with small head shields, is this sexual dimorphism? Or a different species? Or, does it mean the small ones are still growing, thus immature? We will discuss these concepts more when we talk about dinosaur reproduction in Chapter 17. When humans guide selection, as they do when breeding dogs, racehorses, or food crops, it is called artificial selection (or selective breeding). When environmental factors determine favorable traits, that is natural selection. When the preference of a potential mate determines what is favorable, that is sexual selection.

3.3 CHANGE IN POPULATIONS: EVOLUTION IN ACTION After reading this section you should be able to… • Differentiate between species and population. • Give the biological definition of a species. • Describe one example of evolution in action.

Now that we’ve established what evolution is, let’s talk about who evolves. Can you evolve in the manner referred to by Darwin? The answer is no! Scientifically speaking, individuals do not evolve—only populations do. Populations are groups of individuals that all belong to the same species. There are a number of ways scientists define a species, but for our purposes, we will use the “biological species concept” definition: a species is all members of a group that can interbreed and produce viable (capable of living) and fertile (capable of bearing young) offspring. Therefore, a group of wild horses in Montana would comprise a population of horses, and all horses comprise a species. Conversely, although donkeys look very similar to horses in many ways, they can’t produce fertile offspring when they are bred with a horse—a horse and a donkey make a mule (Figure 3.8), that while viable, can’t produce its own babies. It is unquestionable, and demonstrable, that populations have changed over time. Let’s look at a few examples of changes in populations.

3.3.1 Wild Corn There are many food crops humans utilize today that, through domestication and generations of selective breeding (i.e., artificial selection)

61

62

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms? Figure 3.8  A donkey (A) and a horse (B) can breed to make a mule (C), which is viable, but can’t reproduce.

(A courtesy of A. Pingstone, public domain; B courtesy of Kaitlyn Tiffany; C courtesy of J.R. Lascorz, https://commons.wikimedia. org/wiki/File:09.Moriles_Mula.jpg.)

by humans, have become extremely different in shape, size, color, and nutritive value from their original “wild” populations. Corn, for example, originated as a grassland plant called teosinte. There are still regions where teosinte thrives, and when we compare the genomes of this grass to the tender, juicy staple of backyard summer cookouts, they are almost identical (and therefore, very closely related). But as you can see in Figure 3.9, you would have a very hard time buttering an ear of teosinte.

3.3  Change in Populations: Evolution in Action Figure 3.9  Through selective breeding, modern corn was produced from the grassland plant teosinte.

(Teosinte courtesy of M. Lavin, Lavin https:// commons.wikimedia.org/wiki/File:Teosinte_ ear_(Zea_diploperennis).jpg; corn courtesy of G. Peters, https://commons. wikimedia.org/wiki/File:Corn_on_the_cob_ (5178296206).jpg.)

3.3.2 Selective Breeding of Dogs and Cats Let’s look at another example of selective breeding. In this case, humans are also the selective agents, because they decide certain traits have value—dogs that run fast, for example, or cats with big ears, or no tail. Then, when these dogs or cats are bred with individuals who possess similar traits of interest, those traits can be refined and exaggerated in successive generations. Thus, this process can produce a wide variety of phenotypes over time, including a pug from a wolf (ancestral dog) (Figure 3.10) or a flat-faced Persian cat from the ancestral African wildcat.

3.3.3 Peppered Moths For centuries, the peppered moth flourished in England. The majority of individuals in this moth population were white with a dusting of dark spots (a “peppered” phenotype), but a small percentage were dark in color. This asymmetrical distribution of color in moth populations arose because when moths possessing the peppered phenotype rested on the bark of white birch trees, they were virtually invisible to birds, while the dark moths were easily spotted and eaten (Figure 3.11). However, with the onset of the Industrial Revolution, the smoke and soot from the new and increasingly abundant factories inundated the environment, and

Figure 3.10  The pug (and all domestic dogs) is a product of many years of selective breeding starting from the wolf. (Pug courtesy of Abuk SABUK,

https://commons.wikimedia.org/wiki/ File:Fawn_pug_2.5 year-old.jpg; wolf courtesy of Mas3cf, https://commons. wikimedia.org/wiki/File:Eurasian_wolf.jpg.)

63

64

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms? Figure 3.11  Illustration showing the evolution of industrial melanism in the peppered moth. Before the industrial

revolution, the lighter varieties were better camouflaged against the light birch trees, left. When industrial soot darkened the trees, the lighter moths became easier to spot by birds preying on the moths. (Courtesy of Siyavula Education, https://flic. kr/p/mFV3wM.)

soon turned the bark of the birch trees dark. Suddenly, the white moths that had been so well-hidden stood out starkly against the soot-darkened bark and were an easy target for birds, while moths with the dark phenotype blended in. As a result, the dark phenotype became very abundant in the population for many years. Then, in the 1960s, England began a campaign to reduce industrial emissions. This was good for the environment—the birch bark gradually returned to its natural color—but bad for the dark moths, which once again became easy prey. Thus, the white phenotype again became predominant in the moth population, while the dark ones became increasingly rare. This is a classic example of a population undergoing selection in response to environmental change. Natural variants always existed (tenet one), but the changing environment determined which of these dominated (tenet four).

3.3.4 Drug Resistance Drug-resistant bacteria are a direct example of evolution that is of grave concern to society. Many different types of bacteria invade tissues of organisms, causing a variety of diseases. In fact, you are constantly being colonized by different strains of bacteria. Since the development of antibiotics, we now routinely treat diseases caused by these invading bacteria with antibiotics, and chances are that you have taken a course of antibiotics for an illness (e.g., strep throat, sinus infection, pneumonia). However, what can frequently happen is when people start to feel better, they stop taking their antibiotics too early. As a result, a small portion of that bacterial population can survive—the portion that is genetically predisposed to be antibiotic resistant. When not exposed to antibiotics, these resistant microbes are a minor portion of the population—barely detectable in the general population, but exposure to antibiotics gives them an advantage over the non-resistant ones, and they thrive when the drugs remove their competitors. When these survivors multiply and re-infect someone, the new population will be dominated by the resistant phenotype, and the medication will not be as effective at stopping the progression of illness. The evolutionary response of these microbes to antibiotics is a large and growing problem in human populations.

3.3.5 Human Diversity Human diversity also testifies to evolution. Both the fossil record and genetic analyses show that the human lineage began in Africa. Geographically close to the equator, our ancestors experienced strong sunlight for 12 hours a day, favoring dark pigments (melanin) in the skin to protect DNA in cells from ultraviolet radiation, particularly as they lost

3.4  Drivers of Evolution: Variation and Selection

the body hair covering once shared with their simian relatives. When some human populations moved out of Africa toward more northern climates, these same pigments were no longer needed for solar protection, and in fact prevented these populations from using the shorter hours of weaker sunlight to produce needed vitamin D. Through selection, these northern populations lost melanin pigmentation, producing paler skin. Thus, the human species today has a wide range of skin tones, all the result of different environmental conditions experienced by ancestral populations.

3.4 DRIVERS OF EVOLUTION: VARIATION AND SELECTION After reading this section you should be able to… • Describe the two primary sources of genetic variation in populations.

Now that we’ve established what evolution is, and provided evidence that it occurs, it’s time to dig a little more deeply into how the process works to shape populations (including dinosaur populations) over time.

3.4.1 Sources of Variation The first component required for evolution is genetic variation. There are two main ways in which genetic information can be altered and subsequently passed to the next generation.

3.4.1.1 Sexual Recombination During sexual reproduction, genes contributed by each parent are rearranged in new combinations when the gametes (sperm and egg) are formed. The offspring gets traits from parents, but this shuffling means that those genes they inherit are not identical to those present in the parents. This is partly why children do not look like exact copies of either parent, and why siblings from the same set of parents aren’t identical— unless they are identical twins.

3.4.1.2 Genetic Mutation A genetic mutation is an alteration in an organism’s genetic code. This change can occur either because the DNA is copied incorrectly as cells divide or through damage caused by the environment (e.g., chemical exposure, radiation, or, in some cases, drug use). In either case, these can cause substitutions, insertions, or deletions of base pairs within the DNA strand. These errors can have differing levels of effect upon an organism’s phenotype. Some genetic mutations will have no observable effect on the organism’s phenotype, while others might produce small changes that don’t affect the ability of the organism to survive. Some, however, can result in substantial or even lethal changes. Mutations are only relevant to evolution if they are germline mutations— those that occur in reproductive cells (e.g., egg or sperm cells), because only in these cells is genetic information passed to the next generation. Conversely, somatic mutations, which occur in non-reproductive cells, aren’t heritable, so even though they can have profound effects on an organism (e.g., some cancers, like lung cancers, have been linked to somatic mutations induced by compounds in cigarette smoke), they aren’t relevant for evolution because they are not passed on to offspring. Once genetic variation is introduced to a population, whether from recombination or mutation, selective pressure may act upon it. These

65

66

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms?

variable traits may confer an advantage, a disadvantage, or a net neutral effect in terms of an organism’s ability to survive and produce offspring—the two ultimate drivers of all life. This selective pressure can come from a number of different sources. For this discussion, we will focus on selective pressure from the environment (i.e., natural selection) and mate selection (i.e., sexual selection).

3.4.2 Natural Selection Environmental factors play a dominant role in driving evolutionary change. Think about the environment as a filter for all the variation we discussed in the previous section. Environments change—through forces like plate tectonics, mountain building, or glaciation, and as they do, they put selective pressure on populations to adapt to these changes. Factors present in the environment (e.g., temperature, rainfall, food availability) act on the variations within a population, favoring some phenotypes, while making others less able to compete in that environment. For an example of adaptive change through natural selection, look at polar bears. Polar bears are known for their large size, fierce predation, and, of course, white fur (Figure 3.12). But genetic studies show that

Figure 3.12  Polar bears (A) and grizzly bears (B) are both subspecies of the brown bear. Occasionally they will cross

paths in the wild and mate, producing a pizzly bear (C). Polar bears are a great example of adaptive selective. (A and B courtesy of K. Tiffany; C courtesy of Stefan David, https://flic.kr/p/c8pL99.)

3.5  Speciation, Microevolution, and Macroevolution

polar bears are a relative newcomer to the bear family, and are actually a subspecies of the brown bear, to which grizzly bears also belong. Even though they look very different and inhabit different territories, occasionally, their paths cross and they potentially mate, resulting in “pizzlies” (a hybrid between grizzly and polar bears). This reproductive connection makes them, by definition, members of the same biological species. Polar bears emerged through isolation of habitat caused by the massive glaciers of the Pleistocene, and only those with evolutionary advantages, including ideal coat color and thickness (as well as other advantageous traits, like larger body size) survived and produced offspring. As the glaciers advanced and bear populations adapted to live above the arctic circle, they experienced long periods of darkness, making it important for them to capitalize on what solar energy they could for warmth. So, although the ancestral Alaskan brown bear population has brown fur and dark skin, polar bear skin is very black, but covered by hair that is translucent (it appears white because it scatters sunlight). This translucent fur over black skin allows them to absorb heat from infrared radiation while simultaneously camouflaging them in ice and snow. Polar bear hairs also have a hollow core, which makes them a great insulator. Together, these traits allow polar bears to lose almost no heat to the environment.

3.5 SPECIATION, MICROEVOLUTION, AND MACROEVOLUTION After reading this section you should be able to… • Distinguish between microevolution, speciation, and macroevolution. • Describe two examples of macroevolution.

So far, we've mostly talked about examples of microevolution—small changes that help an organism within a population survive and change, but which haven’t yet produced another (reproductively isolated) species. Right away then, you can see how difficult it is to recognize with certainty a dinosaur species—two fossil organisms sharing a lot, but not all, of the same traits, might indeed be different species. But they might also be adult and immature forms of the same species, or even male and female from the same species. From the vantage point of 65 million years in the future, we can’t exactly determine whether two extinct organisms could interbreed, let alone whether their offspring would be fertile, and without this information, it is impossible to determine with certainty that they are members of the same species, using the biological definition of species. Speciation occurs when one species gives rise to a different species over time. This usually results from populations of the same species becoming reproductively isolated. For example, when a major and permanent barrier is placed between groups so they can no longer interact—like a mountain range or an ocean. This is called allopatric speciation—meaning “different lands”. But speciation can also occur without these large barriers, and can be driven by the need to reduce competition—when some individuals of a population begin to specialize in night-time feeding, while the rest eat during the day, eventually resulting in differing adaptations. This is referred to as sympatric speciation—the ranges still overlap, but they are isolated by time in this example. When populations of the same starting species are isolated, evolutionary change can

67

68

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms? Figure 3.13  Reconstruction showing the arrangement of continents during the Early Jurassic (top) and the Late Jurassic (bottom). (Reprinted with

permission from Chris Scotese.)

occur rapidly. What is evidence for this? Figure 3.13 shows the world and continental positions in the early and late Jurassic, a time when we see major changes in dinosaur populations and the origin of many new groups. At the beginning of the Jurassic, the continents were just beginning to break apart. Dinosaurs from this time period are overall fairly similar. All large sauropods (Chapter 10) look pretty much the same, and the meat-eaters likewise share many features, even though they were found geographically distant from one another. But, as the continents continued to drift and became separated by new oceans, the dinosaur populations became reproductively isolated from one another and began to differentiate. This is true today as well. Regions of the planet that have been isolated a long time, like Australia, New Zealand, and Madagascar, have animals and plants not found anywhere else on the planet. Probably the most well-known examples of speciation were recorded by Darwin himself, during his famous travels on the HMS Beagle to the Galapagos. This series of islands off the west coast of South America are very isolated, both from mainland South America and from other islands; hence the animals that are found on each island are unique. Even though the islands are relatively close together and straddle the equator, the climate on each is quite different, with different types of plants, different aridity, topography, and other factors. Darwin noted that finches, small birds that are widespread on continental South America, were also found on each of the Galapagos islands, but they differed greatly from each other, depending on which island they made their home. What happened? The environmental conditions on each island dictate which plants are found there. On some islands are nutritious nuts within hard shells available for the finches to eat; on other islands, grasses and grains dominate. On another island, the finches have access to small seeds, and on still others are plentiful insect populations. Over time, the birds on each island have acquired very distinctive beaks with features that make them more efficient at eating their particular food. It is easy to see

3.5  Speciation, Microevolution, and Macroevolution Figure 3.14  Image showing the variation in beaks among four finches found on the different Galapagos islands. (Courtesy of John Gould, public

domain.)

that beaks that break open hard nuts must be very different than beaks that probe for beetles in trees, and indeed, that is reflected in the shapes of the finch beaks (Figure 3.14).

3.5.1 Microevolution vs. Macroevolution The finches above are an example of microevolution, which refers to small-scale changes (relatively speaking) occurring over a relatively short amount of time—i.e., tens of generations and thousands of years in vertebrates (much faster in insects, and faster still in microbes which have shorter generation times). But how much change could occur if those small variations continued to accumulate over much longer periods of time? Thousands of generations? Millions and millions of years? Mutations accumulate incrementally over time; thus, the more time since two species diverged, the greater the change. When genetic and morphological changes accumulate over long time periods, a population can be totally unrecognizable from its precursor species. For example, genetic and morphological evidence strongly supports whales having their origins in a group of artiodactyls (even-toed ungulates, like deer) called Pakicetus (Figure 3.15). Fossils of Pakicetus superficially resemble deer more than they do whales as we know them today. Yet, their genetic make-up still reflects this ancestry, despite the great variation in form. Thus, macroevolution is simply microevolution, but extended

Figure 3.15  Pakicetus was amphibious and considered to be the earliest whale. (Courtesy of Kevin Guertin, https://

commons.wikimedia.org/wiki/File:Pakicetus_ Canada.jpg.)

69

70

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms?

out to a very, very long time scale, and the connection between these “small-scale” changes and major shifts is not often observable over the course of a lab experiment, a human lifetime, or even the course of human history. Macroevolution is change beyond the species level. Macroevolution posits that all of the diversity of life on this planet results from evolutionary changes that have accumulated from the starting point of a single ancestor, which in turn gave rise to all other living species; in other words, all life on this planet arose from a single common ancestor. Here, we limit this discussion to vertebrates, because that is a shared feature of dinosaurs (our favorite critter) and us (with whom we are most familiar). Now, on the surface, that basically says that you and a tree and a snake and a parrot all have an ancestor in common a very, very long time ago. But you don’t have a whole lot of features in common with a tree, really. So what is the evidence for this common ancestry? You may have heard some people claim that the theory of evolution has a gap in it: that there are no “transitional species” that look like a cross between the ancestor and the living descendant. But when you think about it, every species is transitional, because mutations accumulate incrementally, and evolution has no end goal that organisms are transitioning toward. Every offspring looks slightly different or has slightly different features than its parent. We just have too short a lifetime to observe and follow these changes over millennia. So how do we track these changes? We can see a host of evolutionary transitions in the fossil record. The first fossil we recognize as a bird is almost indistinguishable from a closely related dinosaur found in the same quarry. It was only after this fossil was carefully prepared, and faint impressions of feathers were seen in the sediments, that it was placed within birds (Figure 3.16). Archaeopteryx is perhaps one of the most well-known transitional fossils. In addition to feathers, Archaeopteryx had another bird-like feature, a furcula (i.e., wishbone). But Archaeopteryx also had many reptile-like features, including three fingers with claws, a long bony tail, and teeth (which no modern birds possess). Archaeopteryx clearly represents a lineage of dinosaurs that were transitioning from reptile-like animals to modern birds.

Figure 3.16  The bird-like Archaeopteryx (A) is a famous transitional fossil that shares many characteristics with modern birds but also with reptile-like dinosaurs such as Compsognathus (B) that it lived alongside. (A courtesy of H. Raab, https://

commons.wikimedia.org/wiki/File:Arch​aeopt​ eryx_​litho​graph​ica_(​Berli​n_spe​cimen​).jpg​ ; B courtesy of H. Zell, https://commons. wikimedia.org/wiki/File:Compsognathus_ longipes_01.jpg.)

3.5  Speciation, Microevolution, and Macroevolution

Similarly, progressive changes of certain “transitional” features can also be tracked in the lineage leading to modern horses. The earliest members of this lineage were tiny, short-faced, forest‐dwelling browsers, about the size of a dog. So how did these become the large, fast, grassland animal so familiar to us today? The fossils of these horse species record gradual changes in the lineage over time. The animals not only increased in size, but the jaws became deeper and more robust, the face became more elongated, and their teeth developed high crowns with folded enamel and long, deep roots. Early fossil horses also had anywhere from three to five toes on each foot. But, over time, the fossils show that except for the middle toe, the bones of their feet became thinner and shorter, until eventually the toes didn’t even touch the ground. In today’s horses, these bones are only splinters, tightly adhered to the third metatarsal, or cannon bone. We can trace the stages between the small browser and modern horses, which in essence are walking around on one big toe for each foot (Figure 3.17). There isn’t just one straight line from the tiny multi-toed horses to today’s version, however. There were many side branches from the earliest equine ancestor, but these did not leave living descendants. In fact, among the many branches within this lineage, today there exists only one genus, Equus. All others are extinct, with no living descendants. Similarly, in the human lineage, there are many side branches from the first member of our genus, including Homo habilus, Homo erectus, Homo neanderthalensis, and Homo sapiens. Only one remains, and all humans, no matter where they live, are members of only one species---Homo sapiens. This branching nature of evolution is important because it provides a counter to the linear argument that chimpanzees can’t exist if humans evolved from them. It isn’t that humans evolved from chimpanzees, but more accurately that chimpanzees and humans branched off and evolved from a now extinct common ancestor. The fossil record has produced many beautiful examples of transition fossils, including Archaeopteryx, Pakicetus, which was a transition between terrestrial mammals and whales, and Tiktaalik, which had both fish-like and tetrapod-like (four-legged animals) features. These transitional fossils provide evidence for macroevolution or change beyond the species level. As more and more fossils are discovered, we will be able to build a more complete picture of the macroevolution of all species from our most recent common ancestor.

Figure 3.17  The transition of horse legs through time. Eohippus which lived

50 million years ago and was about the size of a medium dog is on the far right, and modern horses are on the far left. (Courtesy of K. Tiffany.)

71

72

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms?

3.6 THE PACE OF CHANGE: GRADUALISM VS. PUNCTUATED EQUILIBRIUM After reading this section you should be able to… • Compare two different models for the pace of evolution through time. • Define and give an example of co-evolution.

In addition to the origin of unique traits and subsequent radiation of lineages, another concept to be aware of is that evolution does not always occur at a constant rate. The rate, or pace, of evolution varies through time and within lineages. As Darwin envisioned it, evolution was a slow and steady process, which we now refer to as gradualism. It should be clear at this point how this would occur—small variations slowly accumulating over many generations, leading to slow but inevitable changes in populations over time. However, that doesn’t fully explain what we sometimes see in the fossil record. Instead, we see fossil lineages that exist for millions of years with hardly any observable changes in their morphology, followed by a series of rapid, almost instantaneous (geologically speaking) changes. This evolutionary mode, first described by Stephen J. Gould and Niles Eldredge, is referred to as punctuated equilibrium—long periods with little to no measurable change (stasis or equilibrium), punctuated by rapid change. These two evolutionary modes are illustrated in Figure 3.18. Both are supported by evidence in the fossil record. In the example above for horse evolution, we have a concise record of very well-preserved fossils, beginning with Eohippus (dawn horse), the short-faced, small, four-toed browser with low-crowned teeth in the Eocene (50 million years ago). As we move forward in time, Eohippus becomes rare, and then is not seen again, but instead, by the Oligocene (about 35 million years ago), we see Mesohippus, which is larger, with a longer face and expanded jaw, but still walking on four toes. Miohippus lived about 25–30 million years ago. One of its toes is greatly reduced, and though it retains three toes, its side toes begin to get small and thin, while the middle toe expands and gets more robust. In Parahippus, 20 million years ago, the side toes are very slender and cannot support weight. The face elongates, and the legs begin to show proportions more in line with a faster runner. Pliohippus, which lived about 6–12 million years ago, begins to show features of a modern horse, and although smaller and stocky, its limbs show the proportions of fast runners. The horse lineage, therefore, is a good example of gradualism.

Figure 3.18  Punctuated equilibrium (A) is the idea that there are long periods of no morphological change punctuated by rapid speciation. In phyletic gradualism (B), morphological variation is slowly changing populations until speciation events occur.

3.7  Evolution: Fact or Theory?

But, what about trilobites? This mysterious arthropod, somewhat reminiscent of a beetle, or better, a horseshoe crab, shows up very early in marine sediments of the Cambrian (485–540 million years ago). Exceptionally well-preserved trilobite fossils can be found in Cambrian sediments wherever they are distributed across our planet. It is not clear which organisms were their ancestors, but with their first appearance they are already widely diversified, and paleontologists have identified thousands of species over their ~250 million-year reign. They are a good example of punctuated evolution because they are already well defined as separate species with virtually no “intermediate” features. The truth is, how we interpret the pace of evolution can depend on a variety of factors, and there is evidence of both punctuated equilibrium and phyletic gradualism in the fossil record. But rates can vary based upon the species we observe, the mutation rate in a given species, the continuity of the fossil record, and the ability to recognize the effects of taphonomy and time averaging.

3.6.1 Co-Evolution Now, what happens to the pace of evolutionary change when very different lineages evolve together—especially ones that are in a predator-prey relationship? We often observe changes in both of these lineages that seem linked. They may lead to an increase and/or diversification of weaponry on one side (bigger claws or sharper teeth), and an increase and diversification of defense mechanisms (bony armor or camouflage) on the other. This is often referred to as an “evolutionary arms race”, or, more scientifically, co‐evolution. The pronghorn is an example of co-evolution. The pronghorn is one of the fastest living herbivores, and although it is often referred to as an antelope, it is not closely related to the “true” antelopes of the old world, rather its closest living relative is the giraffe! The pronghorn roams the plains of western North America, and is endemic to this continent, meaning that it originated there, as did horses. The American antelope is the fastest land mammal in the entire western hemisphere! Cheetahs can run up to 80 mph. They are significantly faster, and would probably not go hungry based on speed alone. On the north American continent today, pronghorn are preyed upon by cougars (40–50 mph), wolves (less than 40 mph), and coyotes (35–40 mph). Why does the antelope have to be so much faster than its most likely predator? When the pronghorn originated and radiated in the Pleistocene (2.5 million years ago), it shared its range with an active, but now extinct cat, called Miracinonyx, or the American cheetah, and its favorite food was…you guessed it, the pronghorn. This speedy predator pushed successive generations of pronghorns to run ever faster to avoid being eaten. But the pronghorn was also driving Miracinonyx to greater speeds, approximating those of the cheetah today. Miracinonyx went extinct only a few thousand years ago. Will the pronghorn slow down a bit now that this predator no longer threatens them?

3.7 EVOLUTION: FACT OR THEORY? After reading this section you should be able to… • Support or refute the statement “evolution is both scientific fact and theory”.

73

74

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms?

So, is evolution a fact, or a theory? The answer is “Both”. Evolution is a fact, in that evolution has occurred and left indisputable traces—ones we can still observe or, in some cases, manipulate for our own benefit. It is also a theory: a hypothesis that has been extremely well-supported, over hundreds of years of research, at multiple levels, from the molecular to morphological, and through a multitude of independent lines of evidence. Evolution by descent from a common ancestor is the simplest explanation for many diverse biological phenomena, and for the diversity of life on this planet. Recall Chapter 1, where we discussed the scientific method, and what it means to make a scientific statement. If evolution is a scientific statement, a hypothesis, or a theory (the strongest statement concerning “how” or “why” that science can make), it must be falsifiable. But scientific theories are well-supported and robust, and while new findings might lead to slight changes, the evidence for evolution is so strong that it is likely to not ever be falsified. In fact, no argument against evolution has been shown to hold up to scientific scrutiny, despite hundreds of years and many experiments attempting to do so. However, there are plenty of diverse phenomena for which evolution from a common ancestor is the simplest, most logical explanation. We list a few interesting examples below. Evidence for evolution includes (but is not limited to): • All organisms originate from a single cell: All life today, from a bacterium to a human baby, to a carrot, begins with a single cell. In the case of a bacteria or amoeba, these organisms remain as a single cell, just as we hypothesize for the origin of all life. However, you also started life as a single cell, a zygote fused from a sex cell, or gamete, from each of your parents that grew and divided into you. The recapitulation of all life from a single cell during ontogeny suggests that all life initially started this way—which would make sense if all life evolved from a single-celled common ancestor. • All life shares a large portion of their genetic code: With recent technological advances, we can now obtain the total sequence (the genome) of DNA of any living organism. For example, when we compare DNA sequences across species, we find that almost all multicellular animals, from simple sponges to human beings, have genes that code for the protein collagen. Collagen, regardless of the organism from which it derives, contains recognizable sequences and uniquely modified amino acids that are similar. Furthermore, collagen is organized the same way, as crosslinked fibers, and has the same function in all organisms that have the gene for collagen. But there are slight variations in some regions of the DNA sequence among organisms. These variations don’t affect protein function but allow us to compare groups at the level of genes. When we do, we find that some groups have more bases in common than others. The simplest explanation (remember parsimony?) is that those groups with the most DNA in common have an ancestor in common more recently than they do with other groups. • All life reads the same genetic code: The same DNA sequence can be read by any organism to produce the same proteins. This has been capitalized on by the pharmaceutical industry. We can identify the genes that code for a particular protein—say, insulin—and splice this human gene into a bacterium. As that bacterium divides into a population of bacteria, all individuals

3.8  What We Don’t Know

will also possess the spliced gene. As their DNA is read—transcribed into RNA and then translated into proteins—the human gene is also read, and the bacteria begin to produce human insulin which can be collected and administered to humans with faulty genes. Thus, as distantly related as humans and bacteria are, bacteria can read the code for human DNA, and be used to produce medicine that can save a life. The simplest explanation for this is that the code itself arose in a shared common ancestor. • Homologous structures: Homologous structures are those that are similar in position and/or structure because they have the same evolutionary origin (see Chapter 4, phylogenetics), but may not necessarily function in the same way. An example is the vertebrate forearm. All tetrapods have had, at one point in their lineage history, two forelimbs. And, in all these organisms, the limbs consist of one bone in the upper part of the arm (the humerus), and two in the lower (the radius and ulna). There’s a lot of variation in the hand/finger bones between a bird, a horse, a pterosaur, and you, but the number and position of the humerus, radius, and ulna remains the same, even though birds and horses use their arms very differently than you. This common structure is evidence that the ancestor of all tetrapods, way back in the Devonian, also had this pattern in its forelimbs. Looking even further back, this onebone, two-bone pattern is also found in the lobe-finned fish! The most parsimonious way to explain this pattern is that they all inherited these bones from a common ancestor. With all of this accumulated evidence for the theory of evolution, it stands as the strongest and most well-supported explanation of why we see such diversity among living and fossil organisms and explains how organisms have changed through time. Biologist Theodosius Dobzhansky wrote a famous essay titled “Nothing in Biology Makes Sense Except in Light of Evolution”, and the title itself is often used to illustrate the explanatory power of evolutionary theory. It is important then that we study dinosaur paleobiology in the light of evolutionary theory. As you read further, it will be impossible to answer many of the questions that dinosaurs elicit, like “how (or why) did they get so big?”, without considering them in the context of evolutionary theory.

3.8 WHAT WE DON’T KNOW 3.8.1 What Is the Pace of Evolutionary Change? One big area of research focus in evolutionary biology is determining the pace of speciation (and conversely extinction) among organisms. There are two primary methods that researchers use to better understand the rates of evolutionary change: 1) molecular data coupled with phylogenetics (Chapter 4) for extant organisms and 2) the fossil record. However, these two methods often produce different estimates. Questions to consider: • Can the two methods of estimating evolutionary rates be better integrated to improve our understanding of the pace of speciation and extinction? • What can be said about the evolutionary rates of groups with little to no fossil record (soft-bodied organisms)? • What can the rate of evolutionary change based on extant animals tell us about the completeness of the fossil record and what are the implications for dinosaur discoveries?

75

76

CHAPTER 3    How Do We Explain Variation among Past and Present Organisms?

CHAPTER ACKNOWLEDGMENTS We thank Adam Hartstone-Rose and Christopher Halweg for graciously reviewing this chapter. Adam is an Associate Professor of Biology and Chris is a Teaching Assistant Professor of Genetics, both at North Carolina State University.

INSTITUTIONAL RESOURCES Understanding Evolution. University of California Museum of Paleontology: http://evolution.berkeley.edu/

LITERATURE Silvestro, D., Warnock, R. C., Gavryushkina, A., and Stadler, T. (2018). Closing the gap between palaeontological and neontological speciation and extinction rate estimates. Nature Communications, 9(1), 1–14.

Marshall, C. R. (2017). Five palaeobiological laws needed to understand the evolution of the living biota. Nature Ecology & Evolution, 1(6), 1–6.

4 4

HOW DO WE KNOW WHO IS RELATED TO WHOM? SYSTEMATICS AND PHYLOGENETIC RELATIONSHIPS

O

ne of the idiosyncrasies of being human is that we love to classify and group things. We classify everything from music (e.g., jazz, rock, classical) to shoes (e.g., sneakers, dress shoes, sandals) to cars (e.g., sedan, wagon, convertible). This is a good thing because it makes it easier to communicate about and compare things in a more precise way. Scientists, of course, tend to classify things much more extensively and specifically than some of the casual ways a non-scientist might group them. For example, biologists group animals based upon morphological and genetic features they have in common, geologists group rocks based on their texture, how they were formed, and the minerals that comprise them, and chemists group molecules based on their elemental composition and the types of bonds holding them together. For scientists, the criteria used for classification is crucial in forming groups that are meaningful. Let’s say that you were asked to put three dinosaurs, Triceratops, Tyrannosaurus rex, and Apatosaurus, into two groups. How would you group them? You might put Triceratops and Apatosaurus in the same group, because overall they seem to have more features in common with each other (e.g., quadrupedal, herbivorous) than either does with T. rex. However, as we will see later in this chapter, grouping them this way does not accurately reflect how these three dinosaurs are evolutionarily related to one another. (Hint: Apatosaurus is more closely related to T. rex than Triceratops!) In this chapter, we will discuss some of the rules that biologists have used to group organisms, and how our current set of rules—a method known as phylogenetics—allows for evolutionary relationships to be discerned.

IN THIS CHAPTER . . . 4.1 WHAT’S IN A NAME? TAXONOMIC CLASSIFICATION 4.2 GROUPING CRITERIA: SIMILARITY VS. RELATEDNESS 4.3 “GROWING” A TREE: CLADES AND CLADISTICS 4.4 PHYLOGENETICS, IN SUMMATION 4.5 WHAT WE DON’T KNOW

78

CHAPTER 4    How Do We Know Who Is Related to Whom?

4.1 WHAT’S IN A NAME? TAXONOMIC CLASSIFICATION After reading this section you should be able to… • List the taxonomic rankings in the correct hierarchical order. • Define and give an example of binomial nomenclature.

Look at the animal pictured in Figure 4.1. What do you call this animal? Populations of this species of large cat live all the way from Canada to the very tip of South America, and the people that live across that wide expanse of Earth have many different names for it: mountain lion, panther, puma, cougar, catamount, even mountain screamer—and these are only some of the names applied to members of this one species alone. This causes a serious issue for scientific investigation—if some researchers only know this animal as a cougar, and others only know it as a puma, and still others only know it as a mountain lion, the biological and ecological research published on this animal will be confusing, misleading, and incorrect. The words we use in scientific discourse must be precise and universal. Scientists use a standardized system of measurement for research to ensure all data are quantified and reported in a comparable way (i.e., the metric system or the International System of Units [SI]). Similarly, we must have a standardized way to identify and discuss animal species, so that all researchers are using the same terminology, whether in China, Uganda, Guatemala, or the United States. Thus, taxonomy is the study of classifying and naming organisms in a standardized manner, providing a convention that all scientists everywhere use to talk about species or groups.

4.1.1 Traditional Taxonomy In the 1700s, Carl Linnaeus devised a hierarchical (ranked) system of biological classification to group animals, vegetables, and minerals into ordered groups. If you’ve ever played the game “Twenty Questions”, and wondered why the first question is commonly “Is it animal, vegetable, or mineral?”, this is where that tradition comes from! Obviously, the system is much different now than when Linnaeus first proposed it. For starters, “minerals” have no business in a biological classification scheme, and the way we decide how to place animals into groups is different than Linnaeus envisioned. Additionally, the number of hierarchical rankings

Figure 4.1  This animal is known alternatively as a cougar, a puma, and a mountain lion, among many other names. What problems might that cause

for scientific research into its biology and ecology? (Courtesy of National Park Service, https://commons.wikimedia.org/wiki/ File:Moun​tain_​Lion_​in_Gr​and_T​eton_​Natio​ nal_P​ark.j​pg.)

4.1  What’s in a Name?

(i.e., groups and subgroups) have changed and continue to change as we discover new species and new relationships between species. Although the way we understand and determine relationships has changed since Linnaeus’s day, his system still provides the backbone for the scientific naming conventions (or scientific nomenclature) used by researchers today. In grade school, you might have been taught a mnemonic similar to the following for classifying organisms: “King Phillip came over for good spaghetti”. This sentence is meant to help one remember the hierarchical rankings of the taxonomic classification system from the broadest (kingdom) to the narrowest and most specific (species): kingdom, phylum, class, order, family genus, species (Figure 4.2). Every organism classified by this taxonomic system receives a designation within each, successively more specific grouping. For example, to fully and uniquely classify Tyrannosaurus rex, you would have to rank it as: Animalia (kingdom), Chordata (phylum), Reptilia (class) Saurischia (order), Tyrannosauridae (family), Tyrannosaurus (genus), rex (species). Since this mnemonic was first popularized, however, scientists have added more rankings to this hierarchy as our understanding of life has changed. We now place an even broader group before kingdom (i.e., “domain”), and there are many subgroups that have been proposed to make divisions within the rankings more distinct (e.g., superorder, infraclass, subspecies). For example, a major grouping that Tyrannosaurus rex is a member of is the subphylum Vertebrata, which includes all animals with a backbone. For our purposes, it is not necessary to go into the nitty-gritty details of all the subgroupings—just keep in mind this basic hierarchy as we discuss different groups, and remember that, like all things in science, it is a system that changes and adapts the more we learn about life. Also, notice that within this classification system, all formal group names (except species) are capitalized. Thus, when we talk about the phylum Chordata, the clade Dinosauria, or the suborder Theropoda, it is clear we are talking about an entire group with specific features and including certain members. Conversely, “dinosaur” is an informal referral to any member or subset of members within Dinosauria. Tyrannosaurus rex is a dinosaur, but it is also a member of Dinosauria. Humans and dogs are mammals, and thus members of Mammalia. Additionally, the most general classification term one can use for an organism is a taxon (singular) or taxa (plural) for a group of different organisms. These are terms that refer to a species, genera, or any higher-level group of organ-

Figure 4.2  The taxonomic classification system, depicted as an inverse pyramid to show the progression of the hierarchical rankings from the broadest (Domain) to the most specific (Species). In this

example, the designations for a “mountain lion”, Puma concolor, is shown. (Adapted from artwork by A. Breen, https://commons. wikimedia.org/wiki/File:Taxonomic_Rank_ Graph.svg; Puma image courtesy of National Park Service, https://commons. wikimedia.org/wiki/File:Moun​tain_​Lion_​ in_Gr​and_T​eton_​Natio​nal_P​ark.j​pg.)

79

80

CHAPTER 4    How Do We Know Who Is Related to Whom?

isms, without implying any sort of ranking or grouping. Dinosauria is a taxon, but so is Tyrannosauridae.

4.1.2 Binomial Nomenclature But how does this get us to a scientific name? One of the most enduring aspects of Linnaeus’s system is that every animal gets a unique name from the combination of its genus name and species name. This convention is called binomial nomenclature (bi = two, nomial = name). Using this combination, every species has a distinct name (a binomen) that can be used by all researchers to unambiguously refer to the same animal. The binomen for panthers/cougars/mountain lions is Puma concolor. The binomen for humans is Homo sapiens. Tyrannosaurus rex is the binomen for the iconic, two-fingered dinosaur that is familiar to most children. You may have noticed that Puma concolor, Homo sapiens, and Tyrannosaurus rex are written differently than the text around them. Binomial nomenclature is expressed in a specific style in written text, to unambiguously denote scientific names. The stylistic rules for expressing a species scientific name include: • The name is italicized: Tyrannosaurus rex, not Tyrannosaurus rex • The genus name is capitalized, and the species name is lower case: Tyrannosaurus rex, not Tyrannosaurus Rex, tyrannosaurus rex, or tyrannosaurus Rex. • The species name is never given by itself: Tyrannosaurs rex is never just “rex”, “Rex”, or “rex”. Both the genus and species name must always be used together. • After the first usage, the genus name can be abbreviated: if you’re writing a long text about Tyrannosaurus rex, after the first mention, you can abbreviate the name to T. rex. This abbreviation maintains the capitalization conventions and italics, and is always the first letter of the genus name followed by a period and a space—always T. rex, not T-rex, Trex, or T.rex. This is especially handy when you’re discussing many species within the same genus. For example, a manuscript that discusses the relationship between the hominid species Homo habilis, Homo erectus, Homo neanderthalensis, and Homo sapiens can more simply refer to H. habilis, H. erectus, H. neanderthalensis, and H. sapiens. But, right away, you know that these are members of the same genus, but different species. All humans alive today, no matter where they live or what features they possess, are all H. sapiens. Again, while the genus may be abbreviated, it can never be excluded. The genus name must always be used with the species name.

4.2 GROUPING CRITERIA: SIMILARITY VS. RELATEDNESS After reading this section you should be able to… • Explain how phenetic taxonomy and phylogenetics differ in their approach to classifying organisms. • Describe the difference between ancestral and derived traits. • Differentiate between analogous and homologous characters. • Interpret a phylogenetic tree using the appropriate terminology.

4.2  Grouping Criteria: Similarity vs. Relatedness

Now that we’ve established the naming conventions of the classification system we use, we can now discuss the rules by which we sort taxa into named groups. If you were given a list of animals and were told to sort them into groups, how would you go about it? Would you put together all the species that were the same size or color? Would you put all the animals with wings in one group and all the animals that walk on four legs in another? If you devise a method that looks at overall similarity of form, you run into a problem: the groupings you create do not reveal anything at all about how closely the animals in your groups are related to one another, their ancestry, or the evolutionary development of their traits. For example, birds and bats have wings, but one is a mammal and one is an archosaur, more closely related to alligators than to mammals. They are not closely related at all! Figure 4.3 shows pictures of four different animals. They all look superficially similar, and if you were categorizing animals based on their overall morphological similarity alone, you might group these four together, and posit that ichthyosaurs and dolphins were more closely related to each other than either was to a cow, or a lizard. However, these four animals are only very distantly related to one another. Ichthyosaurs and pliosaurs descend from a reptilian ancestor. Penguins have lost the ability to fly, but their highly modified feathers and long beaks testify to their avian ancestry. Because dolphins nurse their young and still have hair (e.g., eyelashes!), we know that their ancestor, which they share with whales, was a mammal. So, what’s going on here? How can animals that do not have a shared ancestor be so similar in appearance? In this case, the ancestors of each of these groups were terrestrial (land-based) animals that returned to the sea, requiring an obligate swimming lifestyle. The ocean is an environment with strong selective pressures dictated by the physics of fluid dynamics, and animals that swim for a living, no matter what their ancestry, tend to reduce their legs and streamline their body, to enable smoother and faster swimming. Thus, land animals that return to the sea converge upon the same body morph (shape), regardless of their ancestry, and to classify them according to overall similarity, and not ancestry, is not informative. Grouping animals by their overall similarities, without regard for their evolutionary history, is called phenetic taxonomy. Phenetic taxonomies often result in animals that are only distantly related being grouped together in ways that do not reflect actual relationships. Although this was a common approach to biological classification as late as the 1990s, beFigure 4.3  (A) Dolphin, (B) penguin, (C) artist depiction of Pliosaurus, and (D) an ichthyosaur. These four animals

seem to possess many morphological similarities, including flippers and a streamlined body. But do these similarities reflect how closely they are related to one another? (A courtesy of K. Tiffany, taken at the Brookfield Zoo, Chicago, IL; B courtesy of K. FUNAKOSHI https://commons. wikimedia.org/wiki/File:Pygo​sceli​s_pap​ ua_-N​agasa​ki_Pe​nguin​_Aqua​rium_​-swim​ ming_​under​water​-8a.j​pg; C courtesy of M. Lanzas, https​://up​load.​wikim​edia.​org/w​ ikipe​dia/c​ommon​s/4/4​a/Pli​osaur​us_re​stora​ tion_​2019.​jpg; D courtesy of H. Harder, https://commons.wikimedia.org/wiki/ File:Ichthyosaurus_h_harder.jpg.)

81

82

CHAPTER 4    How Do We Know Who Is Related to Whom?

cause of these limitations, it has largely been replaced by phylogenetic systematics (also called cladistics) in which defined groups (or clades) represent shared ancestry. Phylogenesis (phylo = tribe, genesis = origin) refers to the evolutionary development and diversification of species. Systematics is the science of classification and naming these new groups of organisms. Phylogenetic systematics (often referred to simply as “phylogenetics” by paleontologists), then, strives to reconstruct evolutionary relationships between taxa, using unique and shared characteristics (traits), with the ultimate goal of understanding their evolutionary histories.

Figure 4.4  (A) Basic phylogenetic tree, or cladogram, showing the relationship between monotremes, marsupials, and placentals, three groups of mammals. (B) The same tree highlighting the relationship between marsupials and placentals. These two

mammal groups are more closely related to each other than either are to monotremes because they share the synapomorphy of live birth—a derived trait they inherited from their most recent common ancestor (“Ancestor 2”). This synapomorphy unites them together in a more specific subgroup (or clade) within mammals, called Theria.

Characters can be ancestral (or basal), meaning they were inherited from an ancestor and unchanged, or derived, meaning they have been changed or newly acquired in the course of evolution. For example, look at the simple tree in Figure 4.4A which shows three groups within Mammalia. Hair is an ancestral character that all three groups inherited from an ancestor at the node labeled “Ancestor 1” (the nodes, or branching points, represent recent common ancestors, see Section 4.3). However, other traits inherited from “Ancestor 1” are not retained in all these groups. Monotremes lay eggs, as Ancestor 1 would have, but marsupials and placentals both give birth to living young—a change from the ancestral state. Live birth, then, is an example of a derived character for mammals, and a shared derived character for marsupials and placentals. Shared derived characters are characters that are exclusively shared among all members of a group, and are thus used to define that group, or clade. We call these shared derived characteristics synapomorphies (syn = shared, morpho = shape), and they represent a trait that was acquired in the most recent common ancestor shared by all members of the group that possess it. “All” is a particularly important word in these definitions. All members of the group must share the characteristic in order for that group to be a clade. We also call such a group a monophyletic group (mono = one, phylo = tribe) because it represents the related descendants of one recent common ancestor. If the character is not shared by all members of the group, then it cannot be a monophyletic group, and therefore cannot be a clade. In our example, marsupials and placentals share the synapomorphy of live birth, which they inherited from “Ancestor 2”, in which this change from the ancestral state of egg-laying first appeared. Together, marsu-

4.2  Grouping Criteria: Similarity vs. Relatedness

pials, placentals, and their common ancestor make up the clade Theria (Figure 4.4B), which is united by this derived character that all members of the group share. Because ancestral and derived are relative terms, whether a specific trait is considered ancestral or derived is entirely dependent on where you are at in a phylogenetic tree and which taxa you are comparing. In Figure 4.4, hair is an ancestral trait among mammals—monotremes, marsupials, and placentals all have it. As a character, it would not allow us to separate a platypus and a human into different groups; we needed the synapomorphy of live birth to do that. But what if we “zoomed out”, and compared the clade Mammalia to other groups of amniotes, such as lizards (squamates) and birds (avians) (Figure 4.5)? When considering all amniotes, the ancestral state is to not have hair. In this tree, hair is now a derived trait, and can be used to separate mammals from lizards and birds. Thus, hair is derived when considering the entire animal kingdom, but ancestral when only considering mammals. As discussed earlier in this section, taxa can sometimes share features that were independently acquired in each lineage rather than inherited from a common ancestor—for example, the flippers of all the animals shown in Figure 4.3. These superficially similar body shapes are an example of convergence—an instance where evolutionary pressures (e.g., the fluid dynamics of swimming) have caused four unrelated organisms to converge on a similar morphology. We call these analogous traits because, like a verbal analogy, they express a similarity between two things that are, in the end, not the same, because they did not derive from a shared ancestor. In cladistics, we call these homoplastic traits or homoplasies. Rather than shedding light on evolutionary relationships, homoplastic/analogous traits can obscure them if they are not recognized as convergence. This is why classifying organisms based on overall similarity, as in phenetic taxonomy, has fallen out of favor. It is not useful for revealing evolutionary relationships. Let’s return to our example of comparing mammals with lizards and birds. Figure 4.6 now shows the split between monotremes (like the platypus) and Theria within the mammal clade. The group Theria includes placentals, of which bats are a member. Bats have wings, as do birds, which are also shown in this tree. But if we follow the tree down from each group to their most recent common ancestor, “Ancestor 1”, we can see that this early amniote did not have wings. Thus, since birds and bats could not have inherited wings from their shared ancestor, they Figure 4.5  When mammals are placed on a broader phylogenetic tree that includes other amniotes, such as lizards and birds, hair becomes a derived trait. The ancestor (“Ancestor 1”)

shared by mammals, lizards, and birds, did not have hair. Thus, on this tree, it is not a basal (ancestral) trait, but a synapomorphy that was derived by the ancestor of all mammals.

83

84

CHAPTER 4    How Do We Know Who Is Related to Whom? Figure 4.6  In this expanded phylogenetic tree, we can see that although bats and birds both have wings, they did not inherit those wings from their most recent common ancestor, “Ancestor 1”, the ancestor of all amniotes—otherwise, we would see wings in many other amniotes as well. Instead, bats and birds evolved wings

independently of each other, making their wings a homoplastic (analogous) trait.

must have acquired them separately. Their similarity, which arose from convergence, is an analogous trait—a homoplasy. The term “homoplasy” is not to be confused with homology, which is another term for shared characteristics. The bones in the arms of birds, humans, bats, and other vertebrates (Figure 4.7), all derive from the same bones we inherited from a common ancestor. These bones represent Figure 4.7  Illustration of the bones in the forelimbs of various tetrapods.

Despite how very differently these animals use their arms—from wings, to flippers, to grasping hands—all of them are derived from the same bones. These bones, which were inherited from a common ancestor shared by all these animals, are homologous structures, or homologies. H = humerus, U = ulna, R = radius, C = carpals, M = metacarpals, P = phalanges. (Adapted from artwork by W. Leche, https:// commons.wikimedia.org/wiki/File:Arm_​skele​ ton_c​ompar​ative​_NF_0​102.5​-2.pn​g.)

4.2  Grouping Criteria: Similarity vs. Relatedness Figure 4.8  Wings of (A) a dragonfly, (B) a bird, and (C) a bat. Although

all of these wings enable the organism bearing them to fly, their structures are not derived from an ancestor shared by these animals but arose independently in each of them. Thus, these wings are examples of analogous structures, or homoplasies. (A and B courtesy of K. Tiffany. C courtesy of Salix, https://commons.wikimedia.org/wiki/ File:Bat-wing_underside.jpg.)

homologous structures. Conversely, although birds, bats, and dragonflies all have wings capable of powered flight (Figure 4.8), the wings are not derived from a single common ancestor. The insect wing (Figure 4.8A) is made of a chitin membrane that emerges from the thorax. Although bird and bat wings are comprised of the same, homologous bones (Figure 4.7), the arrangement and morphology of the bones and tissues that comprise the wings are different, and arise independently in these two taxa (Figure 4.8B,C)—they are not structures retained from a shared common ancestor. Thus, these wings are analogous structures, or homoplasies. Before we move on, let’s review and expand on our cladistic terminology: • Ancestral (basal) trait: A trait that has not changed from its inherited, ancestral state. In older texts, this may be called a primitive trait, but this terminology has been retired, as the word “primitive” incorrectly implies ancestral character states are more simplistic or less adaptive. An ancestral trait can also be called a plesiomorphy. • Derived trait: A trait that has changed from its inherited, ancestral state. A derived trait can also be called an apomorphy. • Synapomorphy: A derived trait that is exclusively shared by all members of a group (or clade), thus defining that group. • Clade: A group of taxa, defined by synapomorphies, which represents one ancestral taxon and all its descendants. A clade can also be called a monophyletic group.

85

86

CHAPTER 4    How Do We Know Who Is Related to Whom?

• Autapomorphy: A derived trait that is only present in one taxon, uniquely separating and defining it from all other groups or species in a cladistic analysis. • Homologous trait: A trait appearing in two or more taxa that has the same evolutionary origin, but which may have morphological differences because they have been adapted for different functions in derived members of the group (e.g., human arms, horse forelegs, and whale flippers). A homologous trait can also be referred to as a homologous structure or a homology. • Analogous trait: A trait that appears superficially similar in two taxa because it serves similar functions but has different evolutionary origins; they are the result of convergent evolution (e.g., bug wings and bird wings). An analogous trait can also be called analogous structures, homoplastic traits, homoplastic structures, or homoplasies.

4.3 “GROWING” A TREE: CLADES AND CLADISTICS After reading this section you should be able to… • Describe the process used to build a cladogram. • Use phylogenetic methods to construct a character matrix and build a simple cladogram.

We’ve established that the focus of phylogenetic studies is to determine evolutionary relationships between taxa, elucidated through their shared derived characteristics, or synapomorphies. But how do we use synapomorphies to build evolutionary hypotheses?

4.3.1 Reading a Cladogram In the above section, we discussed that phylogenetics uses synapomorphies to group taxa into clades, which express hypotheses of evolutionary relationships between the taxa within the clade. We can express these evolutionary relationships visually as branching “trees”, or cladograms. Cladograms are essentially diagrams of proposed clades within each other. As shown in Figure 4.9, these cladograms can be depicted in a variety of ways, with angled branches coming off a baseline (Figure  4.9A) or with squared branches nested within each other (Figure 4.9B). Whatever the artistic design, in all cases, one spatial relationship must remain the same: branches that are nested more closely together represent taxa that are more closely related to one another than they are to any taxa outside of the grouping. In other words, these taxa have an ancestor in common with each other more recently than they do with other groups. In the four examples of cladograms shown in Figure 4.9, all trees depict exactly the same relationships. In Figure 4.9A, following the branches leading from the taxa at D and E back to their source brings us to a node (marked by the red arrow) that indicates the most recent common ancestor of D and E, which proposes D and E are more closely related to each other than either are to the taxon represented by C. And if you follow the branch leading from the D–E node to where it connects with the branch leading from C, this point is another node (marked by the blue arrow), that indicates that the ancestor of D–E and C, are more closely related to each other than any of them are to the taxa at B, and thus C, D,

4.3  “Growing” A Tree: Clades and Cladistics Figure 4.9  Four different cladograms that depict the exact same relationship between five taxa, regardless of their artistic style or orientation. In all cases, the red arrow

indicates the same paired (sister group) relationship between taxa D and E. Similarly, in all cases, the blue arrow indicates the common ancestor of D, E, and C, which these taxa share in common more recently than any of them share an ancestor with B.

and E all form a group to the exclusion of B (and so on). In text, we could express the relationship between these taxa like this: (A(B(C(D,E)))). In Figure 4.9B, though depicted differently, we see the same pattern. The close relationship between D and E is represented by the horizontal line that connects their branches, and the branch leading away from it (marked by the red arrow) indicates their most recent common ancestor. The horizontal branch between this ancestor and the branch leading to taxon C indicates the C, D, and E group, which arose from a common ancestor at the branch marked by the blue arrow. The further out we move, the more and more distant the relationship is between the members comprising the groups. But even though it looks visually different from 4.9A, notice that in text we could still express this relationship as (A(B(C(D,E)))). Figures 4.9C and 4.9D depict these same relationships, however, in these diagrams, some of the branches have been “rotated” at their nodes. Although such rotations may create a tree that looks very different at first glance, the relationship it describes is the same. Try this: look at the palm of your left hand. From left to right, you see your thumb, index finger, middle finger, ring finger, and pinky. Now, turn your wrist and look at the back of your hand. From left you right, you now see your pinky, ring finger, middle finger, index finger, and thumb. When you turned your wrist, your hand did not change, and neither did the relative placement of your fingers. Your pinky is still the furthest away from your thumb, and your index finger and middle finger are still side by side. The internal relationship between your fingers did not change, even though your hand itself looks different from the other side. Now look at Figure 4.9B and imagine that every node you see is a wrist that can twist. If we twisted the node connected D and E (D,E) (red arrow), we would get (E,D). If we twisted the node connecting D and E with C, (C(D,E)) (blue arrow), we would get ((E,D)C). If twisted both those nodes at the same time, we would get ((D,E)C), which is what we see in Figure 4.9D. In all cases, the sister relationship between D and E is maintained. Look at Figure 4.9A. Which nodes were rotated to get 4.9C? Now we know how to read a cladogram, but how do we build one? The answer is a combination of identifying informative characteristics, determining the state of these characteristics in each taxon of interest (sort of like a binary computer language, either a 0 or a 1), and using brute computational force to mathematically calculate the most likely (i.e., the simplest) evolutionary path that would result in the observed pattern of these characters across all taxa.

87

88

CHAPTER 4    How Do We Know Who Is Related to Whom?

4.3.2 Identifying Characters First, we identify traits that will be used to compare taxa within a group of interest. It is important that the traits we select for this comparison be informative—that is, we want to make sure we’re using derived characters, and avoiding both convergent homoplasies and plesiomorphies (widespread ancestral traits). We discuss in detail above how homoplasies can interfere with determining evolutionary relationships, but why must plesiomorphies be avoided? If we include in our study a lot of traits that haven’t changed from their ancestral state in any of the taxa we’re examining, it tells us nothing about the relationships between each of the taxa. For example, if we are trying to determine the evolutionary relationship between humans, bears, cats, and cows, choosing characters like “has a spinal cord”, “has hair”, and “gives live birth” tells us nothing, because all four taxa share all of those features. Instead, we must choose characters for which some of these animals show a derived state. In extant taxa, we can look to an organism’s genetic code as a source of characters for comparison. Each base (e.g., A, C, G, C) in each position of a taxon’s DNA sequence can be compared as a separate character. Using DNA sequences to determine relationships is robust because DNA directly reflects inheritance and is thought to undergo far less convergence than morphological traits (although there is some controversy to this point). Molecular data are also an independent way to test phylogenetic relationships built upon morphological traits—morphology doesn’t always give the same cladogram as molecules do. However, for dinosaurs and other animals extinct millions of years, sequenceable DNA is usually long gone, and even protein sequences (which are far more durable) are largely degraded. Therefore, as paleontologists, we primarily rely on morphological features of the skeleton, as the shape and structure of the bone tissue is the part of vertebrates most likely to persist tens of millions of years. Thus, we choose features like, “the presence of an asymmetrical fourth trochanter on the femur”, “a perforated acetabulum”, or “the presence of a predentary bone” as characters of interest. Typically, characters are chosen that can be evaluated in a binary way, such as “present or absent”, “round or flat”, “notched or smooth”. Characters that have more than one discrete derived state can also be chosen, such as “presence of three, four, or five” fingers, though these can become a little more complicated in analyses (see below). Once we’ve identified these characters, we put them in a table (called a matrix) and “score” the state of the character for each taxon, where “0” means the taxon possesses the ancestral (basal) form of the trait, and “1” (or “2”) means the taxon possesses a derived form of the trait (Table 4.1). How do we know what the “ancestral state” of a character is? For that, we include an outgroup in our analyses—a taxon that has more ancestral traits than any of the taxa we are investigating. Remember that hair cannot be used to differentiate bears and humans, but it can differentiate either bears or humans from a lizard. In this case, the lizard would be the outgroup. From here, we use computer algorithms to determine which evolutionary path—which arrangement of branches in the cladogram—requires the fewest number of steps (changes from the 0 state to a 1) to arrive at the values in our character matrix. This is where choosing characters with more than one possible derived state becomes a bit more complicated. Do the characters coded as “2” represent one evolutionary step (0 → 2) or two (0 → 1 → 2)? This might not seem like a big difference, but it has important implications for our evolutionary hypotheses. In our earlier example of the character “has three, four, or five fingers”, are we hypothesizing that animals with three fingers went

4.3  “Growing” A Tree: Clades and Cladistics TABLE 4.1 SAMPLE CHARACTER MATRIX Outgroup Taxon

Taxon #1

Taxon #2

Taxon #3 Taxon #4

Trait #1 (0 = N, 1 = Y)

0

0

1

1

0

Trait #2 (0 = N, 1 = Y)

0

1

0

0

1

Trait #3 (0 = A, 1 = B, 2 = C)

0

0

0

1

2

Trait #4 (0 = N, 1 = Y)

0

1

1

1

1

Trait #5 (0 = Y, 1 = N)

0

0

0

1

1

A character matrix is a table of all the characters that have been identified for assessment, and the “state” of all those characters in each taxon of interest. Characters are typically described in such a way that they can either be assessed as “present” or “absent” for each taxon, which can be expressed as a “1” or a “0” on the table. Other character states that can be expressed simply, such as the presence of condition A, B, or C (e.g., the presence of three, four, or five fingers), can also be coded as “0”, “1”, or “2” on the table. In this example, the box in the matrix shaded grey indicates that Taxon #2 is scored as “1”, or yes/present, for Trait #4. Note that the outgroup is scored all “0”, representing the ancestral condition for all traits.

directly from having five fingers to three (one step), or that they first lost one finger, then another (two steps)? Ultimately, how to “count” such characters is complicated and largely dependent on the nature of the character itself. Thus, characters selected for phylogenetic analyses are usually binary, “0” or “1”. The arrangement of branches that requires the fewest number of evolutionary “steps” to form is considered the most likely to be correct, or most parsimonious. Remember, that doesn’t necessarily mean that it is the correct tree. The path of life can take an occasional twist and turn! However, in science, we always use the simplest explanation that fully explains all of the data. To illustrate how this process works, let’s do a quick and easy example. Let’s score a matrix to determine the evolutionary relationship of these three taxa, using a lizard as an outgroup (Figure 4.10). Take a look at these animals and remember that the lizard is the outgroup. What characters would you choose to include in your matrix? Four legs? Fur? Hooves? Claws? Retractable claws? Two eyes? Herbivory? A vertebral column? Ability to purr? Retractable claws? A long, narrow snout? Of the options above, “four legs”, “two eyes”, and “a vertebral column” are all plesiomorphies that are present in all the taxa, including the outgroup. Thus, they are of no help to us here. Instead, we must make sure we choose characters that are not present in all members of the group. In Table 4.2, we’ve listed 12 potential characters that are variably present in the listed taxa. For each character, we’ve scored the taxa with a “0” if they share the ancestral state of the feature with the lizard outFigure 4.10  (A) Cat, (B) dog, (C) cow, and (D) lizard. If you were trying

to determine the evolutionary relationship between the cat, dog, and cow using phylogenetics (and the lizard as the outgroup), what characters would you choose to evaluate? (Images courtesy of K. Tiffany.)

89

90

CHAPTER 4    How Do We Know Who Is Related to Whom? TABLE 4.2 CHARACTER MATRIX FOR TAXA SHOWN IN FIGURE 4.10 Characters

(Outgroup) Lizard

Dog

Cat

Cow

Fur (0 = N, 1 = Y)

0

1

1

1

Endothermic (0 = N, 1 = Y)

0

1

1

1

Herbivorous (0 = N, 1 = Y)

0

0

0

1

Retractable claws (0 = N, 1 = Y)

0

0

1

0

Hooves (0 = N, 1 = Y)

0

0

0

1

Enlarged canines (0 = N, 1 = Y)

0

1

1

0

Live birth (0 = N, 1 = Y)

0

1

1

1

Carnassial (shearing) teeth (0 = N, 1 = Y

0

1

1

0

Foot posture (0 = plantigrade, 1 = digitigrade, 2 = unguligrade)

0

1

1

2

Teeth in sockets (0 = N, 1 = Y)

0

1

1

1

Mammary glands (0 = N, 1 = Y)

0

1

1

1

Elongated muzzle (0 = N, 1 = Y)

0

1

0

0

For each of the 12 selected characters, the four taxa are scored as “0” if they match the outgroup, and “1” if they have a derived feature that doesn’t match the outgroup. In this example, there is also a character for which there might be two derived states, which are scored as either “1” or “2”. Note that the lizard scores all 0s. This should always be the case of the outgroup, since they polarize what is ancestral and what is derived.

group, and “1” if the feature is derived from what we observe in the outgroup. For example, the lizard gets a “0” for fur, since the ancestral state is to not have fur, and all other taxa get a “1” since they have evolved this feature. Right away you should notice that our outgroup, the lizard, is scored as all 0s. This should always be the case for an outgroup, because the outgroup is there to tell us what the ancestral states of all the traits are. You should also notice that, of the 12 characters, there are five that dogs, cats, and cows all share that lizards don’t: fur, endothermy, live birth, socketed teeth, and mammary glands. These are synapomorphies that distinguish Mammalia as a clade which includes cats, dogs, and cows. They don’t help us distinguish between cats, dogs, and cows, but they show us that these three taxa are more closely related to each other than any of them are to the lizard outgroup. To express visually in a phylogenetic tree would look like (Figure 4.11). Dogs, cats, and cows are grouped together in an unresolved clade (a polytomy) that excludes the outgroup, which is rooted at the bottom of the tree. This group is “unFigure 4.11  Cladogram showing the tree that can be built when only the five traits from our matrix that a dog, cat, and cow all share are considered.

These characters are all synapomorphies that group these mammals together, excluding the lizard outgroup, but none of them can help us determine evolutionary relationships between them, which is what we’re interested in. For that, we must include characters that do not have the same character states for all taxa of interest.

4.4  Phylogenetics, in Summation Figure 4.12  Cladogram showing a resolved evolutionary relationship between cats, dogs, and cows.

Using the characters in our matrix, cats and dogs share three derived features (synapomorphies) with each other, while the cow has three derived features unique to it (autapomorphies). This allows us to place cats and dogs into a group, showing that they are more closely related to each other than to cows.

resolved” because, when only considering these five traits, it’s not clear how these three taxa are related to one another—which two are more closely related than either are to the third. All that can be determined is that they are more closely related to each other than they are to the outgroup. Thus, when choosing characters for our matrix, it is important to avoid plesiomorphic characters (shared by everyone, including the outgroup) as well as make sure we include characters that aren’t shared by everyone except the outgroup. To resolve this polytomy, we need additional characters to guide us. Looking again at the matrix, we can see that cats and dogs share three derived features in common (digitigrade foot posture, carnassial teeth, and enlarged canines), while the cow has three derived features that are unique to it (autapomorphies) and are absent in both the cat and dog (herbivory, unguligrade foot posture, and hooves). The differences in scoring of these five characters make a very strong case that dogs and cats are more closely related to each other than either of them are to cows, and thus, we can group them together (Figure 4.12). Additionally, cats and dogs each have one autapomorphy that is unique to them, distinguishing them from each other—retractable claws and an elongated muzzle. In this very simple example, we were able to do the math in our head to figure out which taxa shared more features in common. However, real phylogenetic studies contain dozens of taxa and hundreds of characters, which are impossible for anyone to resolve by hand. For these, researchers use computer algorithms to determine mathematically the tree requiring the least number of evolutionary steps, as well as to calculate the statistical likelihood of its correctness—a process that can take days of computing time, depending on the speed of your processor!

4.4 PHYLOGENETICS, IN SUMMATION Phylogenetic systematics is a powerful tool for studying relationships and common ancestry. We will use systematic concepts throughout the rest of this text, placing new features that diagnose each dinosaur group on the dinosaur family tree. We will also utilize these concepts to make the most parsimonious inference about some aspects of dinosaurs that we don’t currently know, using a technique called extant phylogenetic bracketing (EPB). In EPB, we look at living relatives of the extinct animal (including some relatives that are more basal (have more ancestral traits), and some that are more derived than the animal of interest) to reconstruct a feature of dinosaurs for which we don’t currently have fossil data to inform our understanding. For example, let us ask the following

91

92

CHAPTER 4    How Do We Know Who Is Related to Whom?

question: how many chambers did Tyrannosaurus rex hearts have? Two? Four? Five? Soft-tissue fossils are rare, and organs are even rarer. Only one possible fossilized dinosaur heart has been described, and CT scans of this structure suggest it is a geologic concretion, not an organ. In the absence of direct fossil evidence, how do we build and test our hypotheses about dinosaur paleobiology if we don’t have such basic physiological information? The EPB can help us answer, or at least identify the most likely answer, for this question. The group Dinosauria is alive and well today in the form of extant birds (Aves), thus, members of Aves are extant, more derived relatives of the extinct dinosaurs. Conversely, dinosaurs and crocodiles share a common, ancestral archosaur relative in common; thus, living alligators and crocodiles are a more distant, ancestral relative of dinosaurs. When this relationship is depicted on a tree (Figure 4.13A), notice that crocodiles and birds—two extant taxa— “bracket” T. rex on this phylogenetic tree. Hence, we have made an “extant phylogenetic bracket”. Now, how do we use it? Let’s ask our question about heart chambers of the extant taxa. We know that crocodiles have a four-chambered heart. We also know that birds have a four-chambered heart. This means that a four-chambered heart is a feature that was both ancestral to dinosaurs (because their basal relatives have it) and that has been retained in their more derived relatives (because birds, the most derived dinosaurs, still have it). Thus, because the taxa on either side of dinosaurs all have four-chambered hearts, it is likely T. rex did as well. However, what if we ask did Triceratops have feathers? This time, we see on the bracket that one of the extant relatives (the birds) have feathers, but the other does not (Figure 4.13B). In this case, the EPB doesn’t give us very clear insight. If both relatives had feathers, or if neither of them did, we could infer that condition in Triceratops. However, since only one of them possess feathers, all the EPB can tell us is that feathers arose at some point in the dinosaur lineage—but not the exact point and whether Triceratops is included. Thus, inferences made using the EPB are the most robust when both extant bracket taxa share the features. The application of phylogenetic principles has rewritten the way we do paleontology, but also how we do all biology. It is the fundamental basis for comparing DNA strands to determine relatedness. It is fundamental to how we develop drugs to fight particular illnesses, and it allows us to trace when new traits were acquired in lineages, even across geologic time.

Figure 4.13  Extant phylogenetic bracket of (A) Tyrannosaurus rex and (B) Triceratops. In both cases, the extinct

dinosaur is bracketed by extant living taxa— crocodiles, to which they are more distantly related by a basal archosaur common ancestor, and birds, which are more derived members of the group Dinosauria. In A, we see that because crocodiles and birds both have four-chambered hearts, it is likely that T. rex did as well. However, in B, we see that because crocodiles do not have feathers, but birds do, it is impossible to tell using EPB alone whether Triceratops had feathers.

4.5  What We Don’t Know

More importantly, phylogenetic studies allow us to make predictions. For example, suppose we test every single living organism on the planet, and we find that, to one degree or another, all life has a small compound called a porphyrin, and that compound has an iron atom. Iron is a very toxic element, and it destroys proteins and DNA and tissues. So, the presence of this iron trapper in all life forms, from the simplest bacterium to humans, makes it a plesiomorphic trait. It also implies that it was present in the common ancestor of all life. Now, suppose you have been granted a billion dollars in research money to search for evidence of life on Mars. Would you look for a target protein like collagen, that makes up bones and tissues that aren’t present outside of Animalia? Or would you target porphyrin, a molecule present at the very root of the tree of life? That is how we use phylogenetics to generate testable hypotheses of evolutionary relationships. If porphyrin is present in all life on Earth, and if life on Mars and life on Earth share a common ancestor through planetary seeding (see Chapter 5), that might be a component they have in common. Another example that might be more relevant to your everyday life involves medicine. Suppose you thought you had developed a medical cure for cancer, a simple pill one could take that would destroy all tumors. But the ingredients in this drug are, when separate from each other, very toxic to vertebrate organs. How, then, would you test this drug to ensure that it is safe? How would you determine who to test it on? Would you propose starting your tests immediately on humans? Or could you start out by testing it on bacteria like Escherichia coli? Because bacteria don’t get tumors, testing on them probably wouldn’t be very useful. Instead, you might want to begin your tests with a mouse. Why? Why do we tend to use mice for our medical research, and not fish or a lizard? Because they’re mammals, like we are, and share more features with us—the ultimate recipient of the drugs—than fish or lizards. This is how we use phylogeny directly in drug design—it rests on the concepts of shared derived traits!

4.5 WHAT WE DON’T KNOW Although phylogenetics is a powerful tool for classifying organisms and understanding evolutionary relationships, there are some uncertainties that come along with its use.

4.5.1 What Is the Correct Number of Characters to Use to Be Sure We Have Arrived at the Most Parsimonious Evolutionary Relationship? The number of characters needed to be confident that we have identified the most likely evolutionary relationship among groups varies between different analyses, based on factors like how many taxa are being evaluated and how distantly or closely related they are (e.g., different species of bears vs. different species of mammals). It may not be possible to ever answer the question of how many are “enough”. How confident is “confident enough?” In the past, the answer to this question was largely based on the limits of computer processing capabilities. However, as we move forward, processing large data sets are less of an obstacle. In addition to how many, there is also the question of which characters to use. Two scientists could derive different relationships for the same taxa if they use very different characters, or even if they use the same characters but interpret the character states for a species differently (see Chapter 7 “What We Don’t Know” for an example of different phylogenetic interpretations in the grouping of dinosaurs).

93

94

CHAPTER 4    How Do We Know Who Is Related to Whom?

Questions to consider: • What limitations does the fossil record put on the number and types of characters we can use to reveal phylogenetic relationships? How might those limits affect our ability to be confident in our hypotheses of evolutionary relationships between long-extinct taxa? • How does a phylogenetic tree based solely upon morphological characters (as is usually the case for fossils) differ in robustness and rigor from one that can combine molecular and morphological data? • How might qualitative morphological characters (i.e., characters that describe shape or texture) affect the robustness of an analysis versus morphological characters that are more quantifiable or absolute? How might that affect your choices for characters when constructing a matrix for extinct taxa? • In what specific ways might taphonomy (see Chapter 11) affect the interpretation of morphological characters in fossil taxa?

4.5.2 What Does It Mean When Phylogenetic Relationships Based on Morphology Differ from Those Based on Molecular Evidence? For more recent organisms, molecular material (DNA) is often used to construct phylogenetic relationships. But what does it mean when this produces a different cladogram than the traditional use of morphological characters? Does this necessarily imply that one type of data has a bias or limitation that makes it less reliable, or that the way we code characters or DNA sequences needs to be modified? Questions to consider: • As the fields of ancient DNA and molecular paleontology progress, and more and more biomolecules are recovered from extinct organisms, how might this impact currently established phylogenetic relationships? • What are the challenges of using molecular characters for extinct organisms?

CHAPTER ACKNOWLEDGMENTS We thank Dr. Steven Jasinski for his gracious review and suggested improvements to this chapter. Dr. Jasinski is the Curator of Paleontology and Geology at the State Museum of Pennsylvania.

INSTITUTIONAL RESOURCES The History of Life: Looking at the Patterns from UC Berkeley: https​: //ev​oluti​on.be​ rkele​y.edu​/evol​ibrar ​y/art​icle/​0 _0_0​/evo_​03 Reading a Phylogenetic Tree: The Meaning of Monophyletic Groups from Scitable by Nature Education. https​: //ww ​w.nat​ure.c​om/sc​itabl​e /top​icpag​e /rea​ding-​a -phy​logen​etic-​tree-​the-m​ eanin​g-of- ​41956​/

4.5  What We Don’t Know

LITERATURE Baum, D. A., and Smith, S. D. (2013). Tree Thinking: An Introduction to Phylogenetic Biology. Roberts, Greenwood Village, CO, pp. 399–403. Gregory, T. R. (2008). Understanding evolutionary trees. Evolution: Education and Outreach, 1(2), 121. Meisel, R. P. (2010). Teaching tree-thinking to undergraduate biology students. Evolution: Education and Outreach, 3(4), 621–628.

Novick, L. R., Catley, K. M., and Schreiber, E. G. (2012). Understanding evolutionary history: An introduction to tree thinking. https​: //qu​beshu​b.org ​/coll​ectio​ns/po​s t/89​1/dow​nload ​/ Tree ​-thin​ king_ ​bookl​et_8-​12.pd​f

95

5 5

HOW DO WE KNOW WHEN AND HOW LIFE BEGAN AND EVOLVED? THE ORIGIN OF LIFE AND EVOLUTION THROUGH TIME

F

or over half of the entire history of our 4.6 billion-year-old planet, the only living things around were very simple, single-celled organisms more similar in size and shape to bacteria than to you. In fact, the nucleus that separates the genetic programming (i.e., its DNA) of an organism from its cellular activities (e.g., building proteins, metabolism) didn’t appear until almost 2 billion years after life began in the form of these very simple organisms. The advent of a nucleus was a major innovation in life history, allowing major advances in the chemistry of life. But then it took another 1 billion years—or more—before we see fossil evidence of the first multicellular organisms around 600 million years ago. So, for almost 3 billion of the ~4.6 billion years of Earth history, you would need a microscope to see life at all (Figure 5.1). In order to understand how dinosaurs got here, we must start from the very beginning of life on Earth and walk through its evolution over geologic time until we arrive at the reign of the dinosaurs. Only by putting dinosaurs in the context of all other living organisms can we begin to understand them.

5.1 DEFINING LIFE After reading this section you should be able to… • Write a concise definition of life.

How did life begin, and why did it become increasingly complex? To discuss these questions, we first need to define what we mean by “life”.

IN THIS CHAPTER . . . 5.1 DEFINING LIFE 5.2 GETTING STARTED: HYPOTHESES FOR THE ORIGIN OF THE FIRST LIFE 5.3 WRITTEN IN STONE: EVIDENCE FOR EARLY LIFE 5.4 LIFE THROUGH TIME: FROM EARLY MULTICELLULAR LIFE TO THE TIME OF THE DINOSAURS 5.5 THE MESOZOIC ERA: AGE OF THE DINOSAURS 5.6 WHAT WE DON’T KNOW

98

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

Figure 5.1  Timeline of Earth’s history showing the four eras of geologic time along with some of the major milestones in the evolution of life.

Based on living organisms that we can observe today, we know that everything “alive” exhibits all the following traits: • Incorporates all four classes of macro-biomolecules: (1) DNA (nucleic acids), which carries the genetic “blueprint”; (2) proteins, which can be structural (like collagen) or functional (like enzymes); (3) lipids, which store energy and make up cell membranes; and (4) carbohydrates, which also can be structural (cellulose or lignins of plants) or provide energy (glucose in our cells). From the smallest bacterium to the largest whale, all living things contain all four molecular components—and so dinosaurs must have as well. • Be composed of cells: All living organisms are composed of cells, which are lipid membranes that contain all the biomolecules listed above. They are essentially the smallest functional unit of life. • Consume: They must take in nutrients or energy (e.g., plants using the sun to photosynthesize) from the environment. • Metabolize: Metabolism is the sum of chemical reactions needed to break nutrients down to their smallest building blocks, plus those reactions that use those building blocks to build new tissues for growth, repair, or reproduction. • Expel waste: They must get rid of the waste products generated by metabolic processes. • Reproduce: They must pass on some or all of their genetic information to the next generation. In the case of sexual reproduction, the offspring always differ slightly from their parents. • Grow: In microbes, growth and reproduction can be virtually synonymous; the simplest bacteria grow little in size, but they divide and the colony grows. However, for all multicellular organisms, growth and reproduction differ. • Respond to stimuli: This can be as simple as plants turning toward a light source, microbes responding to chemicals of decay, or the avoidance of noxious compounds or heat. Right away you should see a problem when trying to apply these parameters to extinct life, which only exists now as fossils—these processes are no longer being carried out! We cannot measure the metabolic rates of a dinosaur or watch them eat or reproduce. So how do we know that they were once living? Although these traits constrain our definition of life today, would all of them have to have been met when life was just beginning on the primitive Earth? Could a simpler, or even different, form of life exist, perhaps beyond Earth, that does not display all the above criteria? Because of these questions and others, attempts to define life have been met with much debate and controversy. Some scientists have further refined the definition of life to simply state that it is a system capable of sustaining itself, while undergoing processes of natural selection and

5.2  Getting Started: Hypotheses for the Origin of the First Life

possessing variations that can confer advantages. The National Aeronautical and Space Administration (NASA), which is concerned with detecting life beyond Earth, simplifies even further: “Life is a self-sustaining chemical system capable of Darwinian evolution”. Just as life beyond Earth may not exhibit all the above characteristics, it is likely that the earliest life on Earth did not either. Some hypotheses propose that life started out as single strands of RNA that were capable of self-replication. Whether such self-replicating RNA strands would be considered life or just biomolecules, is largely dependent on the definition of life used. Another good example of this problem is viruses, which some scientists consider to be living because they have genetic material (either DNA or RNA, but not both as in all other life forms), reproduce, and evolve. However, they do not have cells, they don’t metabolize, and they can’t reproduce independently without a host.

5.2 GETTING STARTED: HYPOTHESES FOR THE ORIGIN OF THE FIRST LIFE After reading this section you should be able to… • Briefly describe the steps that would be necessary for life to originate. • Explain three possible places that life may have originated.

The question of how life originated involves understanding abiotic processes that can lead to the formation of molecules necessary for the first lifeform. Understanding the early conditions of Earth can help us answer “where?” life may have originated by giving us clues as to the types of settings that would have been favorable for the chemical reactions necessary to build organic molecules. While the scientific questions of how and where life started are inextricably linked, we will explore each separately in this section.

5.2.1 How the First Life Began We may never know for certain how life began, but that doesn’t stop us from putting forth testable hypotheses. As mentioned in Section 5.1, one hypothesis suggests that the first life was probably some type of simple, self-replicating RNA molecule that did not display all the characteristics of life as we know it today. Nucleotides are the “letters” in the “words” of RNA and DNA. Nucleotides are composed of three components, a nitrogenous base, a ribose sugar, and a phosphate group (Figure 5.2), but nucleotides can form long chains that store and replicate genetic information. Unlike DNA, RNA has chemical properties as well as information storage functions and so can act as an enzyme to catalyze chemical reactions that lead to replication. Thus, RNA can bypass the middleman in the current system of DNA→RNA→protein. The ability for these simple molecules to self-replicate would then allow these molecules to evolve. At some point, these molecules would become enclosed in a lipid membrane, forming a proto-type cell that could isolate the genetic material within the membrane from the external environment. Once isolated and somewhat protected, these self-replicating information storers could take on other functions, slowly resembling the simplest cells on earth. But even these simplest of cells are amazingly complex. Criticisms of the “RNA first” hypothesis for the origin of life rest around the idea that RNA, because it is single-stranded, and not twisted into a double helical chain, is much more fragile than DNA and would probably break apart in prebiotic conditions. Others have questioned the

99

100

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

Figure 5.2  The chemical structure of RNA. The nitrogenous bases (C, G, A, U)

are joined to a ribose sugar and are then linked by the phosphate group to form long chains. (Courtesy of Sponk, https:// commons.wikimedia.org/wiki/File:RNANucleobases.svg.)

idea of the replicating information system evolving before the compartment (cellular lipid membrane) and metabolic systems, and have argued that these systems may have originated simultaneously. Regardless of the order in which life’s essential components and systems originated, many researchers have focused on investigating chemical pathways that could produce the necessary building blocks of life (e.g., nitrogenous bases, sugars, lipid membranes, and amino acids) before there was life itself. The most well-known experiment addressing the formation of the constituents for the origin of life was conducted by scientists Stanley Miller and Harold Urey at the University of Chicago in 1952. They proposed that, if Earth’s early atmosphere were low in free oxygen, the reaction between chemicals available in both the atmosphere and the early seas could, when provided with an energy source, produce the organic building blocks of life abiotically (i.e., without life). They set up a system containing water, methane, hydrogen, and ammonia, all components proposed to exist in the earliest atmosphere, and then supplied this closed system with energy in the form of an electrical spark to simulate lightning (Figure 5.3). After a week, the clear starting fluids became thick and deep brown. When this mixture was analyzed, amino acids and other “organic” compounds were plentiful, but they could not detect either nucleic acids or sugars. So, while this didn’t answer the question of an abiotic origin to life, it did inspire many to follow on the heels of the Miller–Urey experiments, and by changing the conditions slightly, they found that some of the other compounds needed for life, like nucleic acids present in modern DNA could also form abiotically. This suggests that the building blocks of life can form without a living precursor, and gives support to the idea that, given the right starting compounds, life can arise from non-living sources. As we expand our search for life on other planets, understanding the conditions for life to get started on Earth takes on added importance. However, there is still a vast amount of work to be done to clarify the conditions needed for life to form independent, living organisms.

5.2  Getting Started: Hypotheses for the Origin of the First Life

101

Figure 5.3  A diagram of the apparatus that Miller and Urey used to simulate Earth’s proposed early atmosphere.

Heated water vapor containing methane, ammonia, and hydrogen were exposed to an electrical spark and then condensed out into water, which was tested for the presence of organic compounds. (Courtesy of YassineMrabet, https://commons. wikimedia.org/wiki/File:Miller-Urey_ experiment-en.svg.)

5.2.2 Where Life First Began Being able to synthesize the building blocks of life in a lab, without any biological influences, provides valuable insight into the origin of life, but the conditions and chemicals used need to have already existed on the early Earth to be a viable explanation for how life may have originated on Earth. The main components of all living organisms are carbon, nitrogen, hydrogen, and oxygen. These make up sugars, proteins, DNA, and lipids. But, where did they come from? The raw materials required for life had to already be present in the environment, and in fact, Miller and Urey started with these. This adds another layer of complexity to the origin of life on Earth question, as there is much uncertainty regarding what conditions were like on the early Earth. Nevertheless, various hypotheses have been put forth as to what environments on the early Earth were likely to have harbored the chemicals and conditions necessary for life to begin.

5.2.2.1 Hypothesis That Life Began in Shallow Bodies of Water In some models of our planet’s formation, the Earth starts out as not only a very hot environment, but also highly reducing one, in which no free oxygen was available to organisms and there was plenty of methane, ammonia, and water vapor in the atmosphere (these are the conditions simulated by Miller–Urey). Although some scientists disagree with this harshly reducing atmosphere, other experiments similar to Miller–Urey which used a mix of water vapor, nitrogen, sulfur compounds, and carbon dioxide, to simulate an atmosphere rich in volcanic gases, have also produced organic compounds. These experiments demonstrate that a variety of compositions for Earth’s early atmosphere could potentially lead to the abiotic formation of organic molecules. If organic molecules were created via this spark method, it is proposed that they then became concentrated in shallow pools of water (or Warm Little Ponds as they are affectionately called by scientists) on the Earth’s surface, allowing them to react and polymerize (combine) to form biomolecules and eventually life. Evidence: Zircon crystals provide evidence that water and continental crust may have existed very early in Earth’s history (Chapter 2 and Section 5.3). This would have allowed shallow pools of water to form on early continents. If these ponds experienced wet and dry cycles, the wet

102

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

Figure 5.4  The Grand Prismatic Spring in Yellowstone National Park is an example of a hydrothermal pool. The

colors around the rim of the pool are from microbial mats. Similar pools on the early Earth could have been potential sites of the concentration of organic molecules and the eventual origin of life.

cycles would bring in additional “raw materials” and the dry cycles would greatly concentrate these materials, aiding in their polymerization. The pools could have also existed in volcanic hydrothermal zones, similar to those currently found in Yellowstone National Park (Figure 5.4), and may have contained grains of clay, which can play an important role in abiotic synthesis. Clay grains, produced by the weathering of minerals, are finely crystalline, highly reactive, and charged materials. Organic compounds, regardless of their source, have a strong affinity for these grains, and stick to the surfaces of small grains of clay, where they become concentrated. If these rare (at first) compounds were adsorbed onto clay grains, they would be held in place and stabilized, increasing local concentrations as they accumulate, making chemical reactions more likely to occur.

5.2.2.2 Hypothesis That Life Began under Extremely Hot Conditions One hypothesis that is favored by many origin of life scientists is that life originated at hydrothermal vents in Earth’s early oceans (Figure  5.5). Hydrothermal vents occur near the mid-ocean ridges of divergent tectonic plate boundaries (see Chapter 2). Water enters fractures in the Earth’s crust near a divergent boundary, is super-heated by magma bodies, and is vented back out into the ocean. The water leaving the vents is

Figure 5.5  Deep sea hydrothermal vents, like the white smokers pictured here, have been proposed as a likely setting for the origin of life on Earth.

(Courtesy of NOAA.)

5.2  Getting Started: Hypotheses for the Origin of the First Life

extremely hot, from 40–300°C (100–570°F), and can be rich in methane, hydrogen, and sulfur. Hydrothermal vents produce porous chimneys which could concentrate prebiotic molecules, and also have a proton gradient created by differing pHs of the seawater and vent water that could have served as an energy source for early life. It is unclear how long it took for life to begin, but although vent fields are long-lived, individual hydrothermal vents chimneys tend to be short-lived geologically (years to decades), which presents a limitation to the hydrothermal vent origin hypothesis. Evidence: If life began under extremely hot conditions, we would expect two things: (1) that we can observe life existing in extremely hot environments today and 2) that such life has to have the most in common, chemically and/or biologically, with extant organisms that live in what are the currently hottest parts of our planet. It was previously thought that such elevated temperatures as exist at hydrothermal vents would break bonds between molecules as soon as they formed, and life couldn’t exist in such hot waters. But recent explorations of the deep ocean floor have shown that communities of microbes and multicellular life thrive in hydrothermal vent environments. And through analysis of DNA, RNA, and proteins of extant organisms, thermophiles (heat-loving organisms) are proposed to be at the very base of the tree of life. Life may have originated more than once, or in cooler environments, but because all organisms alive today share the most DNA sequences in common with these thermophiles, if life evolved under other conditions, these earlier, alternate life forms went extinct, leaving only the thermophiles to pass genes on to all living organisms today.

5.2.2.3 Hypothesis That Life (or Its Building Blocks) Came from Space This hypothesis is sometimes called “panspermia” or “interplanetary seeding”. It proposes that life began elsewhere—at a different place in our solar system or even a different solar system in our universe—and was transplanted to Earth on comets or meteors that impacted with the planet in the distant past. Early in the planet’s history, when bombardment of the surface by materials of extraterrestrial origin was at its peak, the dust from these impacts would settle on the early Earth, perhaps delivering the raw material for life that became concentrated in shallow ponds. Evidence: Many compounds that are either biochemical precursors or key components for living organisms have been identified in association with asteroids and other bodies, as well as in interstellar clouds through which our planet passes. We can identify organic compounds, even in outer space, by measuring the particular way they interact with light. Each type of carbon-containing compound absorbs light differently, and we can measure this using a process called spectroscopy. The precursors of life; methane, hydrocarbons, and even amino acids, have been detected in the tails of comets, and in association with meteoric components that come to rest on the surface of our planet. In fact, when the famous Halley’s comet last approached the earth, measurements showed that up to 70% of the dust grains forming its tail were composed of (or carried), carbon-, nitrogen-, hydrogen-, or oxygen-based compounds! Even more directly, we have studied meteorites that have fallen to Earth and been collected. An analysis of the Murchison Meteorite that fell to Earth in 1969 revealed that it contains many of the same amino acids and organic compounds obtained by Miller and Urey! Thus, there are many opportunities for organic compounds or primitive life forms, evolved on extraterrestrial bodies, to be incorporated into the Earth.

103

104

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

The biggest problem with this hypothesis is that it doesn’t really solve the problem of how life began. The chemical reactions that brought life from non-living materials would still be required and having panspermia origins simply removes it one step from our own Earth but doesn’t really address the fundamental question of how life arose. Currently, all of these hypotheses are incomplete. We cannot say for certain how or where life began and can only give a broad estimate of when it began, on this one planet. But what we can say is that in the beginning, life was very different from today. It was much simpler on every level, and it took a very long time for it to achieve the complexity and diversity that we see today. We can also say that by all our ways of measuring, all life on this planet, from the smallest, simplest life forms to the most complex, has enough in common that it points to a single origin of life and that all living things are linked to a common ancestor.

5.3 WRITTEN IN STONE: EVIDENCE FOR EARLY LIFE After reading this section you should be able to… • State how long-ago life likely originated on Earth. • Summarize three lines of evidence for the earliest life on Earth.

The rock record is all we have to interpret processes that occurred long before we were here to observe them. However, the very oldest rocks to form on our planet are already much younger than the planet, because rocks dating to when the planet was first forming are no longer around for us to study. As we discussed in Chapter 2, rocks are continually being recycled: magma cools and solidifies to form rocks, the rocks weather and erode, the resulting grains lithify into new rocks, and during subduction, they are again melted. So, we are limited as to how far back in time we can observe to gain perspective on our changing planet. One way that we can trace history is by using zircon. Zircon is a very stable mineral that contains the radioactive element uranium, and resists having its isotopic ratios, and date of formation, reset by high temperatures and pressures in the Earth’s crust (see Chapter 2 for a discussion of radiometric dating). Zircon crystals formed on the early Earth as part of the cooling magma that solidified into the first surface rocks. As these rocks were recycled, the stable zircon crystals remained unaltered and continued to record their age of formation, eventually getting deposited and lithified into younger sedimentary conglomerate rocks. The oldest zircons we have measured from these rocks are just over 4 billion years old, almost as old as the earth itself. In fact, some rocks that have been dated to about 3.8 billion years old already contain evidence of early life. But what is this evidence? How can we know that life has been around that long? There are multiple, independent lines of evidence that life began ~3.8 billion years ago. Some lines of evidence for early life include: • Chemical evidence • Mineral evidence • Fossil evidence

5.3  Written in Stone: Evidence for Early Life

5.3.1 Chemical Evidence As mentioned above, living things must metabolize, using common molecules and elements to build the compounds they need to survive. As part of the process, they partition (or separate) elements into isotopes in a process called fractionation (see Chapter 2 to refresh on isotopes). Isotopes of elements in the environment occur in known, predictable ratios. Any deviation from these ratios is an indication that non-random processes acted to preferentially add or remove one type of isotope—i.e., the “heavier” isotope (with relatively more neutrons) or the “lighter” isotope (with relatively fewer neutrons). It turns out that living organisms almost always prefer lighter isotopes for their chemical process (perhaps all life likes to avoid heavy lifting!), so when we see isotopic ratios that are depleted in (have less of) the heavy isotope from the predicted ratio, it is often used as a marker for life processes. In the oldest rocks, we can already see evidence of this partitioning occurring, even if we don’t have body fossils of living organisms. Some of this chemical evidence can be found in analyses of particles of the mineral graphite within crystals of rocks dating to 3.8 billion years ago. Graphite is pure carbon, and it is hypothesized that graphite represents highly altered remnants of carbon incorporated into once-living organisms through carbon cycling. Carbon cycling is best illustrated by plants that photosynthesize, incorporating CO2 from the atmosphere into biomass—and selecting the light isotope forms of carbon as they do so. So, the measurable increase in the light isotopes of carbon found in these old graphite samples, compared with that measured in the surrounding rocks, provides evidence that these carbons may be organically derived from life. In addition to isotope fractionation, rocks contain other carbon-based compounds that are associated only with living organisms in today’s world. These compounds have changed over the vast time periods between then and now, but they are still recognizable and can be linked to their original forms. For example, prokaryotes have lipid-based molecules called hopanoids that they incorporate into their cell membranes, influencing permeability and structure. Eukaryotes, including humans, need a molecule to perform the same function, but we use steroid compounds like cholesterol, which are an entirely different kind of molecule. Both of these molecular classes are small, lipid-based compounds, but hopanoids are never found in eukaryotes, and steroids are not found in bacteria. Over time, bacterial hopanoids change into extremely stable compounds called hopanes, and these hopanes are present in the oldest rocks. On the other hand, eukaryotic steroids and cholesterols alter to steranes, which are also very stable. Both these compounds are formed only by living organisms, thus, their presence in ancient rocks testifies to the presence of life on Earth during the time period represented by those rocks. Interestingly, hopanes are found in rocks that are much older than those containing steranes; this is one piece of evidence that hopanoid-producing prokaryotes emerged before eukaryotes.

5.3.2 Mineral Evidence The most abundant component of today’s atmosphere is not oxygen, but nitrogen! Oxygen makes up only 20% of the atmosphere. Most evidence suggests that oxygen levels in the early earth atmosphere were even lower. Oxygen was present, but bound in compounds like CO2 or H2O, and thus unavailable for the chemical reactions of living organisms that are common today. If this were not the case, then life probably could not have started, because oxygen is toxic and highly reactive, allowing uncontrolled chemical reactions to occur, making molecules unable to function

105

106

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

in chemical processes needed for life. But eventually, lifeforms began to emerge that responded to a free energy source—the sun—using this energy to grow and reproduce through photosynthesis. The byproduct of photosynthesis, you may remember, is…oxygen! Toxic, poisonous oxygen…at least to many life forms. Those early photosynthetic organisms were poisoning their atmosphere. Life would have been doomed, except that other organisms evolved to thrive in these oxidizing environments. They used the toxic byproduct of photosynthesis as an energy source! The early rock record shows a gradual rise in the concentration of free oxygen in the atmosphere, first locally, then worldwide, as evidence of the emergence and spread of photosynthesizing life. Some of this evidence is, basically, rust. When iron (readily available in many rocks) reacts with oxygen, it oxidizes and turns the familiar, rust-red color we’ve all experienced on our bikes, cars, or tools. Iron-containing minerals are rather common in the rocks at the Earth’s surface. As these minerals weather out of the rocks and are redeposited, they can be oxidized by abundant free oxygen in groundwater, producing rust-red colored sedimentary rocks (called red beds). However, some sedimentary rocks older than 2.5 billion years contain clasts (see Section 2.3) of a mineral called pyrite (fool’s gold). But we don’t see clasts of pyrite in sedimentary rocks formed after 2.5 billion years ago. This informs us that the early atmosphere must have lacked abundant oxygen because pyrite clasts are very unstable and weather too quickly in the presence of oxygen to become part of clastic sedimentary rocks. But, when we examine rocks dating to about 3.5 billion years, we begin to see evidence for increasing oxygen in the atmosphere. In fact, there are entire formations of rocks that were deposited in the ocean that we call banded iron formations (BIFs). These BIFs contain shiny, metallic bands of gray or black, like ribbons of iron, and point to an atmosphere with plenty of free oxygen to form these iron-rich magnetite and hematite layers (Figure 5.6). These BIFs formed in abundance during the period of 2.4 to 1.8 billion years ago, a period known as the Great Oxygenation Event, evidence that photosynthetic cyanobacteria were in full swing during this time, producing plenty of free oxygen.

5.3.3 Fossil Evidence Life on Earth remained microscopic for nearly 3 billion years, which presents two rather large challenges if you are trying to hunt for fossil evidence of the earliest life on Earth. First, microscopic organisms do not have hard parts like bones, teeth, or shells that are likely to be preserved in the rock record. Second, it can often be hard to find fossil remains of microscopic organisms, and even when you think you have, it is often Figure 5.6  This banded iron formation (BIF) is composed of alternating layers of silvery-gray iron oxides and reddish chert (a sedimentary rock).

They provide evidence of free oxygen in the atmosphere that allowed the layers of iron oxide to accumulate. (Courtesy of James St. John, https://flic.kr/p/oEfwPm.)

5.3  Written in Stone: Evidence for Early Life

107

hard to provide evidence that they are not the relics of mineral crystallization or other geologic processes. In 1993, purported microfossils were described by paleontologist William Schopf as filamentous bacteria from 3.5 billion-year-old sedimentary rocks of Western Australia. More recent analysis of carbon isotopes in these samples has been used to support their biogenic origin. Another sample found in Greenland was described as 3.7 billion-year-old stromatolite fossils. Stromatolites are photosynthesizing bacteria that have been around for billions of years and still exist today, although they are rare. They live communally in shallow marine waters and form distinctive mound-like structures as they grow upward in thin layers (Figure 5.7 and 5.8). Many other scientists have disagreed with Schopf’s interpretations of these structures though, suggesting instead that these Figure 5.7  Living stromatolites in Shark Bay, Australia. (Courtesy of Paul

Morris, https://flic.kr/p/5BBAB6.)

Figure 5.8  Cross-section of a fossilized stromatolite. (Courtesy of Didier

Descouens, https://commons.wikimedia.org/ wiki/File:Stromatolites_Cochabamba.jpg.)

108

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

samples are “pseudofossils” resulting from the recrystallization of minerals or other geologic processes. While there is strong fossil evidence in the form of stromatolites for life existing at least 2.5 billion years ago, claims of evidence for the earliest life on Earth dating from 3.5–4 billion years ago are far from definitive. Much more research is needed to strengthen many of these arguments, especially when the evidence is based on indirect observations (isotope signatures) or questionable fossils. The low probability of microscopic organisms being preserved in the rock record, surviving billions of years of geology processes, and being found by researchers does not make this an easy task. Although we may never definitively know exactly when life originated on Earth, we do know that it did originate, otherwise you would not be sitting here reading this book.

5.4 LIFE THROUGH TIME: FROM EARLY MULTICELLULAR LIFE TO THE TIME OF THE DINOSAURS After reading this section you should be able to… • Construct a simplified timeline of the Paleozoic showing some of the major transitions in the evolution of life, including the Cambrian explosion, origin of fish, origin of tetrapods, origin of amniotes, and the origin of synapsids and archosaurs (Figure 5.9).

5.4.1 Faunal Succession Just as we can trace changes in landforms, from one supercontinent (Pangea) to the familiar topography of our planet today, we can also trace changes in life forms. As mentioned in the opening to this chapter, for roughly the first 3 billion years that life existed on Earth, life was relegated to single-celled organisms. As we journey through time, we will work our way from the first multicellular life up to the reign of dinosaurs in the Mesozoic Era. We will briefly stop in each period along the way, highlighting the major biologic and geologic events that constitute the fascinating history of our planet.

5.4.2 The Ediacaran Period (635–541 Ma)

Figure 5.9  Geological time scale with early events marked.

The first evidence of multicellular life comes in the form of simple, soft-bodied creatures that represent the Ediacaran fauna, which appeared in the fossil record approximately 600 million years ago. Most of these creatures look nothing like modern lifeforms, and they have proven difficult to fit into the tree of life with many paleontologists debating their true identity (Figure 5.10). They have been described as everything

5.4  Life Through Time: From Early Multicellular Life to the Time of the Dinosaurs Figure 5.10  An artist’s depiction of what life in an Ediacaran ocean may have looked like. (Courtesy of

Maulucioni, https://commons.wikimedia. org/wiki/File:Ediacaran_sea.png.)

from lichens and algae, to animals or plants, or even some type of intermediate form between plants and animals. No modern relatives of the Ediacaran fauna are known, and by the Cambrian Period, they are almost completely replaced, with only a few rare fossils showing up in the Cambrian before they disappear completely.

5.4.3 The Cambrian Period (541–485 Ma) The Cambrian Period was an exciting time for life, because widely diversified life forms appear for the first time in the fossil record, including both soft-bodied animals similar to those of the Ediacaran, and also animals that show the first evidence of having hard parts, like shells or exoskeletons. In a small quarry in deposits known as the Burgess Shale, located high in the Canadian Rocky Mountains, an enormous amount of diversity is shown in fossils dating to about 500–540 million years ago. These fossils represent the most primitive members of most extant (still living) phyla, like arthropods and flatworms, as well as many others that do not fit in any category of existing organisms. These preserved animals are said to represent the “Cambrian Explosion”, because they represent an “explosion” of diversity that appeared in a geological instant. The Cambrian Period is often called the “Age of Arthropods”, because most of the organisms living during this time period are morphologically similar to arthropods alive today, even though in these same deposits we also see representatives of other phyla—including our own (Chordata)! Many of these creatures were quite familiar-looking, like brachiopods and trilobites, but many were extremely odd. There was the spiny worm-like, nightmare-inducing creature aptly named Hallucigenia (Figure 5.11), the one-meter large (huge by Cambrian standards) predator Anomalocaris (Figure 5.12), or the alien-looking Opabinia, which had an elephant-like proboscis, which perhaps functioned to grab food and bring it to its mouth (Figure 5.13). Geologically, during the Ediacaran, all landmasses were joined together in a supercontinent called Pannotia. During the Cambrian Period, Pannotia began to split apart into smaller continents (a pattern periodically repeated throughout Earth’s history). This would have led to an increase of continental shelves, shallow marine habitats where life in the Cambrian could flourish.

109

110

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

Figure 5.11  Artist’s depiction of Hallucigenia. (Courtesy of MUSE,

https://commons.wikimedia.org/wiki/ File:Hallucigenia_sparsa_-_MUSE.jpg.)

Figure 5.12  Anomalocaris was a Cambrian predator that could be as big as one meter. (Courtesy of MUSE,

https://commons.wikimedia.org/wiki/ File:Anom​aloca​ris_c​anade​nsis_​-_rec​onstr​ uctio​n_-_M​USE.j​pg.)

Figure 5.13  Artist’s depiction of the alien-looking Opabinia. (Courtesy of

Nobu Tamura, https://commons.wikimedia. org/wiki/File:Opabinia_BW.jpg.)

5.4.4 The Ordovician Period (485–444 Ma) The Ordovician was another period of massive radiation of life, one that rivaled the Cambrian. Large areas of shallow seas allow for the diversification of trilobites, cephalopods (squid-like animals), sponges, and algal reefs. The Ordovician is also the period when plants and animals first began to colonize land! Early land colonizers included fungi, non-vascular plants similar to modern liverworts, and some trace fossils even hint that arthropods may have ventured out onto land in the Ordovician.

5.4  Life Through Time: From Early Multicellular Life to the Time of the Dinosaurs

111

On our path toward the evolution of dinosaurs, the next major event is the appearance, diversification, and broad distribution of fish—and these certainly don’t seem to be in the lineage of the mighty T. rex. However, these early fish were not like those familiar fish that populate lakes, oceans, and dinner plates today. Early members of this group were very different. For example, one major, early development within fish (and therefore one of the primary divergences in fish lineages) during the Ordovician is the development of true bony jaws (Gnathostomata). If you have trouble imagining “jawless” fish, we actually have two living examples today: lamprey and hagfish. Lampreys have a cartilaginous skeleton and a circular mouth rimmed by many teeth that are capable of boring into the sides of other fish (although not all members of this group are parasitic, Figure 5.14). Hagfish are even stranger, in that they have a skull but no true spinal column, and only rudimentary vertebrae. They can enter and disembowel dead and dying sea creatures, often devouring their prey from the inside. So even without jaws, these living creatures are very efficient carnivores! The end of the Ordovician marks the first of five major mass extinctions to occur during the Phanerozoic Eon (See Chapter 20 for more on mass extinctions). Although the supercontinent Pannotia had broken apart, there was still a rather large supercontinent named Gondwana that was situated on the south pole. The extinction was likely started by the collision of the island arc Avalonia with the ancient North American continent of Laurentia. This collision resulted in a halt to volcanic activity (and atmospheric CO2 input), as well as increased weathering and erosion of the resulting ancestral Appalachian Mountains (which draw CO2 out of the atmosphere). This disruption to the Earth’s carbon cycle would lead to a rapid (geologically speaking) cooling of the global climate. This resulted in glaciation on the southerly located Gondwana. In addition to cooling, massive glaciation caused sea levels to drop, which had detrimental effects on many of the shallow sea-dwelling organisms of the Ordovician. Although most of the major groups alive during the Ordovician survived the extinction, their diversity was dramatically­ lowered.

5.4.5 The Silurian Period (444–419 Ma) The Silurian Period is notable in our journey to dinosaurs because of the diversification of fish that occurred during this time. True jaws originated and bony internal skeletons. Among jawed fishes, the placoderms are an early, and iconic, group. The head and neck of placoderms were heavily encased in bony plates, and some would eventually get quite large (up to 20 feet!), at a time when most fish remained quite small (Figure 5.15). They were predatory, but their size and bulky armor-like plating made them slow-moving. As time progressed, though, fish also became lighter

Figure 5.14  The Pacific lamprey is a living example of a jawless fish.

(Courtesy of Dave Herasimtschuk, US Fish & Wildlife Service.)

112

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

Figure 5.15  Dunkleosteus was a Devonian placoderm that grew to almost 20 feet long. Placoderms evolved

in the Silurian period. (Courtesy of Dmitry Bogdanov, https://commons.wikimedia.org/ wiki/File:Dunkleosteus_intermedius.jpg.)

and more agile as some lost their heavy armor. The Silurian also saw the first major radiation of land-dwelling (terrestrial) plants, and from the fossils they left behind, we can tell that they were gaining some features of modern plants, including an advanced vascular system that allowed them to grow bigger and live in varied environments.

5.4.6 The Devonian Period (419–359 Ma) The Silurian saw the origin and early diversification of fish, but the Devonian is known as the “Age of Fishes”, because it is during this time their widespread abundance and diversity dominated the ocean. Sharks present in the Devonian are virtually unchanged morphologically from those alive today. Fish divided into two main groups, lobe-finned (sarcopterygians) and ray-finned fish (actinopterygians). Today, most fish are the latter, and when you think of a fish, you are probably thinking of the familiar organisms that possess these reinforced fins, from goldfish to groupers. But the lobe-finned fish possess fleshy fins that contain many bones, organized more like the forelimbs of land-living animals. Lobe-finned fish today consist of only a few groups, like coelacanths and lungfish, but it is thought that this group gave rise to the first tetrapods—or four-legged organisms—that left the water to become the first vertebrates to occupy land. Remember Tiktaalik from Chapter 1? Tiktaalik was a Devonian fish with fins made up of robust bones that would have allowed it to support itself on land, making it a possible common ancestor of all tetrapods (Figure 5.16). The Devonian also gave rise to insects, including millipedes, centipedes, and arachnids. The Devonian stage was being set, geologically, for the formation of the next big supercontinent, Pangea. What is now North America and Europe were joined together as Euramerica and situated near the equator. The continents of South America, Africa, Antarctica, India, and Australia formed another giant landmass, Gondwana, which was situated in Figure 5.16  Artist’s depiction of Tiktaalik. (Courtesy of Zina Deretsky).

5.4  Life Through Time: From Early Multicellular Life to the Time of the Dinosaurs

113

the southern hemisphere. These two massive continents were relatively close together, and began converging before the end of the Devonian, eventually forming, for a second time, a single supercontinent. Temperatures and sea levels were high during the Devonian, flooding much of the continents and leading to plenty of warm shallow seas for fish and other marine life to thrive in (Figure 5.17).

5.4.7 The Carboniferous Period (359–299 Ma) The Carboniferous is known as the “Age of Amphibians” because this group of organisms began to dominant the terrestrial environments of the earth’s surface. However, the amphibians of the Carboniferous did not look much like those of today, such as frogs and salamanders. They were quite large, and some were predatory. They were the first successful and diverse group of vertebrates to colonize the land, but like today’s amphibians, they were limited to the water for reproduction, and that greatly restricted where they could live. Later in the Carboniferous, we see evidence for the very first amniotes, named for one of the most important “inventions” in the history of life on land, the amniote egg. This egg is a complicated structure that wraps the developing embryo inside a three-membrane complex. In living mammals, these membranes surround the embryo and form part of the placenta, and in non-mammals, these membranes are encased in a hard or leathery shell. Together, the membranes and shell prevent the embryo from drying out and provide it with the nutrients it needs to grow. This novel new egg allowed vertebrates to completely lose their dependence on water. With this last constraint lifted, virtually every terrestrial niche could now be occupied by vertebrates, especially the newly evolving group we call reptiles. Reptiles were diverse and successful, and radiated to occupy many niches, including herbivorous ones. Of course, among these early reptiles were the ancestor of the dinosaurs. Another group to arise from the amniotes during the Carboniferous was the Synapsids (see Chapter 7), a lineage that would later lead to mammals. The Carboniferous Period also saw the highest levels of atmospheric oxygen in Earth’s history, with levels near 35% compared with today’s 20%. This allowed terrestrial invertebrates (who breathe via oxygen diffusion through their body), to reach extremely large sizes. Imagine running into an 8.5-foot-long millipede, Arthropleura, as you walk through the forest, or looking up to see dragonflies with wingspans of 30 inches, or 28-inch-long scorpions skittering along the ground! Many other beloved insect groups also arose in the Carboniferous such as Dictyoptera, the ancestors to modern cockroaches. In the oceans, the extinction of the placoderms at the end of the Devonian allowed sharks to undergo a massive radiation during the Carboniferous, leading to some rather strange sharks like the Stethacanthus with a scrub-brush looking dorsal fin (Figure 5.18). Figure 5.17  Paleomap of the Late Devonian showing the early stages of the supercontinent Pangea, and the vast shallow seas that allowed marine life to thrive. (Reprinted with permission

from Chris Scotese.)

114

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

Figure 5.18  Stethacanthus was a rather odd shark with a scrub-brush like dorsal fin. (Courtesy of Nobu Tamura,

https://commons.wikimedia.org/wiki/ File:Stethacanthus_BW.jpg.)

The Carboniferous also saw continued development and diversity of plants, and the rise of vast forests and numerous swamps that thrived in the moist conditions of the Carboniferous. The “trees” that made up carboniferous forest were not like those of today, but instead were giant-scale trees, more closely related to mosses. Horsetails, club mosses, and ferns were also thriving in the numerous swampy forests of the Carboniferous, the remnants of which would form the largest coal deposits on the planet, and which give this period its name. Other notable plant groups would also arise in the Carboniferous including cycads and early conifers. Throughout the Carboniferous Period, Euramerica and Gondwana continued to converge. This convergence would lead to the formation of the Appalachian Mountains as well as the Urals. By the end of the Carboniferous, the newest and most recent supercontinent, Pangea, was fully formed. The end of the Carboniferous also saw the return of glaciation on the southern pole of Pangea, which had a devastating impact on the vast forests, resulting in a minor extinction event known as the Carboniferous Rainforest Collapse.

5.4.8 The Permian Period (299–252 Ma) In the Permian, amniotes diversified further, and the ancestors of familiar turtles, lepidosaurs (lizards and snakes), and archosaurs (crocodiles, dinosaurs, and birds), as well as the earliest ancestors of mammals, first appear. Once again, we see the role the position of the continents played in life’s evolution. In the early Permian, the continents had all come together, uniting again into one single landmass we call Pangea, and one giant ocean that covered the rest of the planet. The interior of Pangea became hotter and dryer through the Permian, conditions to which the new reptiles were well-suited. It also favored different types of vegetation than existed during the much wetter Carboniferous. It is during the Permian that we see the appearance of the first modern trees, including conifers, ginkgos, and cycads, all of which have living descendants. During the Permian, amniotes diversified into two distinct groups. On one side were the synapsids, named because of where certain holes occurred in their skulls. These included the sail-backed pelycosaurs like Dimetrodon that would rule in the early Permian (Figure 5.19) and give rise to descendants that showed progressively more mammal-like features, referred to as therapsids. The Middle and Late Permian would be ruled by large therapsids like dinocephalians, gorgonopsids, and dicynodonts (named for their two tusks, “two dog tooth”). Most notable for us humans, the cynodonts (“dog teeth”) that arose in the late Permian, and

5.4  Life Through Time: From Early Multicellular Life to the Time of the Dinosaurs

115

Figure 5.19  Dimetrodon, was a Permian synapsid. It was not a dinosaur

and is actually a very distant relative of humans (see Chapter 7). (Courtesy of DiBgd, https://commons.wikimedia.org/wiki/ File:Dimetrodon_grandis.jpg.)

already showed some very mammal-like features, would go on to evolve into true mammals during the Triassic. The other branch of amniotes that arose in the Permian included the anapsids and diapsids. Anapsids had no holes in their skull, and Pareiasaurs, a large (up to 10’ long) herbivorous group of anapsids that arose late in the Permian, may have been early ancestors of turtles (Figure 5.20). What we think of today as “true reptiles” (diapsids) arose and began to diversify, but they still lived in the shadows of the synapsids and the other dominant Permian group, the great amphibians. Only three lineages of amphibians exist today, but in the Permian, they were much more diverse and widespread, roaming the humid and tropical landscapes. Some were very large, at least compared with today’s versions. Even though it is hard to feel threatened by a frog, some ancient amphibians were active predators, as evidenced by forward-facing eye sockets and sharp teeth. However, like modern amphibians, these remained tied to the water for reproduction. The Permian ended with the largest mass extinction the world has ever seen, and some evidence suggests that it may have been caused by massive volcanism, or an extraterrestrial impact, or perhaps both (we will return to this in detail in Chapter 20), but the cause is largely shrouded in mystery. The massive ocean was almost sterilized, with 90–95% of lifeforms going extinct, as well as most of life on land (70%). Recovery was slow, and when life did return in abundance, many major players were gone forever from the world’s stage. Trilobites, which survived since the Cambrian, went extinct during the Permian, as did most of the remaining large and successful amphibians and many groups of therapsids.

Figure 5.20  Pareiasaurs were large Permian synapsids that may have been early relatives of turtles. (Courtesy of Nobu Tamura,

https://commons.wikimedia.org/wiki/ File:Pareiasaurus_serridens.jpg.)

116

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

The great and mysterious extinction ending the Permian Period also ended the Paleozoic, an era covering ~300 million years of incredible change in the diversity and complexity of life on this planet. The extinction ushered in the Mesozoic Era, the period of “middle life”, that is also known both as the “Age of Reptiles” or the “Age of Dinosaurs”.

5.5 THE MESOZOIC ERA: AGE OF THE DINOSAURS After reading this section you should be able to… • Describe what was occurring geologically and tectonically from the Permian through the Cretaceous. • Given a paleomap, identify which Mesozoic Period it is representing. • State the time period and approximate date (Mya) for the origin of dinosaurs. • Explain why the Triassic–Jurassic extinction was so important in the evolution of the dinosaurs.

The Mesozoic Era began after the End Permian extinction, some 252 million years ago, and lasted until the Cretaceous–Paleogene extinction 65 million years ago. It is divided into three periods, the Triassic, Jurassic, and Cretaceous. While the Mesozoic is often referred to as the “Age of Reptiles”, dinosaurs evolved early in the Triassic and persisted until the end of the Cretaceous period, thriving and evolving for roughly 170 million years! For this reason, the Mesozoic is also known as the “Age of Dinosaurs”. For paleobotanists (those who study ancient plants), the Mesozoic era is known as the “Age of Conifers”, as they would flourish after the end Permian extinction to become the dominant land plants of the Mesozoic era. Here, we focus primarily on the Triassic Period, looking at the evolutionary emergence of our favorite creatures, the dinosaurs. During this period, the archosaurs (that put in a first appearance in the Permian) diversified into two lineages, the Pseudosuchia (or fake crocodiles), and the Avemetatarsalia (or bird feet). Pseudosuchia (also referred to as crurotarsi, or “crossed ankles” in older literature) gave rise to crocodiles, alligators, and their extinct relatives, while the Avemetatarsalia, also called Ornithodirans, gave rise to dinosaurs, pterosaurs, and all living and extinct birds (Figure 5.21). We will touch on some of the major geologic Figure 5.21  Simplified family tree of Archosauria.

5.5  The Mesozoic Era: Age of the Dinosaurs

and non-dinosaurian biologic events from the Triassic through the Cretaceous, but changes in the dinosaurian lineages during these periods will be covered in Chapters 8 and 9 (Ornithischia and Saurischia).

5.5.1 The Triassic Period (252–201 Ma) By the early Triassic, the world was recovering from the worst extinction event ever experienced. The biodiversity so prevalent in the Permian was greatly diminished; it would take 30 million years to reach the same level of diversity revealed in Permian fossils. Gone forever were the giant sail-backed reptiles like dimetrodon. The great diversity of these synapsids, animals that would include mammals, was reduced to just two lineages, the Anomodontia and the Theriodontia, which were ancestors to mammals. But what was bad for the mammals was good for the dinosaurs! At the start of the Triassic, all of Earth’s continents were fused together forming the supercontinent Pangea, which was centered on the equator (Figure 5.22). This landmass stretched almost from pole to pole and remained in place for almost 25 million years. This had a profound effect on the climate. Ocean currents were not hindered, and warm equatorial waters could mix completely with colder polar waters, resulting in much warmer global temperatures. The interior of this large continental landmass was very hot and dry, evidenced by massive formations of wind-deposited sandstones and evaporites. Like the interior of our own North America, it experienced hot dry summers and cold winters. At the start of the Triassic, global climates were warm. In the lower latitudes, summer and winter temperatures didn’t vary much, hovering around 36°C (95o F) in the summer, and only slightly lower in the winter. By Middle to Late Triassic, Pangea began to show the first signs of rifting, or splitting apart, and this was accompanied by significant shifts in climate, because it changed ocean currents and weather patterns, increasing terrestrial humidity. This initial rifting of the continents, which occurred between North America and Africa, would eventually form the Atlantic Ocean. It was accompanied by extensive faulting, which resulted in the formation of rift basins. These low basins would fill with sediment, and this is where we find some of the best Triassic age deposits and fossils. Life showed signs of dramatic diversification in both plant and animal life during the Triassic. Many well-known groups put in a first appearance here, including pterosaurs (flying reptiles closely related to dinosaurs, see Chapter 10), true mammals, turtles, and, of course, dinosaurs. What was so different? Why were the animals after the great extinction so very different than before?

Figure 5.22  Paleomap showing the supercontinent Pangea during the early Triassic Period, 248.5 million years ago. (Reprinted with permission

from Chris Scotese.)

117

118

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

As is often the case with mass extinctions, wiping the slate clean gives organisms that were once hiding in the background a chance to branch out and adapt to new environments because their competition is so greatly reduced. Whereas synapsids and amphibians ruled the Permian, the fresh start of the Triassic allowed archosaurs and other diapsids to flourish, diversifying and radiating to fill in the niches left empty by the once-dominant synapsids. These new archosaurs included Triassic crocodiles that arose and diversified before dinosaurs (Figure 5.23). Two of these groups were active, agile, terrestrial animals superficially very similar to the early dinosaurs. The third, from which modern crocodiles probably descended, was a little more familiar in shape, but still more upright and active than crocodiles today—and MUCH larger. Other archosaurs that appeared in the Triassic included the heavily armored aetosaurs, which looked and probably acted like slow-moving tanks (Figure 5.24), and the long-snouted phytosaurs that probably competed with crocodiles for fish (Figure 5.25). The small, but deadly (based on their teeth) traversodonts (affectionately known as the “squirrels from hell”), and the robust rausuchids also competed for space and resources (Figure 5.26). Pterosaurs arose from the archosaur line as well but are more closely related to dinosaurs than they are to crocodiles, and, contrary to popular belief, they are not dinosaurs. We will talk about them in more detail in Chapter 10. Finally, the dicynodonts and cynodonts, herbivorous and carnivorous creatures on the line leading to

Figure 5.23  Hesperosuchus agilis was a Middle Triassic crocodylomorph.

(Courtesy of Jeff Martz.)

Figure 5.24  Desmatosuchus spurensis was a large Triassic aetosaur. (Courtesy

of Jeff Martz.)

5.5  The Mesozoic Era: Age of the Dinosaurs

119

Figure 5.25  Smilosuchus adamanensis was a large Triassic phytosaur.

(Courtesy of Jeff Martz.)

Figure 5.26  Postosuchus kirkpatricki was a large Triassic rauisuchid.

(Courtesy of Jeff Martz.)

mammals, were plentiful in parts of the Triassic world. Many mistakenly think that mammals couldn’t or didn’t evolve until the dinosaurs went extinct, but in fact, mammals and dinosaurs originated about the same time, and co-existed throughout their reign…and still do! In tandem with mammals, the dinosaurs made their first appearance in the Middle Triassic. However, dinosaurs were rare, and minor players for most of the Triassic. The earliest evidence we have of dinosaurs is found in sediment from the Early to Middle Triassic. Toward the middle of the Triassic, we find the very first bones of dinosaurs. Eoraptor (the dawn stealer) and Herrerasaurus (Herrera's lizard) (Figure 5.27) were both carnivores, and both were recovered from Argentina. These fossils suggest that the earliest dinosaurs were already swift, bipedal predators, but much smaller than the giant predatory dinosaurs that would come later in the Mesozoic. By the end of the Triassic, dinosaurs were still small, but relatively diverse, and already showing signs of the features

Figure 5.27  A model of Herrerasaurus with a skeletal cast in the background. (Courtesy of Brian Smith,

https://flic.kr/p/mgyKr.)

120

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

Figure 5.28  Coelophysis, another early Triassic dinosaur. (Courtesy of Jeff

Martz.)

that would set them apart from all other organisms, features that contributed greatly to their success. Eoraptor and Herrerasaurus were not the only Triassic dinosaurs. We also see skeletons of Coelophysis in Triassic sediments (Figure 5.28). This dinosaur was small, agile, and slender, but because we find many coelophysids together, we impart to them a very advanced feature—that of living in packs, or family groups. The first relatives of the great, longnecked sauropods also put in an appearance before the end of the Triassic, and show another advanced trait, herbivory. But for now, in the Triassic, dinosaurs would spend the first 35 million years of their existence living in the shadows of their more successful archosaur cousins. The Earth would experience another mass extinction event at the end of the Triassic Period. While not as devastating as the End Permian extinction, it still ranks among the top five deadliest extinction events to occur on Earth. The Triassic–Jurassic extinction event is thought to have been caused by widespread volcanism related to the separation of Pangea. As the North American and Eurasian plates began to pull away from Africa, this rifting would lead to widespread volcanic eruptions that would dump large amounts of carbon dioxide into the atmosphere, which, of course, would dramatically alter the end Triassic climate. This drastic climate shift would lead to the extinction of many groups, including large numbers of archosaurs. The only archosaurs that would survive the end Triassic extinction were the crocodylomorphs, the pterosaurs, and the dinosaurs.

5.5.2 The Jurassic Period (201–145 Ma) The first major split in the separation of Pangea led to a global mass extinction, but it was one that would provide an opportunity for the dinosaurs to become the dominant players on the world scene. They passed into the Jurassic relatively unfazed by the extinction event, and then, again probably because of reduced competition, they began to change, diversifying rapidly to fill every niche left empty by the demise of other archosaurs. As Pangea continued to split apart into the smaller continental landmasses that we know today, it would greatly shape dinosaur diversity and evolution. In the Triassic, dinosaurs could move across the entire globe unimpeded, and consequently, dinosaurs of this time period shared many features regardless of where they were found. As landmasses become further separated throughout the Jurassic and Cretaceous, these ocean separations would create increasingly distinct dinosaurian fauna in different parts of the world. Throughout much of the Jurassic, the world’s landmasses remained split into two large continents, Laurasia and Gondwana, which were separated by the young north Atlantic Ocean (Figure 5.29). The Jurassic climate remained warm, but humid and not as arid as the Triassic, allowing for widespread, lush forests that were filled with the dominant conifer trees. The oceans of the Jurassic were filled with marine reptiles, including ichthyosaurs, plesiosaurs, pliosaurs, and marine crocodiles (see  Chapter  10). Fish were abundant, along with modern-looking

5.5  The Mesozoic Era: Age of the Dinosaurs

121

Figure 5.29  Paleomap showing the continental arrangements during the Late Jurassic Period, 158.4 million years ago. The supercontinent Pangea

continues rifting, forming the ancestral Atlantic Ocean between the separating North American, Eurasian, and African plates. (Reprinted with permission from Chris Scotese.)

sharks and invertebrates like cephalopods (ammonites and belemnites). On land, the diversity of dinosaur evolution would be on full display, and dinosaurs begin to be a little more familiar. In the Jurassic, we see the peak of diversity for large, herbivorous sauropods such as Brachiosaurus, Brontosaurus, and Diplodocus, who thrived on the abundant vegetation of the Jurassic forests (see Chapter 9). Other herbivores of the Jurassic included Stegosaurs and some ornithopods like Camptosaurus and Dryosaurus (see Chapter 8). Preying on the herbivores were the large therapod carnivores of the Jurassic like Ceratosaurus and Allosaurus (see Chapter 9). Finally, the skies were also teeming with life as pterosaurs continued to diversify in the Jurassic and ruled the skies (see Chapter 10). But the pterosaurs of the Jurassic, shared the skies with the first avian dinosaurs, including the famous Archaeopteryx (see Chapter 19).

5.5.3 The Cretaceous Period (145–65 Ma) The Cretaceous Period would see the last remnants of Pangea finally split into the continents that we are familiar with today (Figure 5.30). The climate would become extremely warm and humid throughout the Cretaceous, after a brief cooling at the end of the Jurassic. Sea levels were very high in the Cretaceous due to high ocean temperatures (water expands when heated) and the rapid rate of seafloor spreading that was occurring as the southern Atlantic, Indian, and Antarctic ocean were forming due to Pangea splitting apart. This created vast shallow seas, including some that flooded the continental interiors. The Western Interior Seaway that would divide the North American continent into smaller land areas was one such example (Figure 5.30). Although conifers would continue to dominate the Early Cretaceous, a new player in the plant world, the angiosperms, were getting their start Figure 5.30  Paleomap of the Late Cretaceous Period some 86 million years ago. Pangea has fully split, resulting

in the continents we are familiar with today. Sea levels were high in the Cretaceous, and you can see the Western Interior Seaway that divided the North American continent. (Reprinted with permission from Chris Scotese.)

122

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

in the Early Cretaceous. Angiosperms are plants that produce flowers and fruit surrounding their seeds. As angiosperms began to diversify in the Early Cretaceous, they would go on to dominate the forests of the Middle to Late Cretaceous. Dinosaurs continued to diversify throughout the Cretaceous, and as the continents became more fragmented due to continental splitting and shallow seas (Figure 5.30), dinosaur faunas became more localized. Places like North America and Asia contained various herbivores like hadrosaurs, ceratopsians, and ankylosaurus alongside the predatory tyrannosaurs and maniraptorans. The southern continents were inhabited by titanosaurian sauropods and abelisaurid theropods (e.g., Carnotaurus). Mammals continued to live in the shadows of the dinosaurs and remained small. Although Pterosaurs continued to fill the skies, and reached their peak in size, their diversity was slowly declining as they competed with the efficient newcomers, the birds. Marine reptiles would continue to be major players in the Cretaceous seas. Although Ichthyosaurs became extinct in the Mid Cretaceous, Mosasaurs would take their place in the last 20 million or so years of the Late Cretaceous (see Chapter 10). The end of the Cretaceous Period would see the world experiencing another mass extinction, one of the five deadliest. This is the extinction event that would end the ~140 million-year reign of the non-avian dinosaurs. The plesiosaurs, mosasaurs, and remaining pterosaurs also reached their end in this extinction event. But accompanying the end of these lineages was the beginning of many more, as this extinction ushered in the Cenozoic Era, known as the Age of Mammals. For more on the Cretaceous/Paleogene extinction, see Chapter 20. We will end our walk through time here, at the end of the dinosaurs. However, many new and exciting events would happen throughout the Cenozoic Era. Mammals would take over as the dominant animals on the terrestrial stage, giving rise to such creatures as saber-toothed cats and woolly mammoths. Dinosaurs would make one final push for dominance in South America, however, in the form of terror birds. These were large (almost 10’ tall), flightless, carnivorous birds that filled the niche of the apex predators of South America. They would remain there until the isthmus of Panama formed about 2.7 million years ago, opening the door for North American mammals to travel south and outcompete the terror birds, driving them to extinction. Sadly, the reign of the magnificent dinosaurs ends with a tweet, from the only remaining dinosaurs, the modern birds.

5.6 WHAT WE DON’T KNOW The unanswered questions that exist from life’s 3.8 billion years on Earth are far too numerous to cover here. We will touch on three, two of the really big unanswered questions, and one related to dinosaur origins.

5.6.1 How, Where, and When Did Life Originate on Earth? A lot of progress has been made in the study of the abiotic synthesis of organic molecules necessary for life, but many questions still remain before we solve this great mystery. The mystery is multifaceted, raising a host of yet-to-be answered questions. Questions to consider: • Where on the early Earth did the first life evolve and what exactly were conditions like on this primitive Earth? • How early did life originate on Earth? We have very solid evidence that it was here by 3.5 billion years ago, and maybe even earlier.

5.6  What We Don’t Know

• If life originated on Earth as early as it could, does that mean life is a chemical inevitability if conditions are right?

5.6.2 How Did Eukaryotic Cells Arise? Although we didn’t cover the origin of eukaryotic cells in this chapter, they are cells with a defined nucleus that houses genetic material (DNA) and which is enclosed in a membrane. All multicellular organisms, including humans and dinosaurs, are eukaryotes. Prokaryotes (bacteria and archaea) do not have a nucleus or other organelles. There are hypotheses regarding how eukaryotic cells arose, but the origins of this major advance in life are not known, nor are any intermediates identified. One leading hypothesis for the origin of eukaryotic cells states that organelles like mitochondria and chloroplasts arose when one bacterial cell engulfed another, with the engulfed cell becoming the organelle. The evidence for this is that mitochondria have their own membranes and DNA and can replicate separately from the cell itself to meet changing energy needs. Questions to consider: • How did one cell engulf another when living bacteria are not capable of endocytosis (the process of a cell taking in matter)? • How could one cell have engulfed another and not digested it completely, but instead maintained it as a separate functioning part of the larger cell?

5.6.3 Why Were Dinosaurs Able to Survive the Triassic– Jurassic Extinction Event Relatively Unscathed, Unlike Other Triassic Archosaurs? Unlike most other archosaurs, dinosaurs were mostly un-impacted by the Triassic–Jurassic extinction event. Biologically and ecologically, they were not that different from many of their archosaur cousins at the time, mostly just smaller. But surviving allowed them to greatly diversify and become the giants that so capture our imaginations today. Questions to consider: • What was it about dinosaurs, compared with the other Triassic archosaurs, that made them able to survive the Triassic–Jurassic extinction? • If all Archosaurs had been wiped out, what would the Mesozoic world have looked like without dinosaurs?

CHAPTER ACKNOWLEDGMENTS We thank Dr. Jonathan Lindsey for his gracious review and suggested improvements to Sections 5.1 and 5.2. Dr. Lindsey is a Glaxo Distinguished University Professor in the Department of Chemistry at North Carolina State University.

INSTITUTIONAL RESOURCES University of California Museum of Paleontology: https​: //ev​oluti​on.be​rkele​y.edu​/ evo1​01/II​E2aOr​igino​flife​.shtm​l Life Through Time Exhibit: Natural History Museum Humboldt State University: http:​//www​2.hum​boldt​.edu/​natmu​s /e_L​ifeTh​rough​Time.​html

123

124

CHAPTER 5    How Do We Know When and How Life Began and Evolved?

LITERATURE Allwood, A. C., Rosing, M. T., Flannery, D. T., Hurowitz, J. A., and Heirwegh, C. M. (2018). Reassessing evidence of life in 3,700-million-year-old rocks of Greenland. Nature, 563(7730), 241.

Schopf, J. W. (1993). Microfossils of the Early Archean Apex Chert: New evidence of the antiquity of life. Science, 260(5108), 640–646.

Brasier, M. D., Green, O. R., Jephcoat, A. P., Kleppe, A. K., Van Kranendonk, M. J., Lindsay, J. F., Steele, A., and Grassineau, N. V. (2002). Questioning the evidence for Earth's oldest fossils. Nature, 416(6876), 76.

Schopf, J. W., Kitajima, K., Spicuzza, M. J., Kudryavtsev, A. B., and Valley, J. W. (2018). SIMS analyses of the oldest known assemblage of microfossils document their taxon-correlated carbon isotope compositions. Proceedings of the National Academy of Sciences of the United States of America, 115(1), 53–58.

Nutman, A. P., Bennett, V. C., Friend, C. R., Van Kranendonk, M. J., and Chivas, A. R. (2016). Rapid emergence of life shown by discovery of 3,700-million-year-old microbial structures. Nature, 537(7621), 535.

Weiss, M. C., Sousa, F. L., Mrnjavac, N., Neukirchen, S., Roettger, M., Nelson-Sathi, S., and Martin, W. F. (2016). The physiology and habitat of the last universal common ancestor. Nature Microbiology, 1(9), 1–8.

Patel, B. H., Percivalle, C., Ritson, D. J., Duffy, C. D., and Sutherland, J. D. (2015). Common origins of RNA, protein and lipid precursors in a cyanosulfidic protometabolism. Nature Chemistry, 7(4), 301.

6 6

HOW DO WE USE ANATOMY OF LIVING ANIMALS TO UNDERSTAND DINOSAURS? BONES AND ANATOMY

O

ften the only evidence we have for the existence of a dinosaur is the bones it leaves behind, and all that we know about them comes from traits expressed in the bones. If we know the size and shape of bones, where the joints are relative to the places where muscles attach, and how these features compare with living animals we can observe today, we can deduce (within reason) how these extinct animals must have moved. This is called functional morphology, a branch of biology that rests upon the principle that form determines function, and if you know the form, you can infer a function. This chapter will provide needed background on the form of bones and anatomy that will be helpful for discussions of function in later chapters.

6.1 ANIMAL CONSTRUCTION: TYPES OF TISSUE After reading this section you should be able to… • List the four types of organ tissue and give an example of each. • Describe the relationship between cells, organs, and tissues.

Vertebrate organisms, no matter how big or small, are organized into a hierarchy. At the smallest level, an organism is made up of cells (which themselves are made of the four biomolecules: carbohydrates, lipids, nucleic acids, and proteins). All cells that have a similar origin, and a similar function, form tissues. No matter where in the body they are located, there are only four tissue types. All four tissues must be present to make an organ.

IN THIS CHAPTER . . . 6.1 ANIMAL CONSTRUCTION: TYPES OF TISSUE 6.2 DEFINING AND CLASSIFYING BONE 6.3 WHAT DO BONES DO? 6.4 NAVIGATING THE SKELETAL MAP: REGIONS AND DIRECTIONAL TERMS 6.5 WHAT WE DON’T KNOW

126

CHAPTER 6    How Do We Use Anatomy of Living Animals to Understand Dinosaurs?

The four distinct tissue types are: • Epithelial: Tissues that cover and line organs. Generally speaking, epithelial tissues are leakproof. They can be found lining glands, blood vessels, etc., and they function to maintain a barrier between the organ and the environment (whether internal or external). In fact, the “leakproof” and covering features of epithelial tissues make them an integral part of the largest organ in your body—your integument (skin). • Nerve: Tissues that form the body’s communication network, which control and regulate its functions. For example, when you move your fingers, that is the result of nervous tissue transmitting electrical impulses between your fingers and your brain. • Muscle: Tissues that contract for movement. There are three types of muscle tissue: cardiac muscle, which controls the pumping of the heart; smooth muscle, which is responsible for automatic, involuntary movements (like squeezing food through your intestines); and skeletal muscle, striated muscle that you voluntarily control—to run, move your fingers to type, or shift your eyes to read these sentences. • Connective: Tissues that connect things, cushion things, insulate things, and/or support things. Connective tissues can be said to aid in communication by supporting nerve tissues. Most connective tissues consist of cells, and fibers and matrix secreted by those cells. Bone is a connective tissue. Multiple organs comprised of these four tissue types together form an organ system based upon an overall related function. For example, your mouth, teeth, tongue, salivary glands, esophagus, stomach, and intestines make up your digestive system, which functions to process food. Although your teeth differ in function, structure, chemistry, and composition from your stomach, they both act to break down food into usable parts. Thus, both are vital parts of the digestive system. All organ systems present in a body are needed for the organism to function. Your skeletal system is an organ system, thus, each bone comprising it (e.g., femur, scapula, radius) must have all four tissue types, the same as any organ. The most dominant tissue in the skeleton is connective tissue. In fact, we consider “bone tissue” to be a connective tissue itself. Bone tissue is made up of collagen fibers and a matrix containing these fibers, which are secreted by cells called osteocytes and osteoblasts. The collagen matrix secreted by these cells is mineralized, making bones rigid and strong, and enabling them to support the weight of vertebrate animals as they move. In addition to the connective bone tissue that makes up the majority of each bone in your body, blood vessels lined with epithelial tissue course through each bone. Very small smooth muscle cells surround each of these blood vessels, and, of course, muscles inserting on the bone are responsible for its movement. The functional unit of bone, called an osteon (a microscopic structure that looks like a bullseye) has a very small vein, artery, and nerve running through its center. If you have ever broken a bone, you know it contains nerve tissue—otherwise it wouldn’t hurt so bad. Because bone is a complex living tissue, it responds to stress. By looking at different aspects of bone in living animals, we can see how bones influence, and are influenced by, movement. Because of this, they hold an indelible record of the biology of all vertebrates. This understanding of the physics of movement and the cellular responses of bone is critical

6.2  Defining and Classifying Bone

to our interpretation of all aspects of dinosaur biology. We will address how we use bones to shed light on a dinosaur’s biology, physiology, evolution, and behavior in its environment in later chapters, but for now, it is important to establish some foundational principles and terminology about bone.

6.2 DEFINING AND CLASSIFYING BONE After reading this section you should be able to… • Describe the properties of bone, noting its primary constituents. • State the four categories of bone based on morphology and give an example of each. • Define the two types of bone development and bone tissue. • Explain how bone microstructure gives clues about animal physiology.

Let us start with a discussion of what bone is. Bone is a composite tissue, similar in some respects to plywood. It is comprised of both mineral (~60%) and protein (~20%), with the remaining ~20% being made up of mostly water, blood, and other components. The mineral portion, or “inorganic phase” of bone, consists of a specific mineral, made up of calcium and phosphate joined to form hydroxylapatite. The mineral component gives bone its hardness and provides resistance so muscle contraction actually gets you somewhere. Bone also serves the very important function of mineral storage, particularly of calcium. The rest of your bodily functions rely on this, because your muscles will not move and your heart will not beat without calcium. When it is not consumed in adequate quantities to continue these functions, the stored calcium in the bone can be utilized to make up the difference. In fact, it has been hypothesized that the mineral storage function of bone is probably what it was first used for, with movement facilitated by muscle acting on bone as a secondary function. The “organic phase” of bone is comprised mostly of the protein collagen I, though there are small amounts of other collagens and non-collagenous proteins present. The tough fibrils of collagen I form a framework for the bone as it is developing. Although highly organized, collagen is quite bendable and flexible and could never function in movement without an association with a hard mineral to provide resistance. Mineralization occurs when tiny crystals of hydroxylapatite align with collagen fibers, becoming intimately associated with the molecule. This association of organic fibers and mineral crystals makes bone rigid and hard, yet flexible and elastic, so it doesn’t (usually) snap when you twist an ankle or step down off a curb too hard. Together, these components make bone a very strong material that is rigid enough to support a body as immense as the largest sauropod, but also flexible enough to prevent catastrophic fracturing under the pressure and stresses of movement. Although many organisms have hard body parts comprised of both protein and mineral—clam and mollusk shells, for example—these are not bone, as these shells incorporate a different mineral (calcium carbonate). Only vertebrates possess the hydroxylapatite-collagen composite that is true bone. Thus, possessing bone tissue is a defining character (or autapomorphy, see Chapter 4) for this group. How bones are classified depends on the questions being asked about them; different questions will require different classification schemes. Bones can be classified by their chemical composition (i.e., collagen I

127

128

CHAPTER 6    How Do We Use Anatomy of Living Animals to Understand Dinosaurs?

and hydroxylapatite) at one level. Bones can also be classified by how their tissue is organized microscopically—what we see if we study bone using light microscopy or electron microscopy. Or, bones can be grouped according to how they are formed in embryos—your flat bones, like portions of the skull and pelvic bones, form by a very different process than the long bones of your limbs. We can categorize bones by types within a single bone—the ends of a long bone are structurally different than their shafts. But perhaps the most familiar way bones can be classified is according to their gross morphology—that is, their overall shape. Individual bones can be classified according to the following morphologies: • Long bones: Bones that are at least twice as long as they are wide. These include the bones that make up the forelimb (humerus, radius, and ulna) and hind limb (femur, tibia, and fibula) (Figure 6.1A). • Short bones: Bones that are longer than wide, but the ratio of length:diameter is closer to 1:1 than long bones. Short bones include bones in the arch of the foot (metatarsals) and palm of the hand (metacarpals), and fingers (phalanges) (Figure 6.1B). • Flat bones: Bones that are flat in shape and (relatively) thin. Whereas long and short bones are like rods, flat bones are more or less like plates. Examples include most of the bones in the skull, the shoulder blade (scapula), and bones in the pelvis (ilium, pubis, and ischia) (Figure 6.1A). • Irregular bones: Bones that don’t fit into the other categories and are “irregular” in shape, such as the ankle (tarsal) and wrist (carpal) bones, and the vertebrae (Figure 6.1B). Because not all bones form the same way, they can also be classified by their process of formation. Figure 6.1  (A) Human skeleton with examples of long bones in the arm (humerus, radius, ulna) and flat bones in the hip (pelvis) and shoulder (scapula) labeled. (B) Human foot with examples of short bones in the arch of the foot and toes (metatarsals and phalanges) and irregular bones in the ankle and heel (tarsals) labeled.

(Courtesy of Kaitlyn Tiffany.)

There are two types of bone development: • Intramembranous bones: These bones grow from within membranes. Early in development, cells specialize, and some become connective tissue cells. These cells have the potential to become bone cells or cartilage cells. They lie within membranes consisting of proteins, like collagen, and other components that the cells themselves secrete. When these cells are signaled by certain triggers within the developing embryo, they change directly into bone cells and begin secreting bone. Bones formed in this way only

6.2  Defining and Classifying Bone

129

grow in two dimensions (more or less), and they remain mostly flat—thus, flat bones (e.g., the scapula and ilium and many bones of the skull, see above) are intramembranous bones. • Endochondral bones: These bones form very differently than intramembranous bones. Rather than going from a non-differentiated connective tissue cell directly to bone cells, the cells first become chondroblasts, or cartilage-forming cells, and they make a small, three-dimensional model of the eventual bone. Cartilage is avascular and rather slow-growing, and doesn’t normally mineralize, so it would not be very useful for adult function. It would be a lot like trying to move your body by muscle action on Jell-O! This small cartilaginous model is invaded by blood vessels when it gets to a certain size and the blood carries bone cells and mineral into the cartilage model. The invasion of blood makes the cartilage die, and it is soon replaced by bone in the growing embryo. Thus, bones formed in this way from a cartilaginous precursor are called endochondral bone (“endo” = “within”; “chondro” = “cartilage”). We will come back to this later, in Chapter 18, when discussing dinosaur physiology and growth. Additionally, bones are not homogenous in structure. The texture of bone varies within a single element. Most individual bones contain two types of textures: • Cortical bone: A dense tissue that provides support and resistance. • Trabecular (spongy) bone: A lacy, delicate tissue that supports the soft tissues within bone that produce blood, and may also act to dissipate compressional forces acting on the bone. Also called trabecular, cancellous, or spongy bone. Figure 6.2 shows a rib bone in cross-section, so that both cortical and trabecular bone can be seen. At the microscopic level, bone is also categorized by texture. Cortical bone sliced thin and examined under a microscope in cross-section almost looks like it is filled with bullseyes. These circular structures are best seen in the cross-section of a cut long bone, and are called osteons (Figure 6.3). Osteons are comprised of layers of cells, separated by the

Figure 6.2  Cross-section of a dinosaur rib. Dense, compact cortical can be seen on

the outer edge; spongy trabecular bone is in the center. (Courtesy of E. Schroeter.)

130

CHAPTER 6    How Do We Use Anatomy of Living Animals to Understand Dinosaurs?

Figure 6.3  Thin section of a dinosaur bone showing the bullseye shaped osteons. At the center of the circular

osteon is the cross-section of the canal through which a small capillary, vein, and thin nerve would pass. The small black dots are the holes, or “houses”, that hold the bone-forming osteocytes. (Courtesy of Wenxia Zheng.)

bone matrix they secrete. At the center of the osteon is a circle (when cut in cross-section)—or a longitudinal tunnel that runs parallel to the length of the bone. This canal holds the veins, arteries, and nerves that supply the bone cells with nutrients and remove waste. The combination of bone matrix, cells, and the central canal with its vessels and nerves together make a Haversian system. The cells of bone are utterly unique among vertebrate cells. These cells are called osteoblasts (osteo = bone, blast = to form) when they are actively secreting bone matrix, and they are shaped rather like little cubes. But, as the matrix accumulates, the cells become trapped, and cannot move freely to exchange wastes into or get nutrients from the blood vessels. So, when embedded in bone, the cells elongate, taking on a roughly cigar shape, and from the cell “body”, hundreds of filopodia (little feet) extend into the surrounding matrix. These cells are then called osteocytes (osteo = bone; cyte = cell). It is through the filopodia that they communicate with osteocytes in the next layer, forming a cellular chain that acts like a “bucket brigade”, passing messages and nutrients from one cell to the next. When animals need the calcium stored in bone for growth, reproduction, or other metabolic processes, cells called osteoclasts (osteo = bone, clast = eater) secrete acid and enzymes to break down the bone, releasing calcium to the blood. This erodes the osteons, leaving big holes in the bone called “erosion rooms”. Then, when that metabolic need no longer exists, bone is once again laid down by osteoblasts—but the osteons, now called Haversian systems, are bigger than the primary osteons. They also have a defined border. So, when you see these secondary osteons in bone, you can tell that the bone belongs to older individuals. This process continues throughout life, so sometimes in the bones of old animals, you can see second, third, and fourth generations of remodeled and reformed osteons. This is one way we can use bone microstructure to infer things about extinct animal physiology, like growth rates, or ontogenetic age (see Chapter 18). Other physiological indicators include the changes in the bone when an animal begins to slow down its growth rate as it begins to reach maturity. Bone cells deposit bone very rapidly in young animals (or when

6.3  What Do Bones Do?

fractures are healing or in certain other conditions). A newborn human can triple its weight and add inches to its length in just a single year, requiring such rapid deposition of bone. But as animals reach maturity, bone growth slows dramatically, leaving lines, much like tree rings, on the outer surfaces of long bones. These are called lines of arrested growth, or LAGs. We will talk more about the physiological inferences we can make from these features in Chapter 18.

6.3 WHAT DO BONES DO? After reading this section you should be able to… • Describe five purposes that bones serve in living organisms.

Bones are important for many reasons, some of which are obvious; they provide protection for delicate internal organs, like the brain, spinal cord, and heart, and also provide an internal scaffolding to hold bodies up against gravity. But there are additional functions of the skeleton that are less obvious. Functions of the skeleton include: • Protect organs • Support the body against gravity • Provide attachment sites for muscles and resistance to contractions, resulting in movement • Store vitamins and minerals • Produce red blood cells While the first two are somewhat self-explanatory, we go into the last three in detail below.

6.3.1 Provide Attachment Sites for Muscles Bones provide a rigid surface that muscles require to act against for efficient movement. When you change a tire in a car, a jack (the muscle) must work against the rigid ground (bone) to gain leverage to lift the car. Bones form the rigid resistance to muscle action. Without bones, your muscles could still contract, but it wouldn’t result in directional movement (and you would look pretty weird as well!) Bones are the sites of attachment for muscle groups. Looking at the raised marks or “scars” these muscle attachments leave on bone is the primary way we infer musculature in dinosaurs, and from that, their movement and speed. Thus, understanding these bony features is key to understanding how dinosaurs moved. Each muscle is connected with tendons to two bony attachment sites— the origin and insertion. The origin is the bony attachment site that, when the muscle is flexed, doesn’t move, whereas the insertion is the one that does. Think about your biceps. Your bicep originates on your shoulder blade (scapula) and inserts on your forearm (radius). When you flex your biceps, what moves and what doesn't? Muscles can only contract. Thus, their origin and insertion on the skeleton define their range of motion, and by looking at only the bones, it is possible to approximate movement in any animal. Because contraction is all muscles do, most muscles have another muscle that works in opposition to the first. The biceps, for example, flex the arm, bringing your wrist and hand closer to the body. But if you want to extend your arm at the elbow, straightening your arm, the triceps must contract.

131

132

CHAPTER 6    How Do We Use Anatomy of Living Animals to Understand Dinosaurs?

6.3.2 Store Vitamins and Minerals Another function of bones is to store vital minerals and ions. For example, muscles, including the heart, will not contract without adequate supplies of calcium. Bones store calcium and phosphate, and the cells within bone live in a delicate balance between those types that lay bone down in the presence of extra calcium (osteoblasts, see Section 6.1), and those cells that dissolve bone to release calcium when needed (osteoclasts, see above). It has been proposed that the evolution of bone as a tissue was initially selected because of this vital need to keep a reliable calcium source in multicellular organisms that were becoming increasingly metabolically active. Fish, the first true vertebrates, are certainly more metabolically active than, for example, mollusks like clams.

6.3.3 Produce Red Blood Cells Finally, bones, mostly trabecular bone, house bone marrow. Marrow is a semi-solid tissue containing collagen and other proteins, but the main function of marrow is to produce blood cells. In adult mammals, marrow is mainly converted to fat, but can be reactivated when the need for new blood cells is great. Because marrow also contains fat, it is highly nutritious. When animals kill prey or scavenge, the inside of the bone is a prime target because of this, and they will break bone apart to access it. In addition to red blood cells, in mammals, the marrow is also an important part of the immune system.

6.4 NAVIGATING THE SKELETAL MAP: REGIONS AND DIRECTIONAL TERMS After reading this section you should be able to… • Explain two ways that a skeleton can be divided into regions. • State and define the four directional pairs that are used to identify bone locations in a skeleton. • Relate the position of one bone to another using appropriate directional terms.

Now that we’ve covered the different types of bones and bone tissues, we must consider how these bones are arranged in the skeleton. Depending on the aspect of the skeletal biology or function we are concerned with, we often divide the skeleton into distinct regions. One of the most common ways to divide the skeleton is into the axial skeleton and the appendicular skeleton. The axial skeleton includes the skull, spinal column (neck, back, and tail), and ribs. These elements together make up the axis of symmetry of the skeleton; if you draw a line down a vertebrate’s axial skeleton, each side will be a mirror image of the other (Figure 6.4). The appendicular skeleton includes the bones in the shoulder and pelvic girdles, arms, and legs—all the bones of the appendages. A general rule for remembering which category a bone belongs to is that if it is from a part of the body you have two of (e.g., arms, feet, hips, shoulders) then it’s probably from the appendicular skeleton. If it’s from a part of the body you have only one of (e.g., skull, rib cage, spinal column) it’s probably from the axial skeleton. Another way we can talk about regions of the skeleton is to talk about the cranial skeleton (which includes all the bones of the skull) and the post-cranial skeleton (which is all the rest of the skeleton except the skull, Figure 6.5). “Post-cranial” means “after the head”, and indeed, the

6.4  Navigating the Skeletal Map: Regions and Directional Terms

133

Figure 6.4  Skeleton of a bat with the axial skeleton outlined in yellow and the appendicular skeleton outlined in blue. (Courtesy of Kaitlyn Tiffany.)

Figure 6.5  Skeleton of a bat with the cranial skeleton outlined in yellow and the post-cranial skeleton outlined in blue. (Courtesy of Kaitlyn Tiffany.)

post-cranial skeleton is everything that comes after the skull. You might wonder why we would designate the skull alone as an entire “region” of the skeleton. Although it’s common to think of the skull as one skeletal element, there are many individual bones that make up the vertebrate skull (22 in humans, and around 30 in dinosaurs), and, considering the vast differences in head morphologies between some dinosaurs (e.g., T. rex vs. Triceratops) one can spend a lifetime discussing the crania of dinosaurs alone! Besides, many of the defining differences in dinosaurs (or indeed, most animals) reside in the skull. The post-crania of an Edmontosaurus and a Brachylophosaurus are not that much different, but their skulls vary significantly. Now that we’ve divided the skeleton into regions, like a geographic map we now need directional terms for navigating it if we want to discuss dinosaur anatomy. In geography, we use terms like east, west, north, and south. However, it’s important to note that these terms can’t stand alone, but are only used in relation to something else. For example, common geographical phrases referring to areas of the United States—“The East Coast”, “the South”, “the Pacific Northwest”—all use these directional terms in a way that only makes sense in relation to the United States as a whole and the geographic North. Anatomical directional terms are the same—they describe the positions of bones relative to other bones.

134

CHAPTER 6    How Do We Use Anatomy of Living Animals to Understand Dinosaurs?

Figure 6.6  Toy model of Allosaurus with cranial-caudal and dorsal-ventral anatomical terms labeling general regions of the body. Although the terms

are used here in relation to the animal’s whole body, remember that they can also be used when discussing the relative position of features anywhere inside the body as well. (Courtesy of E. Schroeter.)

Anatomical terms have complementary pairs, just like directional terms (e.g., east-west, north-south, left-right). Anatomical directional terms include: • Cranial-caudal: Cranial means “toward the head” and caudal means “toward the tail”. Thus, we use these terms to describe the position of things relative to the head or tail of a dinosaur. For example, the heart of a dinosaur is cranial to its hips, but caudal to its shoulders (Figure 6.6). • Dorsal-ventral: Dorsal refers to the top surface of an organism and ventral refers to the bottom surface of an organism. For example, a Stegosaurus has bony plates dorsally (i.e., on its back), but not ventrally (i.e., on its belly) (Figure 6.6). To help remember which is which, remember that sharks, whales, and dolphins have “dorsal fins” on their back. • Lateral-medial: Lateral and medial refer to the position relative to the midline of an organism. Imagine drawing a line from your nose straight down, dividing your body into right and left halves (Figure 6.7); this “midline”—is also called the “axis of symmetry” because we are symmetrical about this line. Lateral refers to something further away from the midline, and medial refers to something near the midline. For example, your ears are lateral to your eyes, and your nose is medial to your eyes. • Proximal-distal: Proximal and distal refer to the position relative to the body core (more or less the heart), where proximal is closer to the core and distal is further away from it (Figure 6.8). For example, the knee is proximal to the foot, and the wrist is distal to the elbow. Figure 6.7  This toy Stegosaurus shows lateral-medial anatomical directional terms. Although the terms are used here

in relation to the animal’s whole body, remember that they can also be used when discussing the relative position of features anywhere inside the body as well. (Courtesy of E. Schroeter.)

6.5  What We Don’t Know

135

Figure 6.8  Toy Brachiosaurus with proximal-distal anatomical directional terms. The proximal regions of the neck

and tail are closer to the body core; distal regions are further away. (Courtesy of E. Schroeter.)

These terms will be used throughout this text, so it will be helpful to become familiar with them. Because humans don’t have tails and walk fully upright, some terms that work well for dinosaurs (and almost all other vertebrates) don’t fully translate to our very unique posture. For example, whereas the top-most (dorsal) surface of all dinosaurs, dogs, cats, cows, etc. are their backs, and their bottom-most (ventral) surface is their belly, in humans, our backs/bellies are oriented perpendicular to the ground. So, for humans, we use the term anterior (front) and posterior (back) to refer to what is the ventral and dorsal surfaces in other organisms, respectively. This can get confusing, because some people tend to use anterior-posterior in humans interchangeably with cranial-caudal in other animals, even though they are not quite the same. Thus, for the remainder of this book, we will stick with cranial-caudal and dorsal-ventral when referring to dinosaurs.

6.5 WHAT WE DON’T KNOW 6.5.1 When Did the First Bone Tissue Evolve and How Did It Originate? We find fossils of bony fish very early in the fossil record, around 420 million years ago in the Late Silurian Period, but are they the first to have tissue bone? We are also not certain how mineralized tissue types like bone developed in the lineage leading to vertebrates. It is unclear what biological or environmental conditions triggered the mineralization of tissues, whether bone, which came later, or other minerals like calcium carbonate or aragonite, which are used by invertebrates. Questions to consider: • What was the driver for adopting calcium phosphate in bone mineral rather than calcium carbonate, which many other organisms use to mineralize hard parts? • What kind of advantages did bone confer on the first organisms to possess it?

136

CHAPTER 6    How Do We Use Anatomy of Living Animals to Understand Dinosaurs?

• How did animals go from an external (dermal) skeleton to an internal (endoskeleton) one? • What advantageous did an internal bony skeleton have over a bony dermal skeleton observed in early fish?

INSTITUTIONAL RESOURCES Wikipedia Glossary of dinosaur anatomy. A helpful reference that defines terms used in descriptions of dinosaur anatomy (https​: //en​.wiki​pedia​.org/ ​wiki/​Gloss​ary_ o​f_din​osaur​_ anat​omy).

LITERATURE Keating, J. N., Marquart, C. L., Marone, F., and Donoghue, P. C. (2018). The nature of aspidin and the evolutionary origin of bone. Nature Ecology & Evolution, 2(9), 1501.

Wagner, D. O., and Aspenberg, P. (2011). Where did bone come from? An overview of its evolution. Acta Orthopaedica, 82(4), 393–398.

7 7

HOW DO WE KNOW WHAT A DINOSAUR IS? DIAGNOSING AND DEFINING DINOSAURIA

W

hat exactly is a dinosaur? If you were to go out and ask people on the street if they know what a dinosaur is, most of them will say they do: dinosaurs are big, scaly, reptiles that have been extinct a long time…right? But “defining” or thinking about dinosaurs in this way leads to a lot of errors. Just because something is extinct doesn’t make it a dinosaur. Just because an animal lived during the Mesozoic Era doesn’t make it a dinosaur. Just because something is a “fossil” doesn’t make it a dinosaur. Like everything else in science, to discuss a topic, one must first define it. So what does make something a dinosaur?

7.1 DEFINING DINOSAURIA: DINOSAURS VS. DINO-NOTS After reading this section you should be able to… • Explain why classifying dinosaurs and building dinosaur family trees can be challenging.

IN THIS CHAPTER . . . Of the animals pictured in Figure 7.1, how many do you think are dinosaurs? If you separated some as not dinosaurs, on what criteria did you base your decision? Don’t get frustrated if you can’t determine the “dinos” from the “dino-nots” right away; “dinosaur” coloring books and toymakers have led generations of children astray with respect to the scientific definition of Dinosauria. For now, let’s take a look at some examples that are more familiar. What is the most general, and then most specific group into which you would place all of the organisms in Figure 7.2? From the smallest to the largest, you probably recognized all the animals in Figure 7.2 as dogs—even the ones that just came out of the bathtub. What traits do they all share that allow us to distinguish them from non-dogs?

7.1 DEFINING DINOSAURIA: DINOSAURS VS. DINO-NOTS 7.2 THE ANCESTRAL PATH: THE EVOLUTION OF DINOSAURIA 7.3 TRUE DINOSAURS: THE DINOSAURIA 7.4 THE DEFINITION OF DINOSAURIA 7.5 WHAT WE DON’T KNOW

138

CHAPTER 7    How Do We Know What a Dinosaur Is?

Figure 7.1  Of these 12 “dinosaur” toys, which ones actually depict dinosaurs? (Courtesy of E. Schroeter.)

Figure 7.2  What is the most specific group in which you can place all these animals? (Courtesy of Kaitlyn Tiffany.)

Let’s try another example. How would you identify the animals in Figure 7.3? Likely, you easily recognized them all as cats, even if you have never seen a hairless cat. Clearly, all of these cats—including the cartoon cats—share features that allow you to, consciously or unconsciously, group them together to the exclusion of dogs, mice, bears, or birds. This is the basic principle of how we group dinosaurs as well. There are a number of shared derived features, or synapomorphies (see Chapter 5),

7.2  The Ancestral Path: The Evolution of Dinosauria

139

Figure 7.3  What is the most specific group in which you can place all these animals? (Courtesy of Kaitlyn Tiffany; Felix the Cat created by Otto Messmer, public domain.)

that paleontologists have identified as belonging to all members of Dinosauria, and only Dinosauria, and the presence or absence of these features are used to diagnose whether or not something is a dinosaur. This might sound like a straightforward process, but there are a number of ways this can get complicated when trying to categorize extinct taxa. One big challenge is that taphonomic loss (loss of biological information after an organism’s death; see Chapter 11) usually leaves us with nothing but bone morphology on which to base definitions; the occasional (and exciting) preservation of soft tissues like skin isn’t common enough to rely upon for robust classification. Thus, we primarily rely on skeletal features to build dinosaur “family trees” and to differentiate the dinosaur branch from all other branches on the greater tree of life. The fact that we rarely find a complete skeleton of a dinosaur is another challenge in using skeletal features to classify dinosaurs; you can’t compare the bone morphology of two dinosaurs if you only find the arm and neck of one and the tail and leg of the other!

7.2 THE ANCESTRAL PATH: THE EVOLUTION OF DINOSAURIA After reading this section you should be able to… • State if dinosaurs belong to a certain taxon. • State particular features that would allow you to classify an organism as a member of each group listed below. • List four synapomorphies of archosaurs.

So where do dinosaurs fit in the tree of life in relation to other species? Let’s first get our bearings with the taxonomic classification of dinosaurs within living organisms.

140

CHAPTER 7    How Do We Know What a Dinosaur Is?

• Domain: Eukaryota • Kingdom: Animalia • Phylum: Chordata • Subphylum: Vertebrata • Superclass: Tetrapoda • Series: Amniota • Subclass: Diapsida • Division: Archosauria • Subdivision: Avemetatarsalia • Superorder: Dinosauria We’ve included here some of the most important groups to which all dinosaurs belong. So, let’s take a walk through the highlights of the dinosaur lineage, and discuss the derived traits along the evolutionary path to Dinosauria.

7.2.1 Eukaryota and Animalia Eukaryotes are organisms that are comprised of cells with nuclei and organelles. Fungi (including yeast), plants, and animals are all eukaryotes. Animals are multicellular eukaryotes that do not possess cell walls and cannot produce their own food (i.e., they’re heterotrophs). Sponges, clams, octopi, insects, worms, lizards, and mammals (and many other groups) are all animals. Hopefully, the placement of dinosaurs as animals isn’t a surprise!

7.2.2 Chordata Chordata is a group that includes all creatures with a notochord, a cartilaginous rod that, in more derived members of this group, helps to form the vertebral column. You, for example, have a notochord that became part of your spine while you were developing as an embryo, and so did dinosaurs. Extant (living) members of this group include tunicates (e.g., sea squirts) (Figure 7.4), lancelets, jawless fish (e.g., lamprey), cartilaginous fish (e.g., sharks), bony fish (e.g., goldfish), amphibians (e.g., frogs, salamanders), lizards, snakes, turtles, archosaurs (crocodiles and birds), and mammals.

Figure 7.4  A tunicate, or “sea squirt”.

Tunicates have a notochord, and thus are members of Chordata. However, they lack a vertebral column, and are therefore not members of Vertebrata. (Courtesy of Nick Hobgood; https://commons.wikimedia.org/ wiki/File:Tunicate_komodo.jpg.)

7.2  The Ancestral Path: The Evolution of Dinosauria

7.2.3 Vertebrata Vertebrates are animals that have both a notochord and a vertebral column (i.e., backbone). This excludes tunicates and lancets from this group. Vertebrata includes all animals that possess bony skeletons (like the ones of dinosaurs on display in museums), plus animals that have softer, cartilaginous skeletons. Extant members of this group include jawless fish (e.g., lamprey), cartilaginous fish (e.g., sharks and rays) (Figure 7.5), bony fish (e.g., goldfish), amphibians (e.g., frogs, salamanders), lizards, snakes, turtles, archosaurs (crocodiles and birds), and mammals. Only vertebrates possess true bone, which is a composite of specific proteins and a mineral called hydroxylapatite (see Chapter 6). We know that dinosaurs are members of this group because, beyond finding fossilized pieces of their vertebral column, we can also observe the microstructure of their fossilized bone tissue under the microscope and confirm that its microstructure is consistent with the true bone of living vertebrates.

7.2.4 Tetrapoda Tetrapods (tetra = four; pod = foot) are animals that have notochords, backbones, and four limbs, which allow them to live on land for at least part of their life cycle. Based on their many shared features, we know that tetrapods arose from a group of fish that had fleshy, lobed fins called Sarcopterygii (sarco = flesh, ptery = wing). The emergence of early tetrapods in the Paleozoic Era was a pivotal moment in Earth’s history, as it allowed vertebrates to invade terrestrial habitats for the first time. From this initial emergence, tetrapods became diverse and widespread, giving rise to species such as Cacops (Figure 7.6), an amphibian from the Early Permian. Extant members of this group include amphibians, lizards, snakes, turtles, archosaurs, and mammals. You may be asking why snakes are considered tetrapods. Even though living snakes no longer have limbs, their ancestors did. In fact, the skeletons of some pythons and boa constrictors still possess tiny pelvic bones in the abdomen (Figure 7.7), and some fossil snakes show tiny legs. Therefore, the loss of limbs in this group is a derived trait, a change that occurred in this lineage after it inherited a tetrapodal anatomy. Thus, snakes are still members of the group Tetrapoda. Remember, phylogenetics is focused on evolutionary relationships, so the evolutionary path that an animal took to arrive at its morphology is based upon what features it inherited from its ancestors, and is a vital part of determining its position on the tree of life.

7.2.5 Amniotes Amniotes are animals that have a notochord, backbone, four limbs, and produce eggs that are surrounded by three separate membranes (i.e., the Figure 7.5  A leopard shark (Triakis semifasciata), an example of an extant chondrichthyian—a fish with a cartilaginous skeleton. Sharks, frogs,

dinosaurs, and humans are all members of Vertebrata. (Courtesy of Kaitlyn Tiffany.)

141

142

CHAPTER 7    How Do We Know What a Dinosaur Is?

Figure 7.6  Skeletal cast of Cacops aspidephorus, an amphibious tetrapod from the Early Permian.

This doesn’t look like your average frog, however. What features do you think tell us that Cacops was an amphibian and not a reptile? (Courtesy of Kaitlyn Tiffany; skeletal cast imaged at the Field Museum.)

Figure 7.7  (A) Partial skeleton of an African Rock Python (Python sebae) showing vestigial pelvic bones. (B) Partial African Rock Python flesh mount. The yellow circle indicates the nub of the vestigial limb that is externally exposed. (Courtesy of Kaitlyn

Tiffany; images of skeleton and flesh mount taken at the Field Museum.)

Figure 7.8  Diagram of an amniote egg, showing the amnion, chorion, and allantois. The development of these

membranes allowed eggs to be laid in terrestrial environments. (Courtesy of CNX OpenStax; https://commons.wikimedia.org/ wiki/File:Figure_29_04_01.png.)

amnion, the chorion, and the allantois) (Figure 7.8). The development of these membranes meant that eggs could be laid in terrestrial environments without becoming desiccated (dried out), thus forever freeing this lineage from its dependence on water. Thus, amphibians are excluded from this group. Whereas tetrapods outside of Amniota (i.e., amphibians, such as frogs and salamanders) must lay their eggs in water for them to remain viable, the evolution of these egg membranes freed amniotes from this tie to the water and allowed them to occupy drier habitats. Another key feature that sets amniotes apart from amphibians is the possession of a secondary palate—which in humans is the bony ridge that forms the roof of your mouth. A secondary palate separates the nasal and oral cavities from each other, allowing amniotes to chew and

7.2  The Ancestral Path: The Evolution of Dinosauria

143

swallow while continuing to breathe. This adaptation made amniotes more efficient at utilizing food sources. Most amphibians can “breathe” through their skin (as long as it is wet) so this adaptation was not as important to them. Together, the hard palate and amniotic egg opened many new niches for amniotes, in which there had previously been no competition. Extant members of this group include lizards, snakes, turtles, archosaurs, and mammals.

7.2.6 Diapsida Amniotes can be further divided based upon features in their skulls— particularly in the number of holes they possess behind their eye socket (i.e., temporal fenestra) (fenestrae = window): anapsids, which have no temporal fenestrae; synapsids, which have one pair of temporal fenestrae; and diapsids, which have two pairs of temporal fenestrae. Turtles have relatively solid skulls in which the only openings are for the eyes (the orbits) and the nasal passages (the nares) (Figure 7.9). Based on this feature, they have historically been called “anapsids” (an = without, apsid = opening) and grouped separately from synapsids and diapsids. However, it is generally now thought that they represent a group of diapsids that have secondarily lost their temporal fenestrae. The exact placement of turtles within diapsids is still debated, as even genetic analyses of extant turtles have yet to fully determine where they fit relative to snakes, lizards, and archosaurs such as crocodiles (see below). Thus, while it is important to recognize that some taxa have no accessory fenestra in their head, it is not clear that the group “Anapsida” is really a valid group, though you may see it in some older textbooks and literature. Synapsids are a group of amniotes that have one pair of temporal fenestrae (Figure 7.10). Synapsids (syn = with, apsid = hole) include mammals— such as yourself—and their ancestors. It is at this point that the lineage leading to mammals separates from the dinosaur lineage. Synapsids include some animals you may have seen in your dinosaur coloring book, such as Dimetrodon (Figure 7.11). Although many people mistakenly believe they are dinosaurs, these sail-backed amniotes have only one pair of temporal fenestrae, and as synapsids they are more closely related to you than they are to dinosaurs, making them a “dino-not”! Diapsids (di = two, apsid = hole) are amniotes that have two temporal fenestrae (Figure 7.12), which allows a wider gape and stronger jaw muscles. Although some more derived dinosaurs lost some of these temporal fenestrae, and others gained more fenestrae, all dinosaurs evolved from an ancestor that was a diapsid. Extant members of Diapsida include lizards, snakes, and archosaurs. Extinct diapsids include dinosaurs, pterosaurs, and swimming reptiles such as mosasaurs, ichthyosaurs, pliosaurs, and plesiosaurs (Figure 7.13). Figure 7.9  Skull of a sea turtle illustrating the anapsid condition: no fenestrae (openings) aside from the orbits and nares. (A) Skull in cranial view. (B) Skull in lateral view. (Courtesy

of Kaitlyn Tiffany.)

144

CHAPTER 7    How Do We Know What a Dinosaur Is?

Figure 7.10  Dimetrodon skull (cast) illustrating the synapsid condition: one pair of temporal fenestrae, in addition to the orbits and nares.

(Courtesy of Kaitlyn Tiffany.)

Figure 7.11  Skeleton (cast) of Dimetrodon. Although they are commonly

mistaken for dinosaurs, these Permian synapsids are more closely related to you than to dinosaurs. (Courtesy of Kaitlyn Tiffany; skeletal mount imaged at the Field Museum.)

Figure 7.12  Iguana skull illustrating the diapsid condition. In iguanas and

many other extant diapsids (e.g., lizards and snakes), the lower bar of bone that encloses the bottom edge of the lateral temporal fenestrae (the lower opening) has been lost (represented by the dashed line). (Courtesy of E. Schroeter.)

7.2.7 Archosauria We are drawing closer to the dinosaur clade, but we aren’t quite there yet. Archosaurs are diapsids, but they have a few additional derived traits, both in their skull and in the rest of their skeleton, that unite them and separate them from other diapsids.

7.2  The Ancestral Path: The Evolution of Dinosauria

145

Figure 7.13  Cladogram showing the relationship between some familiar extant and extinct diapsids. Note that

turtles are shown in three different possible positions, as their exact evolutionary relationship within Diapsida is still unclear.

Archosauria synapomorphies include: • Antorbital fenestrae: A hole in front of their orbits, or eye sockets (ant = before, orbit = eye socket) (Figure 7.14). • Lateral mandibular fenestrae: A hole in the side (lateral surface) of their lower jaw (mandible) (Figure 7.14). • Teeth in sockets: The teeth of archosaurs are set in sockets within their jaws (Figure 7.15). This is called thecodont dentition, and having teeth firmly set in sockets makes these animals less prone to having their teeth ripped out during feeding. Although other groups, including mammals, developed this thecodont condition independently through convergent evolution, this is a derived state from more ancestral diapsids that all archosaurs share. Lizards, for example, have teeth only hooked into one side of the jaw, and rather than being set into the bone, their teeth have strong ligaments holding them in place • A fourth trochanter: A trochanter is a raised ridge, or process, on the shaft of the femur, below the hip joint, that provides a site for muscle attachment (Figure 7.16). This is important because it enabled archosaurs to stand and walk with their legs directly under their body. Thus, these animals were able to walk more upright, which both saves energy and makes them able to walk or run fast-

Figure 7.14  Skull (cast) of Cretaceous crocodyliform Mahajangasuchus insignis with fenestrae labeled. Note

that in Mahajangasuchus, observe both the two temporal fenestra that characterize diapsids, as well as the antorbital and lateral mandibular fenestrae that characterize archosaurs. Skull cast imaged at the Field Museum. (Courtesy of Kaitlyn Tiffany; specimen imaged at the Field Museum.)

146

CHAPTER 7    How Do We Know What a Dinosaur Is?

Figure 7.15  Skull of an American alligator (Alligator mississippiensis).

Inset shows a magnified image of the teeth, which are rooted in sockets. (Courtesy of Kaitlyn Tiffany; specimen courtesy of Adam Hartstone Rose.)

Figure 7.16  Alligator femur with fourth trochanter circled in red.

(Courtesy of Kaitlyn Tiffany.)

er than animals that possess a sprawling gait. The fourth trochanter first appears in the ancestor shared by crocodiles and dinosaurs, and as we will talk about later, a lot of extinct crocodiles walked upright, like dinosaurs, and were capable of running fast. However, crocodiles today are still very efficient, and can raise their bodies to walk and run upright in a way that non-archosaurs-like lizards cannot, making it quite possible for them to catch you on the golf course! It is important to know that archosaurs have “a” fourth trochanter, which is a type of trochanter, not the total number of processes they have on their femur. It is called “the fourth” to distinguish it from a femoral process some mammals have, called “the third” trochanter, which archosaurs do not have. Extant archosaurs include crocodilians (e.g., crocodiles, alligators, and gharials) and birds. Extinct archosaurs include a number of lineages of crocodile relatives, dinosaurs, and pterosaurs. Swimming reptiles such as mosasaurs, ichthyosaurs, and plesiosaurs (Chapter 11) are not archosaurs, but instead branch off in a variety of other diapsid groups, making them officially “dino-nots”. Lizards, snakes, and turtles also branch off here.

7.2.8 Avemetatarsalia Archosaurs are further divided into two main groups, on the basis of how their ankles move (Figure 7.17)! One group, the pseudosuchians, possess a crurotarsal ankle joint (cruro = crossed, tarsal = ankle bones) (Figure 7.17A), while avemetatarsalians developed a derived mesotarsal ankle with a single, planar hinge (Figure 7.17B). This planar hinge supports an upright posture, such as we observe in birds today, versus the more sprawling posture we observe in crocodiles. Despite the fact that “pseudosuchia” means “fake crocodile”, true crocodiles, alligators, and gharials are extant members of Pseudosuchia. Birds are the only living members of Avemetatarsalia, and dinosaurs and pterosaurs are extinct Avemetatarsalians.

7.3  True Dinosaurs: The Dinosauria Figure 7.17  (A) Diagram of a crurotarsal ankle, with the hinge running diagonally between the astragalus and the calcaneum. This type of ankle is found in members of Pseudosuchia, including living crocodilians. (B) Diagram of a mesotarsal ankle, with the hinge in a single plane underneath both the astragalus and calcaneum. This

type of ankle is found in members of Avemetatarsalia, including pterosaurs and dinosaurs. (Adapted from https​://uc​mp.be​ rkele​y.edu​/diap​sids/​archo​mm.ht​ml.)

In some older texts, the clade we now call Pseudosuchia was named Crurotarsi, and the Avemetatarsalia were called Ornithodira. These groups are largely synonymous, but the shifting of some taxa between clades has resulted in the latter names being less accurate. Thus, Pseudosuchia and Avemetatarsalia are currently the most accurate classification for these groups, and we will refer to them as such.

7.3 TRUE DINOSAURS: THE DINOSAURIA After reading this section you should be able to… • Describe the three features that an organism must possess to be classified as a dinosaur. • Differentiate ornithischian dinosaurs from saurischian dinosaurs, and identify which lineage led to modern birds.

From the vastness of all life, we have sequentially worked our way down through key synapomorphies that diagnose the clades in which dinosaurs are nested. Let’s take a quick review. Dinosaurs are multicellular, eukaryotic heterotrophs that: • Chordata: Have a notochord • Vertebrata: Have a backbone • Tetrapoda: Have four limbs • Amniota: Produce eggs with complex membranes that help prevent desiccation • Diapsida: Possess two temporal fenestrae • Archosauria: Possess antorbital fenestrae, lateral mandibular fenestrae, socketed teeth, and a fourth trochanter • Avemetatarsalia: Possess a planar (or hinged), rather than crossed, ankle joint These are all traits that dinosaurs inherited through their ancestors, and which together form this distinct lineage. Ancestrally, all dinosaurs must have them (or have had them and lost them later)—however, possessing these traits are not what diagnoses a dinosaur. Dinosaurs are diag-

147

148

CHAPTER 7    How Do We Know What a Dinosaur Is?

nosed by numerous synapomorphies throughout their skeleton, and the number and nature of those synapomorphies can and does vary as we find new, early dinosaur taxa, allowing us to refine our understanding of dinosaur evolution (and our cladograms). Here, we will focus on just three major dinosaur synapomorphies that set them apart from crocodiles and other archosaurs. To be a dinosaur, you must ALSO possess: • A perforated acetabulum: The rounded ball on the proximal end of the femur inserts into a little socket in the pelvis (i.e., the hip socket). This socket is called the acetabulum, which means “little cup” in Greek. In mammals, it is a solid, cup-like depression—you could drink from it! However, the hip sockets of all dinosaurs have a hole in them (Figure 7.18)—if you were to look into a dinosaur’s hip socket, you could see straight through. In fact, you can do this. Next time you eat a chicken or a turkey thigh, pull off the femur. Once you clear away the meat, you will be able to look at the rest of your dinner through the hip socket. This autapomorphy is unique to dinosaurs. It has been suggested that this adaptation, together with the fourth trochanter, enabled a fully upright posture in this group. • Asymmetrical fourth trochanter: All archosaurs possess a fourth trochanter, but in non-dinosaur archosaurs such as crocodiles, this process is rounded and symmetrical (Figure 7.16). In dinosaurs, the trochanter is distinctly asymmetrical (Figure 7.19). It’s been hypothesized that this asymmetry might have also played a role in supporting their fully upright posture. • Elongated deltopectoral crest: The deltopectoral crest is a ridge on the humerus (upper arm) that provides attachment sites for two muscles, the deltoid (on you, this is the muscle on the outside of your shoulder) and the pectoralis (your “pecs”), hence the term “deltopectoral”. A longer attachment site for these muscles suggests increased power in the forelimb (Figure 7.20).

Figure 7.18  Comparison of pelves from (A) a deer and (B) a turkey. The

acetabulum of the deer is closed, while the acetabulum of the turkey is perforated. (Pelves have been scaled for comparison and do not depict their relative sizes). (Courtesy of Kaitlyn Tiffany.)

7.3  True Dinosaurs: The Dinosauria

149

Figure 7.19  (A) Dinosaur femur (cast) with the fourth trochanter circled in red. (B) Magnified fourth trochanter from an alligator. (C) Magnified fourth trochanter from a dinosaur (cast). Note that the alligator fourth

trochanter is rounded and symmetrical, but in the dinosaur it is asymmetrical. (Courtesy of Kaitlyn Tiffany.)

Figure 7.20  (A) Humerus of a Maiasaurus skeleton (cast). (B) Maiasaurus humerus with deltopectoral crest labeled. (Courtesy

of Kaitlyn Tiffany; skeletal cast imaged at North Carolina Museum of Natural Sciences.)

The first true dinosaurs arose in the Late Triassic, about 230 million years ago. The earliest dinosaurs were carnivorous, bipedal, and small, and were relatively minor players, living in the shadow of the much more successful and diverse crocodilians (pseudosuchians) and therapsids (derived synapsids, also called mammal-like reptiles). From these humble beginnings arose a wide variety of dinosaurs, from ankylosaurs to velociraptors. Birds (or Aves) are the only group of dinosaurs still alive today. Modern birds evolved from a subset of dinosaurs, and we can still see the marks of this ancestry in their skeletons—such as the perforated acetabulum in your fried chicken. Conversely, pterosaurs, though closely related to dinosaurs, lack these dinosaur synapomorphies, making them “dino-nots”, just like the more distantly related mosasaurs, ichthyosaurs, and Dimetrodon. From here, dinosaurs split into two main groups: Ornithischia and Saurischia. In the next two chapters, we will talk about each of these groups in more detail, and discuss the synapomorphies that diagnose them and

150

CHAPTER 7    How Do We Know What a Dinosaur Is?

all their subgroups. For now, we’ll introduce one of the key differences between these groups: the shape of their pelvis. The pelvis in all vertebrates is made up of three bones (which are paired): • The right and left ilia (singular, ilium), which in humans is a bladelike bone where you carry your books and/or babies (colloquially called “the hip bone”). • The right and left ischia (singular, ischium), which in humans are the bones we sit on. • The right and left pubes (singular, pubis), which in humans is the bone you hurt if you stop too suddenly on your bike and slam into the crossbar! As early as 1887, Harry Govier Seeley recognized that the pelvic structures of dinosaurs fall into two broad categories: those that have their pubis pointing forward (Figure 7.21A), and those that have their pubis pointing backward (Figure 7.21B). Dinosaurs with a pubis that points forward have a pelvis that looks somewhat like a tripod (Figure 7.21A); dinosaurs with this hip configuration are called saurischians (saur = lizard, ischia = hip), the “lizard-hipped” dinosaurs. Those with a pubis that points backward, more-or-less parallel to their ischium (also called a retroverted pubis) are called ornithischians, which means “bird-hipped” (ornitho = bird, ischia = hip). These names were chosen because in birds, the pubis points backward; thus, ornithischians were named for the broad similarity of their pelvic anatomy to a bird. However, with more fossil discoveries, it was shown that birds are actually descendants of the “lizard-hipped” dinosaurs, not the “bird-hipped” ones! It turns out that within Saurischia, the lineage of dinosaurs that would eventually give rise to birds developed a retroverted pubis (Figure 7.22) convergently with ornithischians. This illustrates the type of confusion that can arise when we name groups according to their overall morphological similarities rather than their evolutionary origin.

7.4 THE DEFINITION OF DINOSAURIA After reading this section you should be able to… • Define a dinosaur!

Figure 7.21  (A) Pelvis of a Protoceratops (cast), an ornithischian dinosaur. The pubis is small and narrow, and in this dinosaur runs parallel to the much larger ischium; both point caudally. (B) Pelvis of a Daspletosaurus (cast), a saurischian dinosaur. The pubis, which is much larger

in Daspletosaurus and has a “pubic boot” on the end, is angled forward, whereas the ischium is angled caudally, forming an imaginary triangle with the ground. (Courtesy of Kaitlyn Tiffany; skeletal mounts imaged at the Field Museum.)

7.4  The Definition of Dinosauria

151

Figure 7.22  Pelvis of a Deinonychus, a saurischian dinosaur within the clade Maniraptora. Within this derived

group of dinosaurs, the pubis has shifted (retroverted) caudally, becoming parallel with the ischium. This is a condition that is convergent with ornithischians dinosaurs. Modern birds arise from within this group of dinosaurs, which is why birds are, confusingly, “lizard-hipped” dinosaurs instead of “bird-hipped” dinosaurs. (Courtesy of Kaitlyn Tiffany; skeletal mount imaged at the Field Museum.)

Thus far, we’ve discussed the traits, or synapomorphies, that diagnose, or identify, the clades that include dinosaurs, up to Dinosauria itself, and its members. However, this is not the same thing as a scientific definition of a group—just like the definition of a disease is not the same as the symptoms we use to diagnose it. For that, we need a concise description that unambiguously includes all members while excluding “dino-nots”. A clade is defined as the most recent common ancestor of the two most distantly related taxa to be included in the group and all its descendants. Therefore, scientific definitions of clades follow the format “The most recent common ancestor of Taxon A, Taxon B, and all its descendants”. Within Dinosauria, we generally consider the most distantly related branches of the dinosaur tree to be represented by Triceratops, a large, quadrupedal ornithischian dinosaur with an iconic three-horned face (see Chapter 8, Ornithischians) and modern birds, which are derived from a certain group of saurischian dinosaurs (see Chapter 9, Saurischia). Thus, the most widely accepted scientific definition of Dinosauria is “The most recent common ancestor of Triceratops horridus and Neornithes (extant birds), and all its descendants”. In one sentence, we have described every animal that can be considered a dinosaur, because only dinosaurs will have arisen from the most recent ancestor of T. horridus and birds (Figure 7.23). Furthermore, all dinosaurs will be included, even the gigantic long-necked sauropods and the broad-faced duckbills. Now that we know what a dinosaur is, let’s return to our earlier image of dinos and “dino-nots” (Figure 7.24). Knowing what you know now, which are dinosaurs, and which aren’t? What criteria did you use this time around? It turns out, only eight of the animals in Figure 7.1 are dinosaurs! You were probably able to figure this out based on what you’ve read in this chapter. But can you fully diagnose whether each toy is a dinosaur or not based only on the features present in a toy model?

152

CHAPTER 7    How Do We Know What a Dinosaur Is?

Figure 7.23  Cladograms of Dinosauria. Red arrows indicate the most

recent common ancestor of Triceratops and birds. Blue shading indicates all the descendants of that ancestor. These descendants represented all members included within Dinosauria. (A) Cladogram where Triceratops and birds are arranged at the outer branches of the tree. (B, C, D) Alternative arrangements where Triceratops and birds are not placed at the outer branches of the tree. It is important to know that despite the different ways these four trees are arranged, they all depict identical phylogenetic relationships.

Figure 7.24  Knowing what you know now, how many of these are members of Dinosauria? (Courtesy of E. Schroeter.)

7.5 WHAT WE DON’T KNOW 7.5.1 Believe It or Not, There Is Still Uncertainty in How We Classify Dinosaur Groups! As more and more dinosaur skeletons are found and described, the placement of groups within the Dinosauria lineage is likely to change. In particular, as we find more and more specimens closer to the base

7.5  What We Don’t Know

153

of the Dinosauria group (i.e., the common ancestor) it will be harder to be certain where they fit. For example, a recent scientific paper was published that argued for a rearrangement of the whole dinosaur tree, placing theropods more closely related to all ornithischians, while sauropods standalone (Baron et al. 2017). The authors have data to support their claim, but not all paleontologists agree with some of their interpretations of the data (Langer et al. 2017). Questions to consider: • What would be the implications for such a large rearrangement of the dinosaur tree? • What new discoveries will be made that could challenge how we classify dinosaur groups? • How many more groups of dinosaurs exist that we have yet to discover, and where would they fit in the dinosaur family tree?

LITERATURE Baron, M. G., Norman, D. B., and Barrett, P. M. (2017). A new hypothesis of dinosaur relationships and early dinosaur evolution. Nature, 543(7646), 501.

Langer, M. C., Ezcurra, M. D., Rauhut, O. W., Benton, M. J., Knoll, F., McPhee, B. W., Novas, F. E., Pol, D., and Brusatte, S. L. (2017). Untangling the dinosaur family tree. Nature, 551(7678), E1.

8 8

HOW DO WE NAME AND GROUP DINOSAURS? PART I: ORNITHISCHIAN DINOSAURS

I

n Chapter 7, we introduced the two lineages within Dinosauria: Ornithischia and Saurischia. In this chapter, we focus on the ornithischians, which include familiar favorites, such as Stegosaurus, Ankylosaurus, and Triceratops, as well as species that are less familiar (if you don't have a five-year-old child at home), like Ouranosaurus, Kentrosaurus, and Styracosaurus. As diverse and successful as they were, all ornithischians went extinct at the end of the Cretaceous, leaving no members of this lineage with living descendants. Thus, everything that we know about this group we must derive from the fossil record. Here, we take a brief and simplified walk through the main dinosaur groups that comprise Ornithischia, their basic features, and what we know about their phylogenetic relationships to each other. Now might be a good time to brush up on phylogenetic (Chapter 4) and anatomical terminology (Chapter 6) as such terms will be used extensively throughout this chapter.

8.1 ORNITHISCHIANS: DIAGNOSTIC CHARACTERS After reading this section you should be able to… • Describe the diagnostic traits of ornithischians. • Discuss the significance of ornithischian traits.

First, pelvic anatomy (as discussed in Chapter 7) is not the only thing that differentiates ornithischians from the other main branch of dinosaurs, the saurischians (Chapter 9). A number of synapomorphies diagnose this group. Ornithischian synapomorphies include: • A retroverted (pointing backward) pubis: As we discussed in the previous chapter, the pubis of all ornithischians points backward, resulting in the pubis and ischium being oriented close to parallel (Figure 8.1).

IN THIS CHAPTER . . . 8.1 ORNITHISCHIANS: DIAGNOSTIC CHARACTERS 8.2 THE ARMORED ORNITHISCHIANS: THYREOPHORA 8.3 THE BIRD FOOT ORNITHISCHIANS: ORNITHOPODA 8.4 THE FRILLED ORNITHISCHIANS: MARGINOCEPHALIA 8.5 ORNITHISCHIANS: DEFINITION 8.6 WHAT WE DON’T KNOW

156

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.1  Pubis of a Lambeosaurus (cast). In this and other ornithischian

dinosaurs, the pubis points backward (arrows indicate the caudal end of the dinosaur), nearly parallel with the ischium. (Courtesy of K. Tiffany, photographed at the Field Museum.)

Figure 8.2  Skull (cast) of a Maiasaura, with key ornithischian traits labeled, including a predentary bone and a jaw joint set below the level of the maxillary tooth row. (Courtesy of K.

Tiffany, photographed at the North Carolina Museum of Natural Sciences.)

• A predentary bone: This is an “extra” or accessory bone at the very front of the lower jaw (Figure 8.2). Dinosaurs have multiple bones in their lower jaw, but the one bone holding the teeth is called the dentary. The bone anterior to this in ornithischians, then, is called the predentary. • A jaw joint set below the maxillary tooth row: In ornithischians, the joint where the lower jaw articulates with the skull is lower than their upper row of teeth (Figure 8.2). • Ridged teeth: In both the maxilla (upper jaw) and dentary (lower jaw), the teeth are ridged (Figure 8.3) and look a bit like leaves. Some bear tiny little bumps (denticles, meaning “little teeth”—on

8.1  Ornithischians: Diagnostic Characters

their teeth!) on the sides that help to break apart tough plant materials. • A loss of gastralia: Gastralia are “stomach ribs” that are present in saurischians and other animals outside of Dinosauria (Figure 8.4), including crocodiles, so we know having them is an ancestral state for dinosaurs. The common ancestor of all ornithischians lost this trait; therefore, ornithischians do not have them. • Ossified tendons: One of the most obvious traits of this group is that they have tendons along their tail that wrap the vertebrae tightly and hold them in place. In adults, these tendons become ossified; that is, they become mineralized like bone (Figure 8.5) Although some saurischian dinosaurs and birds convergently develop similar ossified tendon tissue, it occurs in different parts of the body, such as the neck and lower limbs. Now that we’ve listed these diagnostic traits of Ornithischia, let’s discuss the biological significance of some of them—in other words, let’s answer the question “what are these traits good for, anyway?”

8.1.1 Traits Associated with Herbivory Thus far, all members of Ornithischia that have been discovered are plant eaters. Although a few ornithischians are proposed to have been omnivorous (e.g., a few species of heterodontids), no carnivores have been identified in this group, and the vast majority of the known species are herbivores. This conclusion is based upon the numerous adaptations to ornithischian skeletons that can be correlated to herbivory, some of which are diagnostic for this group. Thus, although the earliest dinosaurs were carnivores, these shared features within Ornithischia indicate that the most recent common ancestor of all ornithischians had developed the ability to eat plants, a derived trait for vertebrates. But what are these features? First, the pubis, which together with the ilium and ischium, forms a tripod in saurischians, is angled caudally (backward) in ornithischian dinosaurs (Figure 8.1). This is called retroversion (a word that means “to turn backward”). As we will discuss in more depth in Chapter 15, plants are less nutritious than meat, and a plant-based diet usually requires that plants stay in the gut a long time to extract all the nutrients available. This requires the intestines to be longer and more complex, and to hold dietary plant matter longer for extended processing. This, in turn, requires a large space for the gut.

Figure 8.3  Hadrosaur tooth showing the ridges (yellow arrows) typical of ornithischian teeth. (Courtesy of K.

Tiffany.)

Figure 8.4  Skeleton (cast) of Daspletosaurus, a saurischian dinosaur, with gastralia mounted.

Ornithischian dinosaurs do not have gastralia. (Courtesy of K. Tiffany, photographed at the Field Museum.)

157

158

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.5  Tail of a hadrosaur (ornithopod) dinosaur. Arrow points to

ossified tendons running in rows along the neural spines of the caudal (tail) vertebrae in a crosshatched pattern. (Courtesy of M. Schweitzer, photographed at the Great Plains Dinosaur Museum and Field Station with thanks to C. Woodruff.)

A retroverted pubis, turned backward and out of the way, allows room for a larger gut. The loss of gastralia in ornithischian dinosaurs is also associated with a larger gut space. Gastralia are accessory ribs, or “stomach ribs”, that run along the ventral margin of the body (Figure 8.4). Early dinosaurs and many saurischians possess gastralia (though they are lost in sauropods). From this, we can infer that the common ancestor of dinosaurs likely had gastralia. Their loss in ornithischians allows space for a larger digestive system and is a derived trait for this group. The morphology and modifications of the teeth and jaws of ornithischians also point to an herbivorous lifestyle, particularly when compared with animals that did not possess these features. These modifications are particularly prominent in later, more derived ornithischians, and allow much more efficient food processing. The denticles on their teeth aided in ripping and shredding tough plant material for easier digestion and extraction of nutrients. The articulation of the jaw joint at a point lower than the upper row of teeth (the maxillary tooth row) (Figure 8.2) allows the jaw to swing in such a way that the teeth occlude (close together) in one long, simultaneous grinding surface. Finally, in later members of this clade, their jaws contain dental batteries, where row upon row of teeth exist in the jaws, so when one tooth is lost or broken because of tough-textured plants, another moves up to take its place, superficially similar to shark teeth.

8.1.2 Posture The vertebrae that make up the tails of ornithischians are reinforced by a woven network of tendons that lie against the neural spines (dorsal projections) of the vertebrae (i.e., the part that sticks up and out). These tendons ossify, losing their flexibility and becoming rigid bone tissue. This greatly limits the range of motion of their tail. One thing is certain—these dinosaurs could not possibly have dragged their tails. Unless the tail (and back) were broken, they would have had to hold their tails straight out behind them, acting as a counterbalance. The old idea that dinosaurs were slow-moving and dragged their tails, like lizards, was refuted by this kind of evidence. Currently, there are no Triassic dinosaur remains that can be definitively placed within Ornithischia, but this does not mean that there were no ornithischian dinosaurs during the Triassic Period. The absence of fossil evidence could be due to gaps in the fossil record, and because Triassic rock exposures are not as well-studied as later Mesozoic era deposits. Basal ornithischians were almost certainly present, waiting to be found.

8.2  The Armored Ornithischians: Thyreophora

159

Figure 8.6  A cladogram depicting the major groups within Dinosauria. Here,

the ornithischian clade of dinosaurs, which we discuss in this chapter, is highlighted.

Lesothosaurus, a very basal ornithischian, comes from the earliest Jurassic of South Africa (195–206 Ma). After the first appearance of such generic, early ornithischians, the clade split into three major groups: Thyreophora, Ornithopoda, and Marginocephalia (Figure 8.6). We will look at each of these important groups individually.

8.2 THE ARMORED ORNITHISCHIANS: THYREOPHORA After reading this section you should be able to… • Identify the earliest members of this group. • Name the two derived groups of Thyreophorans. • Describe characteristics of the two derived groups of Thyreophorans, and name a common species of each group. • Draw a simple cladogram showing the relationship of Thyreophora clade members.

Thyreos is Greek for “shield”. Thus, Thyreophora means “shield bearers”, a name that refers to a common feature shared by all members of this group—they possess bony plates and spikes on their skulls and/or small bones embedded within their skin that have been hypothesized to function as a form of armor. These are the armored dinosaurs! The cladogram depicting ornithischian taxa (Figure 8.7A) shows that the thyreophorans make up the basal group of ornithischian dinosaurs. Within Thyreophora, we observe two main branches: Stegosauria and Ankylosauria (Figure 8.7B). Ankylosauria can be further divided into ankylosaurs and nodosaurs. Thus, Stegosaurus and Ankylosaurus, dinosaurs that may be familiar from coloring books, are more closely related to each other than either of them are to any other group of dinosaurs. In general, thyreophorans looked and functioned like armored dinosaur tanks. Although most of the later and/or more derived thyreophorans were heavy, quadrupedal, and rather slow-moving, early members of the group were bipedal, like their ancestors. All known thyreophorans were herbivorous and had distinctive, leaf-shaped teeth (Figure 8.8).

160

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.7  (A) Cladogram depicting the placement of the group Thyreophora (highlighted) within the ornithischian clade. (B) Cladogram of Thyreophora. This group includes

basal members, such as Scutellosaurus, as well as two main groups: Stegosauria and Ankylosauria. Ankylosauria is further divided into Ankylosauridae and Nodosauridae.

Figure 8.8  Multiple views of teeth from Paranthodon, an Early Cretaceous ankylosaur. Ankylosaur

teeth are small, ridged, single-rooted, and vaguely leaf-like. The roots are narrow and firmly set in the bone in a socket. (Courtesy of T.J. Rave and S.C. Maidment, 10.7717/ peerj.4529/fig-5.)

Figure 8.9  (A) Silhouette and skeletal elements of Scutellosaurus lawleri, which shows the beginnings of small osteoderms over some of the dorsal vertebrae. (B) Fleshed-in reconstruction of Scutellosaurus showing the typical dermal armor that is a synapomorphy for this clade. (A courtesy of J.A. Headden,

https://commons.wikimedia.org/wiki/ File:Scutellosaurus_lawleri.jpg; B courtesy of N. Tamura, https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=19​46233​7.)

All thyreophorans had bone embedded within their skin. In different thyreophoran clades, these take on different shapes. Some were flat disks, some were upright plates, and some were sharp spikes, but the presence of these dermal bones is a synapomorphy that unites this “armor bearing” clade. This dermal armor can appear very different in different species, but it is always present to one degree or another. All thyreophorans have at least one row of bony plates running parallel to their vertebral column. The earliest recognized thyreophoran is Scutellosaurus (Figure 8.9), a small bipedal dinosaur with bony plates in its skin. In Scutellosaurus and other closely related species, these plates are quite small and not fused

8.2  The Armored Ornithischians: Thyreophora

161

Figure 8.10  (A, B) Dermal armor in the nodosaur Borealopelta markmitchelli. Borealopelta is completely covered with individual plates of bone, some of which are keeled, and long shoulder spikes. This varies from the dermal armor observed in Stegosaurus (C, D), where armor is limited to vertical plates that run along the spinal column, and small, pavement like plates covering the neck. (A and B courtesy of Caleb

Brown, 10.7717/peerj.4066/fig-3; C and D photographed by M. Schweitzer at the Smithsonian Institution.)

together—they only hint at the large, fused plates that form the heavy armor seen in later groups. After the group containing Scutellosaurus diverges, we come to the derived group Eurypoda (Figure 8.7B), which unites two groups of dinosaurs we are interested in: Stegosauria and Ankylosauria. These two groups can be differentiated by the arrangement and extensiveness of bony plates on their back. In ankylosaurs, dermal plates are oriented flat against the body, whereas in stegosaurs they are often upright and pointed (Figure 8.10).

8.2.1 Stegosauria The most well-known member of the group Stegosauria (Figure 8.11) is Stegosaurus (Figure 8.12), a dinosaur that possesses large, vertically oriented, and roughly triangular bony plates on its back and dermal spikes on its tail. The function of these in the living animal has been the topic of much discussion. What did it use these bizarre features for? There are a number of hypotheses that have been put forth to explain the function of the vertical dermal plates of Stegosaurus. One hypothesis is that the plates served as protection and defense against predators. Certainly, it would be hard to take a bite out of the back of a stegosaur without either being poked by the pointy plates or getting a mouthful of bone

Figure 8.11  Cladogram of Thyreophora showing the placement of Stegosauria (highlighted) within the group.

162

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.12  Skeleton (cast) of a Stegosaurus, showing the vertically oriented dermal plates that characterize members of Stegosauria.

(Photographed by K. Tiffany at the Field Museum.)

and no meat. Another hypothesis is that they served a thermoregulatory purpose, similar to an elephant’s large ears. Because the plates are covered with grooves for blood vessels, it is possible that blood running across the wide, flat surface area of the plates could either be warmed (if basked in the sun) or cooled (if exposed to the wind). However, if these plates were indeed used for defense, it would be a huge disadvantage for them to be infused with a large number of blood vessels, because a bite on these bony plates could well lead to death by hemorrhaging! Yet another hypothesis is that the plates were used for species recognition or sexual display. Although it might be tempting to think that the dermal plates of all stegosaurs have the characteristic pattern of those in Stegosaurus, less famous members of this group vary widely in plate morphologies and placement on their backs, hips, tails, and shoulders. For example, Kentrosaurus aethiopicus (Figure 8.13) has narrower plates than Stegosaurus, and these fuse into spikes all the way to their hips instead of just at the tip of their tail. They also had a rather intimidating spike jutting out of each shoulder that is absent in Stegosaurus. Different plate morphologies in each of the stegosaur groups may indicate that the distinct patterns were utilized to help individuals recognize members of their own species—and potential mates--similar to how songbirds use distinct songs. Possible evidence that dermal plates were used for sexual display is that these plates are not well developed in juvenile stegosaurs; rather, they begin to expand later in life. This pattern is consistent across species for secondary sexual characteristics (see Chapter 17). Which hypothesis is correct—defense, thermoregulation, display, or something else? We still don’t know! It is possible (and indeed likely) that the plates had multiple functions. Only with more specimens can we eliminate some of these hypotheses and support others. The tail spikes of Stegosaurus and other stegosaurs have been hypothesized to have been utilized for intra- or interspecific combat. Their use

8.2  The Armored Ornithischians: Thyreophora

163

Figure 8.13  An articulated mount (cast) of the stegosaur Kentrosaurus.

One of the features that differentiate Kentrosaurus from the more popular Stegosaurus is the very long and pointed process off its shoulder. Another is the extent of tail spikes proceeding up the tail to beyond the hip. What features unite this animal with other stegosaurs? (Modified from LoKiLeCh, https://commons.wikimedia. org/wiki/File:Berl​in_Na​turku​ndemu​seum_​ Dino_​Einga​ngsha​lle.j​pg.)

as weapons, either defensive or offensive, was suggested when an Allosaurus tail vertebra was discovered with puncture wounds that seemed to perfectly fit a Stegosaurus tail spike (Figure 8.14). Whether this was indeed made by a tail spike, or other causes, is still debated. It is interesting, however, that the tails of stegosaurs lacked the ossified tendons characteristic of most ornithischians. The loss of these stiffening rods would have provided increased flexibility of movement required for swinging their tails around.

Figure 8.14  The neural process of this allosaur tail vertebra shows a split that is consistent in size and shape with the tail spikes of a Stegosaurus.

This is one possible interpretation, but because the tail spike was not found in direct contact with the vertebra (contrary to what is shown here), it is possible the wound could have a different cause. In any case, this vertebra shows signs of healing, indicating that this wound was not initially fatal. (Photographed by D. Czajka at the Utah State University Eastern Prehistoric Museum.)

164

CHAPTER 8    How Do We Name and Group Dinosaurs?

Some paleontologists affectionately call the cluster of tail spikes at the end of stegosaurian tails “thagomizers”, an informal term adopted from a The Far Side cartoon drawn by Gary Larson in which the spikes are given the moniker by cavemen researchers in honor of a caveman that was killed by them, “the late Thag Simmons”. Humans never interacted with Stegosaurus (or any non-avian dinosaur) but despite this inaccuracy, the cartoon humorously points out something correct: this arrangement of spikes on the stegosaur tail is a morphological structure unique to this group within all of Animalia, and it did not have a name, so perhaps “thagomizer” will stick! (Figure 8.15).

In addition to the two vertical rows of osteoderms running down the spine, derived stegosaurs also have front limbs that are markedly shorter than their hind legs, and femora that are substantially longer than their tibiae (Figure 8.12). What does this say about the ability of members of this group to run (see Chapter 13)?

8.2.2 Ankylosauria Although both stegosaurs and ankylosaurs belong to the armored group Thyreophora, the members of Ankylosauria (Figure 8.16) are the true Figure 8.15  “Thagomizer” is an informal term used by some to indicate the cluster of spikes at the end of stegosaurian tails.

(Photographed by K. Tiffany at the Field Museum.)

Figure 8.16  Cladogram of Thyreophora depicting the placement of Ankylosauria (highlighted) within this group. Note that Ankylosauria further

divides into the groups Ankylosauridae and Nodosauridae.

8.2  The Armored Ornithischians: Thyreophora

165

tanks of this group. Ankylosaurs take dermal armor to the extreme and possess bony plates across most of their bodies. In fact, a distinctive trait that sets this group apart from other thyreophorans is the fusion of this dermal armor to the bones of their skull, which causes them to secondarily lose all the holes ( fenestrae) in the skull that are typical for diapsids and archosaurs, leaving only their eye sockets and nares open (Figure 8.17). The extensive nature of the dermal armor is the reason that the group (and the type species) received its name, “fused lizard” (ankylo = fused, saurus = lizard). Ankylosauria is further divided into two main groups, even though these are very closely related: Nodosauridae and Ankylosauridae (Figure  8.17). Ankylosaurids possess the iconic bony club at the tip of their tail (Figure 8.18), which has been hypothesized to have been used for either self-defense, display, or both. The armor within this group becomes so extensive that some specimens have been found with bony eyelids! Ankylosaurid species include Zuul crurivastator (Figures 8.18 and 8.19), Gastonia burgei, and of course, Ankylosaurus magniventris. Conversely, nodosaurids do not have tail clubs—making it easy to distinguish them from ankylosaurids. Nodosaurs do, however, possess a pronounced collar of spikes around their neck and shoulders (Figure 8.19). The extent, size, and number of these shoulder spikes differ, but all nodosaurs have some version of these bony extensions. Nodosaur species include Animantarx ramaljonesi, Edmontonia ­longiceps, Borealopelta markmitchelli (Figure 8.19), and Nodosaurus textilis.

Figure 8.17  Skull of ankylosaur Zuul crurivastator, showing the fusion of dermal armor to the skull and the loss of all fenestrae except their orbits and nares. (Courtesy of the Royal Ontario

Museum © ROM.)

Figure 8.18  Tail club of ankylosaurid Zuul crurivastator. (Courtesy of the Royal

Ontario Museum © ROM.)

166

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.19  Preserved Borealopelta showing the shoulder spikes characteristic of nodosaurids.

(Photographed by M. Schweitzer at the Royal Tyrrell Museum of Paleontology with permission from C. Brown.)

8.3 THE BIRD FOOT ORNITHISCHIANS: ORNITHOPODA After reading this section you should be able to… • Discuss the synapomorphies that make Ornithopoda unique from other ornithischians. Figure 8.20  (A) Cladogram depicting the placement of the group Ornithopoda (highlighted) within the ornithischian clade. Ornithopoda is the sister group to Marginocephalia within the clade Cerapoda. (B) Cladogram of Ornithopoda. This group includes basal

members, such as Gideonmantellia, as well as successively more derived groups, such as Styracosterna, Hadrosauridae, and Saurolophidae. Saurolophidae divides into two sister groups: Saurolophinae and Lambeosaurinae.

• Describe characteristics of the three derived groups of ornithopods and name a common species of each group. • Draw a simple cladogram showing the relationship of Ornithopoda clade members.

After the divergence of the Thyreophora, there remain two major lineages within Ornithischia: Ornithopoda and Marginocephalia. These two lineages are united as sister groups within the clade Cerapoda (Figure 8.20)—meaning that ornithopods (like Iguanodon) and marginocephalians (like Triceratops) have an ancestor in common more recently, and thus are more closely related to each other than either of these groups are to thyreophorans like Stegosaurus and Ankylosaurus.

8.3  The Bird Foot Ornithischians: Ornithopoda

167

Ornithopoda (Figure 8.20B) is a group of ornithischians that includes some of the most comprehensively studied dinosaurs, in part because there are so many of them, and because some exhibit exceptional preservation. Death assemblages of very large ornithopod herds that include hundreds of individuals of the same species have been discovered. These massive assemblages have allowed some of the first population studies on dinosaurs. Because of the sheer number of individuals in one place, all from the same species over a range of different ages, scientists can identify traits that may be correlated with still-growing juveniles, or fully mature adults. Some ornithopod species are known from exquisitely preserved skeletons—many still in articulation, and some retaining stomach contents, skin or skin impressions, and other original “soft tissue” features—as well as eggs and nests. Thus, there is a lot of information preserved in the fossil record about how members of this diverse, successful group of dinosaurs lived. Traits historically used to define Ornithopoda have changed as we’ve discovered new specimens. Many dinosaurs once considered basal ornithopods, like Hypsilophodon, have been removed from this group entirely. As a result, the diagnosis of this group has recently been in a state of flux. Some features that are currently considered synapomorphies for all ornithopods include an ischium with a shaft that is round in cross-section, and a femur longer than their tibia (Figure 8.21). It was long thought that members of Ornithopoda had pleurokinetic (pleuro = side, or lateral; kinetic = movement) skulls. This complicated word means that their jaw joints allowed them to have additional planes of movement beyond just up and down. In particular, the upper jaws of ornithopods could swing a little out to the sides (laterally) while chewing. This allowed their maxillary teeth in their upper jaw to shear against their mandibular teeth in a long stroke, greatly expanding the cutting/ grinding surface. This pattern of chewing was much more advanced compared with other ornithischians. This hypothesis for skull movement was based in part on the wear facets observed on their teeth—that is, the patterns of how their teeth had been ground down by chewing. The wear facets we observe on ornithopod teeth seem to support this pleurokinetic jaw movement. However, when high-resolution CT was used to image and reconstruct proposed pleurokinetic joints in the skulls of many ornithopods, and their features were compared with living animals that we know have kinetic skulls (e.g., birds, snakes), full movement in these joints was not supported. More recently, some have suggested that rather than the upper jaws swinging outward, ornithopods might have exploited a mobile joint between their predentary and dentary to rotate their lower jaws inward as

Figure 8.21  Skeleton of the ornithopod Parasaurolophus. The

shaft of the ischium, which is rounded in cross-section in ornithopods, is labeled. Additionally, the femora are longer than the tibiae. (Photographed by K. Tiffany at the Field Museum.)

168

CHAPTER 8    How Do We Name and Group Dinosaurs?

they chewed. Although the exact nature of their feeding mechanism is still being debated, the fact that ornithopods—and especially derived ornithopods—were master food processors is clear.

8.3.1 Styracosterna Members of the derived group of ornithopods, Styracosterna (Figure 8.22), are characterized by a number of morphological features. First, their metacarpals (bones that, in you, form the palms of your hands) for digits II–IV become compressed together, forming a narrow column in the middle of their hand (Figure 8.23). This is thought to be an adaptation for weight-bearing in the arms, allowing members of this group to become facultative quadrupeds, whereas Figure 8.22  Cladogram of Ornithopoda indicating the members of Styracosterna (highlighted) within the group.

Figure 8.23  Manus (hand) of Maiasaura (cast). iArrow indicates

the metacarpals, which are compressed together and form a narrow column in members of the clade Styracosterna. (Photographed by K. Tiffany at North Carolina State Museum of Natural History.)

8.3  The Bird Foot Ornithischians: Ornithopoda

169

earlier ornithopods were obligate bipeds. Digits II–IV were, in some members of this group, even bound together with a fleshy covering, leaving a single mitten-like print in trackways (Figure 8.24). Additionally, their toes were broad and shortened, and the unguals (most distal bone in each digit) were covered in a hard keratinous sheath, rather similar to what we see on horse toes. The feet may have had thick pads of cartilage under the bones, to cushion them, as seen in camels or elephants today (Figure 8.25). The best-known representative of this group is Iguanodon, one of the first dinosaurs discovered. This dinosaur was named because its teeth were similar in shape to those of an iguana—only much larger. Figure 8.24  This dinosaur trackway has been assigned to a hadrosaurid, because of the rounded toes and corresponding crescent-shaped “handprints”, consistent with biomechanical and skeletal evidence for this group. (Courtesy of L. Bellarosa,

https://commons.wikimedia.org/wiki/ File:Sito​_con_​orme_​di_di​nosau​ri_di​_Alta​ mura_​(Cret​acico​_Supe​riore​,_Bar​i,_Pu​glia)​ _Foto​_Luca​_Bell​arosa​_.jpg​.)

Figure 8.25  (A) Pes (foot) of a hadrosaur. (B) Keratinous hoof of a horse. (C) The ungual of a horse, which bears the hoof in B. The morphology of the unguals on

the hadrosaur foot is broad and flat, superficially similar to the horse ungual. From this, we hypothesize that members of Styracosterna likely had toes protected with a hard keratin covering similar to that seen in some large herbivores today. (Courtesy of K. Tiffany).

170

CHAPTER 8    How Do We Name and Group Dinosaurs?

Styracosterna also has an opposable fifth digit on the hand (Figure 8.26). Humans and other primates have an opposable thumb (first digit) that bends perpendicular to the rest of their fingers, but members of Styracosterna instead had a “pinky” finger that could do the same. This adaptation may have helped them grasp low tree branches and other food items. Conversely, the thumbs of early members of this group bore large spikes (Figure 8.27). In fact, the thumb spike of Iguanodon, when Figure 8.26  Manus (hand) of a Parasaurolophus, with digits II–V labeled. The fifth manual digit (pinky)

of members of Styracosterna could move in a different plane than the other digits. (Photographed by K. Tiffany at the North Carolina State Museum of Natural Sciences.)

Figure 8.27  A reconstruction of the articulated manus (hand) of Iguanodon, showing the prominent spike on its thumb. (Photographed by

C. Tiffany at the Brigham Young University Museum of Paleontology.)

8.3  The Bird Foot Ornithischians: Ornithopoda

171

discovered, was first mistakenly placed upon its nose in early reconstructions (Figure 8.28)! It was only when an articulated specimen was discovered, with the thumb spike attached to the rest of the hand, that this placement was corrected.

8.3.2 Hadrosauridae After the divergence of the iguanodontids, nested within Styracosterna is a more derived group, Hadrosauridae (Figure 8.29). This group includes the familiar, large, herbivorous dinosaurs known for their famous duck-like “bills” (Figure 8.30). The presence of this “duckbill” is a synapomorphy for this group, and is formed by broadening and laterally expanding the toothless premaxilla relative to more basal ornithischians. Hadrosaurids are the largest of the ornithopods in terms of both size and diversity, and are all facultative bipeds, meaning they probably habitually walked on four legs, but could walk on two when they needed to either run faster or reach high plants. That they did both is supported by the presence of hadrosaur trackways that alternatively do or do not include handprints. Additionally, skeletal evidence shows that the forelimbs of members of this group become elongated over time in this lineage, until their arms are almost equal to their leg length. Hadrosaurids also have lost that big thumb spike that was present in their close iguanodontid relatives—in fact, they lost their whole thumb! Hadrosaurs had well developed dental batteries, the morphology of which was unique to this group (Figure 8.31). Hadrosaurid dental batteries are comprised of rows upon rows of interlocking teeth that form one long

Figure 8.28  This is an early reconstruction of Iguanodon made by Gideon Mantell. Among the many

things wrong in this reconstruction is the placement of the thumb spike on the nose. Another is the very mammal-like pose. We know that Iguanodon was at least facultatively bipedal. What ornithischian feature would prevent a tail from being in the position illustrated here? (https​://co​ mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=16​75324​.)

Figure 8.29  Cladogram of Ornithopoda indicating the members of Hadrosauridae (highlighted) within the group.

172

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.30  Skull of a hadrosaurid indicating the expanded premaxilla that forms the duck-like bill for which this group is known. (Photographed by

K. Tiffany at the Field Museum.)

Figure 8.31  (A) Dental battery in the lower jaw (cast) of a hadrosaur. (B) Inset of dental battery showing the interlocking of individual teeth.

(Photographed by K. Tiffany.)

grinding surface for food processing (see Chapter 15). Combined with their pleurokinetic jaws, and the ability to continually replace worn or broken teeth, hadrosaurids were perhaps the best-adapted vertebrates to ever occupy the niche of herbivory. This group also includes Hadrosaurus foulkii (Figure 8.32), the first species of dinosaur ever discovered in North America. We tend to associate North American dinosaur discoveries with Western states like Montana, Wyoming, and South Dakota, because there are large outcrops of Mesozoic rock exposed at the surface. However, H. foulkii was discovered in Haddonfield, New Jersey, in 1838. Although New Jersey does not have exposed terrestrial rock from the Cretaceous, it does have Cretaceous marine sediments exposed at the surface that represent a time when

Figure 8.32  The original bones of Hadrosaurus foulkii, the first dinosaur discovered in America in 1838 (Haddonfield, New Jersey).

(Photographed by A. Carter at the Academy of Natural Sciences of Drexel University.)

8.3  The Bird Foot Ornithischians: Ornithopoda

173

the Atlantic Ocean encroached much farther inland than it does today. It was from a pit within these green, sandy marine deposits that the first Hadrosaurus was recovered, an excellent example of the “bloat and float” taphonomic process (See Chapter 11)!

8.3.3 Saurolophidae After the divergence of Hadrosaurus, we come to the most derived ornithopods, comprising the group, Saurolophidae (Figure 8.33). Saurolophidae can be further divided into two sister groups: Lambeosaurinae and Saurolophinae. These two groups are primarily differentiated by their head ornamentation. Members of the group Lambeosaurinae, or lambeosaurines, have very large crests on their heads (Figure 8.34), and these crests are often hollow. Because these hollow crests are connected to the air passages in the nasal cavity of these animals, it has been proposed that they may have used their crests to vocalize, with each species and their unique crest producing a different sound. In fact, using CT data to scan the internal features of these crests, researchers have built models of lambeosaurine skulls, and found that they make a variety of sounds if you blow into them through the nasal cavity. This may

Figure 8.33  Cladogram of Ornithopoda depicting the placement of Saurolophidae (highlighted) within this group. Note that Saurolophidae

further divides into the groups Lambeosaurinae and Saurolophinae.

Figure 8.34  Skull (cast) of a Parasaurolophus, a lambeosaurine which bears a large, hollow crest.

(Photographed by K. Tiffany at the Field Museum.)

174

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.35  Skull (cast) of Saurolophus, a saurolophine which bears a small, solid crest. (Photographed

by K. Tiffany.)

be as close as we will come to hearing what extinct dinosaurs sounded like! Lambeosaurine species include familiar dinosaurs such as Parasaurolophus and Corythosaurus. Conversely, members of Saurolophinae lack the large, bony crests of the lambeosaurines, and their skulls bear either a small, solid crest (Figure 8.35) or no crest at all. It was once thought that, because there were no elaborate bony structures on saurolophine skulls, they lacked crests altogether—thus they were referred to as “crestless hadrosaurids”. However, recent discoveries have shown that some of these saurolophines, such as Edmontosaurus, may have had soft, comb-like crests, superficially similar to those of chickens! As a result, although saurolophines did not have the large bony headgear of their lambeosaurine relatives, we can no longer infer that they lacked crests. Future work and more well-preserved fossils are needed to re-examine these species and identify bony correlates that could shed new light on their soft-tissue morphology. Saurolophines include Brachylophosaurus canadensis, Maiasaura peeblesorum, and Saurolophus osborni (Figure 8.35). Interestingly, Maiasaura provided the first evidence for nesting and parental care in non-avian dinosaurs outside of the famous examples from Mongolia, and draws its name (Maiasaura  =  good mother lizard) from this behavior (see Chapter 17).

8.4 THE FRILLED ORNITHISCHIANS: MARGINOCEPHALIA After reading this section you should be able to… • Discuss the synapomorphy that makes Marginocephalia unique from other ornithischians. • Describe the characteristics of the four main groups of marginocephalians and name a common species of each group. • Draw a simple cladogram showing the relationship of Marginocephalia clade members.

Within Cerapoda, the sister group to ornithopods is Marginocephalia (margin = border/fringe; cephalia = head) (Figure 8.36A). This name

8.4  The Frilled Ornithischians: Marginocephalia

175

points to the synapomorphy that diagnoses this group: a shelf of bone, or frill, at the posterior (back) of the skull. The dinosaurs within this group vary greatly in terms of size, morphology, posture, and behavior, but all marginocephalians possessed a shelf of bone on the back of the skull. There are two main groups within Marginocephalia: Pachycephalosauria and Ceratopsia (Figure 8.36B).

8.4.1 Pachycephalosauria Pachycephalosaurs (Figure 8.37) are sometimes referred to as the “bowling balls” of the Cretaceous, for reasons that will soon become apparent. Their name means “thick-headed lizards”, and they are quite literally bone heads; this group is characterized by a very thick dome of bone at the top of their heads above the roof of their braincase (Figure 8.38). It has been hypothesized that these bony domes functioned in intraspecific competition (i.e., in-fighting between members of the same species). In particular, it was proposed that pachycephalosaurs used their domed skulls to establish dominance in herds (and therefore access more mates) by head-butting, much like bighorn sheep ram their skulls together in combat. In this hypothesis, the rounded domes would deflect the force of a head-to-head collision, like a football helmet (Figure 8.39). Because

Figure 8.36  (A) Cladogram depicting the placement of the group Marginocephalia (highlighted) within the ornithischian clade. Marginocephalia

is the sister group to Ornithopoda within the clade Cerapoda. (B) Cladogram of Marginocephalia. This group includes Pachycephalosauria as well as Ceratopsia.

Figure 8.37  Cladogram of Marginocephalia depicting the placement of Pachycephalosauria within the group. Pachycephalosauria is

the sister group to Ceratopsia.

176

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.38  Skull (cast) of a Pachycephalosaurus, showing the thick dome of bone on the top, and the shelf of bone on the back of the skull that is a synapomorphy for this group. (Photographed by K. Tiffany.)

Figure 8.39  Artist rendering of how pachycephalosaurs may have used their domed heads in intraspecific combat. All show the head as the contact

point, ramming the head or other body parts of their competitors. However, there is no evidence that pachycephalosaurs had reinforcing ligaments or robust vertebrae in their neck to sustain direct contact, and the vascularity of the dome would probably make this behavior lethal. What other function could these thick domes have served? (Courtesy of J. E. Peterson, C. Dischler, and N. R. Longrich, https​://do​i.org​ /10.1​371/j​ourna​l.pon​e.006​8620.​g011.)

living animals exhibit similar behaviors upon reaching sexual maturity, this idea was broadly accepted for decades after it was first formalized by vertebrate paleontologist Peter Galton in his 1970 publication. When viewed under the microscope, this idea seemed to be supported, because many of the pachycephalosaur domes were found to be very well vascularized, with long bony struts running perpendicular to the surface of the skull (Figure 8.40). It was proposed this was a structural adaptation for head-butting; that the bony struts acted to reinforce the bone and help resist compression, or that the open vascularity provided cushioning for impact. However, subsequent systematic histological analyses of the domes of many different pachycephalosaurs at a standardized location in the skull showed something interesting: the

8.4  The Frilled Ornithischians: Marginocephalia

177

Figure 8.40  Histological section through the dome of a pachycephalosaur. In this section, we

well-vascularized, fast-growing tissue thought to provide a cushion for head-butting was more prevalent in juveniles, who would not be expected to engage in competition for mates. Conversely, in specimens of fully grown adults, this layer of spongy tissue virtually disappears, and the dome becomes much less vascular, and more solid. This suggests that the spongy, fast-growing tissue is associated with age and growth rates rather than behavior. In fact, closer inspection of histological sections through pachycephalosaur domes suggest the domes themselves grow and also change shape with ontogenetic age. Not all known specimens of pachycephalosaurs possessed domes. Some were quite flat-headed, yet still retained the bony shelf and spikes seen in the domed forms—a synapomorphy for Marginocephalia (Figure 8.41). These diverse forms were labeled as different species within Pachycephalosauria, based upon dome shape. However, further examination of the joints in their skull showed the specimens used to diagnose these taxa were at different stages of development—that is, they weren’t all adults that had finished growing. In pachycephalosaurs (as well as humans, birds, and many other vertebrates, though not all) the bones in the skull are not fully fused together when the animal is born (or hatched), which allows growth. As the animal matures, the bones more solidly fuse together. By looking at the degree of fusion in the skulls, researchers determined that flat-headed pachycephalosaurs like Dracorex hogwartsia (Figure 8.41A) were still actively growing animals, and quite young. Conversely, Stygimoloch spinifer (Figure 8.41B) showed greater (but still incompletely fused) connection in the joints of the skull, consistent with an older, but still not fully adult animal, while Pachycephalosaurus wyomingensis (Figure 8.41C) specimens were fully fused, and thus grown adults. These data led researchers to conclude that, rather than being different species, features thought to be consistent with head-butting instead appear to be ontogenetic—growth changes accompanying maturity! Because adult pachycephalosaurs have solid domes, does that rule out head-butting? Let’s look at an animal we know butts heads—Ovis canadensis, the bighorn sheep. You may have assumed that its skull is solid, but when we look inside, we see that the rams have a large, airfilled chamber in their skull above their brain. This chamber protects

observe a layer of well-vascularized bone, with bony struts oriented perpendicular to the surface of the dome (blue arrow). The presence of this tissue was long argued to be structurally advantageous for head-butting. Additionally, in this specimen, we see an open suture, where the skull is not entirely fused (white arrow). Pachycephalosaur domes form from the fusion of three bones in the skull: the paired frontals and the parietal. In this specimen, the line represents an unfused connection between the frontal and the parietal, indicating that the individual is still young—younger than we would expect for an individual engaging in interspecific competition for mates. In older individuals where this suture is fully closed, the vascular tissue also disappears, suggesting it is associated with growth and maturity rather than an adaption for head-butting behaviors. (Courtesy of J. Horner and M. Goodwin, https​://do​i.org​/10.1​371/j​ourna​ l.pon​e.000​7626.​g008.)

178

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.41  (A) Dracorex hogwartsia; (B) Stygimoloch spinifer; and (C) Pachycephalosaurus wyomingensis.

These three specimens were originally designated as three different species within Pachycephalosauria. However, histological studies have shown it to be likely that, rather than being distinct species, these skulls represent different stages of growth in one species. (Photographed by M. Schweitzer at the Museum of the Rockies, with permission from P. Leiggi.)

their brain during head-butting. Adult pachycephalosaurs have no similar features to protect their brain from the force of impact, suggesting that they did not engage in the head-butting behavior (Figure 8.42). So if they did not butt heads, what was the function of the domes? It’s been hypothesized that, like the horns of bighorn sheep, antelope, or bison, their skull domes may have sported a keratinous sheath, a structure which could have provided colorful displays for mating, or species recognition. Thus, it may have been that this unique skull structure was more like a fashionable hat than a helmet! Whatever the color or shape of the external covering over the dome was, it likely functioned in a sociobiological context, helping juveniles recognize other juveniles and adults recognize other adults. The debate regarding the biological significance and uses of pachycephalosaur domes is ongoing, in part because post-cranial skeletal elements are relatively uncommon, and these are needed to help decipher their paleobiology and interpret patterns of behavior from their fossil record. These dinosaurs are known mostly from their skulls. Ongoing research on new skeletons recently found in North America will likely shed some additional light on these questions.

8.4.2 Ceratopsia The ceratopsian (ceratopsia = horned) dinosaurs are much more wellknown and were more broadly distributed and diverse than their sister

8.4  The Frilled Ornithischians: Marginocephalia

179

Figure 8.42  Cross-section through the skull of a bighorn sheep, Ovis canadensis. Arrows indicate an air-filled

(pneumatic) chamber in the skull above the braincase. This chamber is an adaptation that provides a cushion to protect the brain during head-butting. (Courtesy of M. Goodwin.)

group, Pachycephalosauria (Figure 8.43). Like all marginocephalians, ceratopsians have a bony shelf behind their head, expanding outward as it grows back from the skull in a triangular shape. Although the earliest members of this group had very small and relatively simple frills, with no spikes or bony processes, later, more derived ceratopsians had very diverse and elaborate frill morphologies. Ceratopsians are among the last of the dinosaur groups to emerge, and have thus far only been found in Cretaceous rock of Europe, Asia, and North America—although recent finds may indicate the possible presence of this group in Australia as well. Despite this broad distribution, like all the other ornithischian dinosaurs, they vanished without any descendants at the end of the Mesozoic. One synapomorphy that unites all ceratopsians is that they have acquired an additional bone in their skull, the rostral bone (Figure 8.44). The rostral bone is at the very front (anterior) of the upper jaw, in front of the premaxilla. Together with the predentary bone (which all ornithischian dinosaurs share), the rostral bone forms part of the distinctive, parrot-like beak ceratopsians all share. Additionally, the jugals (cheekbones) of ceratopsians flare out sideways into horn-like projections, making their heads look even broader (Figure 8.44).

Figure 8.43  Cladogram of Marginocephalia showing the placement of Ceratopsia within the group. Note that Ceratopsia is the sister

group to Pachycephalosauria.

180

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.44  Skull of the ceratopsian Wendiceratops pinhornensis. The

ceratopsian synapomorphies—a rostral bone and jugals flared out into horn-like projections, are labeled. (Courtesy of the Royal Ontario Museum © ROM.)

Although a relatively late arrival on the Mesozoic scene, ceratopsians were very diverse and successful. The earliest known ceratopsian is Yinlong, discovered in Jurassic deposits of China. The earliest ceratopsian that has been found (so far) in North America is called Aquilops americanus, and it comes from the Lower Cretaceous, making it about 105 million years old! Another early ceratopsian is Psittacosaurus, a small, bipedal genus named after its resemblance to a fat parrot (psittac = parrot; saurus = lizard). There are at least ten different species of psittacosaurs. Numerous specimens of Psittacosaurus have been found that exhibit incredibly detailed preservation, allowing us to infer much about their possible behaviors, lifestyles, and soft tissue anatomy in life. In one case, multiple Psittacosaurus juveniles are preserved in association with each other, with individuals spanning a range of ages, suggesting that young psittacosaurs might have lived together in groups. Another specimen from the Yixian Formation of China includes 34 Psittacosaurus hatchlings, with the full, articulated skeleton of one much larger individual of the same taxon (Figure 8.45). Although there is still discussion of whether the larger individual was preserved in association with the hatchlings, or whether it was added later by humans, the grouping of so many individual hatchlings together suggests that Psittacosaurus babies weren’t extremely precocial (see Chapter 17), but rather may have needed a longer period of parental care. Another specimen of Psittacosaurus shows incredibly detailed preservation of skin, as well as evidence for structures that (superficially) look similar to porcupine quills, arising from the dorsal part of the tail (Figure 8.46). Most of the rest of the body, including the feet, has preserved skin that shows exquisite patterns of big and small scales. The sparsely distributed quill-like structures are only seen on the tail, not covering the whole body as do the feathers of living (and many extinct) birds. Why is this so stunning? Although we have a lot of examples of dinosaur skin, from many different specimens, feather-like or filament structures were predicted to occur only in dinosaurs on the lineage most closely related to birds, the saurischians. This specimen provided the first hard evidence that integumentary structures—structures perhaps related to feathers—occurred in ornithischians. Since this find, many other ornithischians have been found with filamentous covering, in addition

8.4  The Frilled Ornithischians: Marginocephalia

181

Figure 8.45  This spectacular fossil find appears to show over 30 hatchlings of the dinosaur Psittacosaurus, and the skull of one adult. This close

association of adult and hatchling remains potentially indicate intense parental care. At a minimum, the presence of 30 hatchlings together in one nest suggests that they hatched at roughly the same time (based on size) and that they stayed together for a significant amount of time after hatching. (Courtesy of H. Nguyen, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=11​ 63361​8.)

Figure 8.46  An exceptionally wellpreserved specimen of Psittacosaurus shows blackened skin outlining the shape of the body. The skin profile

to skin. These may be an example of convergence, but if further testing supports chemical and/or morphological overlap with true feathers, it may support the idea that some kind of feather-like structures might have been ancestral, and found in the common ancestor for all dinosaurs, pushing back the origin of feathers (in some form) to the Triassic!

8.4.3 Coronosauria After the divergence of basal ceratopsians like Psittacosaurus, we arrive at the group Coronosauria (Figure 8.47). Within members of Coronosauria, the bony shelf on the back of the head expands greatly, forming a true frill, roughly triangular in shape. To see the progression of the neck frill in ceratopsians, compare the small bony protrusion on the skull of Psittacosaurus to the frill on the coronosaurian Protoceratops (Figure 8.48A). Compare them both to the much more derived coronosaurian Anchiceratops, with its enormous frill (Figure 8.48B). Clearly, frills are getting progressively larger, and with the expansion of such a bony structure comes a great increase in the weight of the head—imagine holding a skull half the size of your body off the ground! In conjunction with the increasing frill size, we see another trait in members of Coronosauria; their first several neck vertebrae are fused together, providing added support for their increasingly large skulls. Additionally, in some groups, we see a reversion in the front limbs to a more splayed posture as a way to accommodate the skull mass. Within Coronosauria, there are three major branches (Figure 8.47): Leptoceratopsidae, a basal (and early) group of relatively small-sized species that includes members such as Leptoceratops and Zhuchengceratops;

adds information on the morphology of the animal during life that is not possible to obtain from the skeleton only. Higher magnification images (not shown) reveal scale patterns that differ, depending on where on the body they are found. The most surprising feature of this dinosaur is the presence of long filaments arising from the distal tail, suggesting features similar to feathers on an ornithischian dinosaur. Why do you think scientists have ruled out that these filaments are the result of taphonomy? (Courtesy of J. Vinther et al., https​://dx​.doi.​org/1​0.101​6/j.c​ub.20​16.06​ .065.)

182

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.47  Cladogram of Marginocephalia showing the placement of Coronosauria within the group. Coronosauria includes the groups

Leptoceratopsidae, Protoceratopsidae, and Ceratopsidae.

Figure 8.48  (A) Protoceratops skull (cast), bearing an expanded (but still relatively small) frill. (B) A partial skull of the chasmosaurine Anchiceratops, including the large brow horns and greatly expanded frill characteristics of this group.

(Photographs by K. Tiffany at the Field Museum.)

Protoceratopsidae, which include members like Protoceratops (Figure 8.48A) and Bagaceratops that have expanded, but still relatively small frills; and Ceratopsidae, which include the most derived ceratopsians. It should be noted that, like many phylogenetic placements, the position of Leptoceratopsidae is in flux; some analyses place it outside of Coronosauria, and some place it even closer to Ceratopsidae than Protoceratopsidae. For now, we’ve placed it as a basal branch within Coronosauria, but future fossil discoveries will ultimately determine what relationship is the most likely to be correct.

8.4.4 Ceratopsidae The most derived ceratopsians, including many of the most familiar species within this group, are members of Ceratopsidae (Figure 8.49). Ceratopsids can be divided into two sister groups: Centrosaurinae and Chasmosaurinae. These groups are (relatively) easily distinguished by the proportions of their horns and frills. Centrosaurines generally have relatively small horns above their eyes, and a single and quite large, robust horn above their nose (Figure 8.50). Additionally, their frills are generally smaller than those of their chasmosaur cousins, but can be quite elaborate, including, in some species, bony spikes around the edges. Centrosaurinae includes the dinosaurs Centrosaurus apertus, Styracosaurus albertensis, and Sinoceratops zhuchengensis. Conversely, chasmosaurines typically have a smaller horn over their nose, and relatively longer eye horns. Their frills are also relatively large,

8.4  The Frilled Ornithischians: Marginocephalia

183

Figure 8.49  Cladogram of Marginocephalia showing the placement of Ceratopsidae within the group. Ceratopsidae divides into two

main sister clades: Centrosaurinae and Chasmosaurinae.

Figure 8.50  Skull of Centrosaurus showing the typical centrosaurine features of a large nose horn and small brow horns. (Courtesy of the Royal

Ontario Museum © ROM.)

and some extremely so. To accommodate the weight of these large frills, many are hollowed out or greatly thinned in the middle. Both chasmosaurs and centrosaurs have grooves on the surface of the bone of the frill, indicating that they were covered with a tissue needing a blood supply, possibly keratin. Because keratin in modern animals can be brightly colored, these dinosaurs might be reconstructed with rainbow-colored frills, although there is currently no direct evidence for color in these animals. The most famous chasmosaurine, and indeed one of the most famous dinosaurs of all time, is Triceratops (Figure 8.51). This group also includes Chasmosaurus russelli, Regaliceratops peterhewsi, and Kosmoceratops richardsoni. Although the relative sizes of their eye/nose horns can typically distinguish between chasmosaurines and centrosaurines, it is by no means

184

CHAPTER 8    How Do We Name and Group Dinosaurs?

Figure 8.51  Skeleton of Triceratops.

Triceratops shows the typical chasmosaurine features of large brow horns and a short nose horn. (Courtesy of EvaK at the Senckenberg Museum, https://commons. wikimedia.org/wiki/File:Tric​erato​ps_Sk​eleto​ n_Sen​ckenb​erg_2​a_Whi​te_Ba​ckgro​und.j​ pg.)

an unbreakable rule. Regaliceratops, a chasmosaurine, has the longest nose horn length to skull size of any known ceratopsian and small eye horns, converging upon centrosaurine features. This illustrates the importance of identifying, evaluating, and comparing as many characteristics as possible when building our phylogenetic trees, always keeping the concept of common ancestry foremost (Figure 8.52).

8.5 ORNITHISCHIANS: DEFINITION After reading this section you should be able to… • Define Ornithischia. • Draw a cladogram showing the relationship of all ornithischian groups.

As you will remember from Chapter 4 (Phylogenetics), the definition of a group is not a list of the traits that diagnose it. Rather, it is a concise statement that identifies the branches of a phylogenetic tree that belong within the group, to the exclusion of all others. The definition of Ornithischia is: All dinosaurs more closely related to Triceratops horridus than to Passer domesticus (the sparrow). Although it is a short sentence, this definition encompasses a lot of information. First, “all dinosaurs” indicates right away that all species within this group will have (or will have had in their lineage) all the features that diagnose the clade Dinosauria (e.g., asymmetrical fourth trochanter, perforated acetabulum; see Chapter 7). Second, it orients us in reference to two extremely divergent, terminal branches of the dinosaur phylogenetFigure 8.52  Skull of Regaliceratops.

Although Regaliceratops is a chasmosaurine, its long nose horn and relatively short brown horns converge on centrosaurine morphology. (Courtesy of Eltemenanki3 at the Royal Tyrell Museum, https://commons.wikimedia.org/wiki/ File:Regaliceratops_Royal_Tyrrell_4.jpg.)

8.6  What We Don’t Know

185

ic tree; on one end, the derived ornithischian (Triceratops), on the other, a derived saurischian (a sparrow). By specifying “more closely related to Triceratops”, we know exactly where to divide the tree. As shown in Figure 8.53, everything to the right of the Dinosauria node has an ancestor in common more recently with Triceratops than a sparrow, while on the left, everything has an ancestor in common with a sparrow more recently than Triceratops. It does not matter if the branch bearing Triceratops is furthest left on the page—what matters is the relationship of where the branches meet (see Chapter 4). This cladogram graphically depicts that all ornithischians, from the armored and spikey ankylosaurus to the plant grinding ornithopods and the big-headed ceratopsians, share a common ancestor more recently with each other than any of them do with birds. The relationships of the “other” dinosaur group will be discussed next (Chapter 9) and as we shall see, unlike ornithischians, that dinosaur branch we still have with us today.

8.6 WHAT WE DON’T KNOW Ornithischian dinosaurs had some unique evolutionary features (e.g., tail spikes and clubs, ornate plates, and unique dental batteries) that we don’t see in extant animals today. Unlike their saurischian relatives, they did not survive the end Cretaceous mass extinction to leave living descendants. Because of this, the fossil record is the only source that we have to answer questions related to ornithischian features that we don’t see in modern animals. Questions to consider: • With respect to the elaborate spikes, plates, and horns of many ornithischian dinosaurs, which hypothesis is correct—defense, thermoregulation, display, intraspecific combat, species recognition, a combination of these, or something else entirely? Is the answer the same for pachycephalosaur skulls as it is for elaborate ceratopsian frills? • Why did ossified tendons play such an important role in ornithischians, and why did a convergent structure arise later in some saurischians? Why do no living large herbivores (all of which are

Figure 8.53  Cladogram of Dinosauria.

Blue shading indicates members of Ornithischia. Red arrows indicate the path to the most recent common ancestor that all groups within Ornithischia share with Triceratops.

186

CHAPTER 8    How Do We Name and Group Dinosaurs?

mammals) evolve similar features if they conveyed such a great advantage to dinosaurs? • What drove the evolution of herbivory in this clade? The convergent evolution of herbivory in saurischians (Sauropods and Aves) occurred much later, and under presumably different selective forces. • If the dental batteries of derived ceratopsians and ornithopods were so well adapted to herbivory, why has nothing remotely similar evolved in mammals?

8.6.1 What Was the Earliest Ornithischian, and Why Did This Diverse, Long-Lived Clade Go Extinct? Questions remain pertaining to both the origin and extinction of the ornithischian dinosaurs. This successful and diverse group has fossil representatives on all continents today, but we do not have a record of the earliest ornithischian. Lesothosaurus and Pisanosaurus (the latter is most likely is a silesaurid, an early relative of the dinosaurs) are two possible early ornithischians. We can work backward from the earliest ornithischians to make predictions of traits that the earliest member would have, but we will not be sure unless fossils are found. Questions to consider: • Why did this successful clade become extinct at the end of the Cretaceous, leaving no descendants, while their saurischian cousins continue to thrive? • If ornithischians had survived the Cretaceous extinction, what would their living descendants look like? • Although bone histology strongly supports an elevated metabolic rate in most ornithischians, particularly later, derived ones, we don’t know if they achieved full endothermy, as illustrated by living theropods. Did their physiology contribute to their extinction?

8.6.2 Why Did Ornithischian Dinosaurs Not Have as Wide a Range of Body Sizes as Saurischians? The smallest ornithischian that has been found to date is the early heterodontosaurid, Fruitadens haagarorum, which reached about 65–75 cm (about 30 inches), and less than 1 kg (about 1.5 pounds) but it may have been still growing. The smallest non-avian adult saurischian so far is Anchiornis huxleyi, at just over 100 grams and about 34 cm (~1 ft) in length. And no ornithischian dinosaur got anywhere near as large as the massive saurischian sauropods! Questions to consider: • Did ornithischian dinosaurs go extinct because of their size, by not having smaller members that could eke out a living during the extinction event? • Is the difference in the size range between ornithischians and saurischians due to a fossil record bias? Were there smaller (or larger) ornithischians that we just haven’t uncovered yet?

CHAPTER ACKNOWLEDGMENTS We thank Dr. John Scannella and Dr. Mark Goodwin for their gracious reviews and suggested improvements to this chapter. Dr. Scannella is the

8.6  What We Don’t Know

187

John R. Horner Curator of Paleontology at the Museum of the Rockies. Dr. Goodwin is Assistant Director of Collections and Research, Emeritus, at the University of California Museum of Paleontology.

LITERATURE Abdalla, O. S. M. A. N. (1979). Ossification and mineralization in the tendons of the chicken (Gallus domesticus). Journal of Anatomy, 129(2), 351. Berge, J. C. V., and Storer, R. W. (1995). Intratendinous ossification in birds: A review. Journal of Morphology, 226(1), 47–77. Brown, C. M., and Henderson, D. M. (2015). A new horned dinosaur reveals convergent evolution in cranial ornamentation in Ceratopsidae. Current Biology: CB, 25(12), 1641–1648. Butler, R. J., Galton, P. M., Porro, L. B., Chiappe, L. M., Henderson, D. M., and Erickson, G. M. (2009). Lower limits of ornithischian dinosaur body size inferred from a new Upper Jurassic heterodontosaurid from North America. Proceedings of the Royal Society B: Biological Sciences, 277(1680), 375–381. Farke, A. A. (2014). Evaluating combat in ornithischian dinosaurs. Journal of Zoology, 292(4), 242–249. Farke, A. A., Maxwell, W. D., Cifelli, R. L., and Wedel, M. J. (2014). A ceratopsian dinosaur from the Lower Cretaceous of Western North America, and the biogeography of Neoceratopsia. PLoS One, 9(12), e112055. Godefroit, P., Sinitsa, S. M., Dhouailly, D., Bolotsky, Y. L., Sizov, A. V., McNamara, M. E., Benton, M. J., and Spagna, P. (2014). A Jurassic ornithischian dinosaur from Siberia with both feathers and scales. Science, 345(6195), 451–455. Goodwin, M. B., and Horner, J. R. (2004). Cranial histology of pachycephalosaurs (Ornithischia: Marginocephalia) reveals transitory structures inconsistent with head-butting behavior. Paleobiology, 30(2), 253–267.

Hedrick, B. P., Chunling, G., Omar, G. I., Fengjiao, Z., Caizhi, S., and Dodson, P. (2014). The osteology and taphonomy of a Psittacosaurus bonebed assemblage of the Yixian Formation (Lower Cretaceous), Liaoning, China. Cretaceous Research, 51, 321–340. Horner, J. R., and Goodwin, M. B. (2009). Extreme cranial ontogeny in the Upper Cretaceous dinosaur Pachycephalosaurus. PLoS One, 4(10), e7626. Klein, N., Christian, A., and Sander, P. M. (2012). Histology shows that elongated neck ribs in sauropod dinosaurs are ossified tendons. Biology Letters, 8(6), 1032–1035. Nabavizadeh, A., and Weishampel, D. B. (2016). The predentary bone and its significance in the evolution of feeding mechanisms in ornithischian dinosaurs. The Anatomical Record, 299(10), 1358–1388. Peterson, J. E., Dischler, C., and Longrich, N. R. (2013). Distributions of cranial pathologies provide evidence for head-butting in dome-headed dinosaurs (Pachycephalosauridae). PLoS One, 8(7), e68620. Vinther, J., Nicholls, R., Lautenschlager, S., Pittman, M., Kaye, T. G., Rayfield, E., Mayr, G., and Cuthill, I. C. (2016). 3D camouflage in an ornithischian dinosaur. Current Biology: CB, 26(18), 2456–2462.

9 9

HOW DO WE NAME AND GROUP DINOSAURS? PART II: SAURISCHIAN DINOSAURS

W

e explored ornithischian dinosaurs in the last chapter, so now we turn to the other main branch of dinosaurs: Saurischia. This group contains an enormous diversity of animals, from the immense, longnecked dinosaurs like Diplodocus and Camarasaurus, to carnivorous dinosaurs like Allosaurus and the infamous Tyrannosaurus rex—and birds! The group containing all these familiar species began similarly to that of Ornithischia—with relatively small, bipedal ancestors in the Triassic, like Eoraptor (Figure 9.1) and Herrerasaurus (Figure 9.2). However, unlike Ornithischia, Saurischia is a dinosaur group whose story does not yet have an end; all living birds are descendants of saurischian dinosaurs, and indeed, are saurischian dinosaurs themselves. Here, we take a brief walk through the main dinosaur groups that comprise Saurischia. We will discuss their basic features, and what we know about their phylogenetic relationships to each other, to ornithischians, and to living organisms. Now might be a good time to brush up on phylogenetic (Chapter 4) and anatomical terminology (Chapter 6) as such terms will be used extensively throughout this chapter.

9.1 SAURISCHIANS: DIAGNOSTIC CHARACTERS After reading this section you should be able to… • State characteristics that unite all saurischians. • Describe at least three major differences between saurischian and ornithischian dinosaurs.

“Saurischia” means “lizard-hipped”. As mentioned in Chapter 7 (Defining Dinosauria) the main feature that diagnoses this group is a tripod-shaped pelvis, in which the pubis points forward while the ischium points back (Figure 9.3). However, this diagnostic feature gradually shifts over time in more derived theropods (see Chapter 19, Avian Transition), so it is important to note that not every saurischian has a tripod pelvis. Deinonychus, for example, is definitely a saurischian dinosaur (all

IN THIS CHAPTER . . . 9.1 SAURISCHIANS: DIAGNOSTIC CHARACTERS 9.2 SAUROPODOMORPHA: TERRESTRIAL TITANS 9.3 THEROPODA: THE CARNIVORES 9.4 SAURISCHIANS: DEFINITION 9.5 WHAT WE DON’T KNOW

190

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.1  Eoraptor, an early saurischian dinosaur. Recent

phylogenetic studies suggest that Eoraptor may be a basal sauropodomorph. (Courtesy of the Royal Ontario Museum © ROM.)

Figure 9.2  Herrerasaurus, an early saurischian dinosaur. (Courtesy of the

Royal Ontario Museum © ROM.)

Figure 9.3  Cast of an Apatosaurus pelvis illustrating the typical saurischian morphology where the pubis is oriented cranially and the ischium is oriented caudally, forming a “tripod” shape. (Photographed by K.

Tiffany at the Field Museum.)

known carnivorous dinosaurs are saurischians, and more specifically, theropods), but its pubic bone has rotated so that it is roughly parallel to the ischium, and faces the tail, rather than facing forward (Figure 9.4). This is because, in the dinosaurs most closely related to living and ancient birds, the pelvis converges on the shape seen in ornithischians. Thus, although not all derived saurischians possess a tripod pelvis, all of them are descended from ancestral dinosaurs that did.

9.1  Saurischians: Diagnostic Characters

191

Figure 9.4  Cast of a Deinonychus pelvis. Although Deinonychus is a

saurischian dinosaur, its pelvic morphology is convergent with the ornithischian trait of a retroverted pubis. (Photographed by K. Tiffany at the Field Museum.)

So, if some saurischians have lost the trait of a forward-pointing pubis, how can we tell if our dinosaur is ornithischian or a derived saurischian? To do that requires looking beyond just their pelvic anatomy. Although there are fewer recognized synapomorphies for Saurischia than Ornithischia, other ornithischian traits can be used in addition to pelvic orientation to arrive at the proper diagnosis (Chapter 8, Ornithischians). Does the dinosaur in question have a predentary bone or ossified tendons on their tail vertebrae, like members of Ornithischia? Conversely, are they known to have gastralia, which ornithischians lack? How would you diagnose the dinosaur in Figure 9.5? The saurischian dinosaurs can be divided into two main groups: Sauropodomorpha and Theropoda (Figure 9.6).

Figure 9.5  Knowing what you know about the skeletal differences between saurischians and ornithischians, what type of dinosaur is Nothronychus? How do you know?

(Art by Scott Hartman courtesy of https:// doi.org/10.7717/peerj.36/fig-2.)

192

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.6  Cladogram depicting the major groups within Dinosauria. Here,

the saurischian clade of dinosaurs, which we discuss in this chapter, is highlighted.

9.2 SAUROPODOMORPHA: TERRESTRIAL TITANS After reading this section you should be able to… • Draw a simple cladogram showing the relationship of Sauropodomorpha clade members. • Describe the synapomorphies of the group Sauropoda. • Summarize the unique characteristics of each group within Sauropoda and name a common species from each group.

Figure 9.7  (A) Cladogram depicting the placement of the group Sauropodomorpha (highlighted) within the saurischian clade. (B) Cladogram of Sauropodomorpha. This

group contains basal sauropodomorphs such as Plateosaurus, as well as more derived sauropod groups, including Diplodocoidea and Macronaria.

Among all the unique morphologies expressed by extinct dinosaurs, there is no group of dinosaurs with more amazing and mysterious paleobiology than Sauropodomorpha. This single group encompasses species that are thought to be among the oldest (e.g., Massospondylus and Plateosaurus), the longest (e.g., Supersaurus is hypothesized to have been ~108–112 ft nose to tail), tallest (e.g., the 65 ft Sauroposeidon could look in the window of a seven-story building), and most massive (Argentinosaurus is thought to have tipped the scales at ~90 tons) terrestrial animals to ever walk the planet (Figure 9.7). How can we make such size estimations for animals that we can’t weigh? Studies have shown we can get rather accurate estimates of the mass of living, terrestrial quadrupeds by measuring the circumferences

9.2  Sauropodomorpha: Terrestrial Titans

193

of their humeri and femora. It turns out that there is a very conserved relationship between the girth of the proximal limb bones of an animal and the weight they must support, regardless of whether that animal is a mammal or a reptile, or their posture. Using this relationship, we can take measurements of sauropod limb bones we discover and estimate their mass in life. This allows us to say that for some species, the body of just one individual would be roughly equivalent to the mass of 17 fullgrown elephants! The largest members of Sauropodamorpha were, overall, smaller than a blue whale—but not by much. Further, blue whales are marine animals that benefit from the buoyancy of water to support their massive bodies. As terrestrial animals, sauropods had to resist the full force of gravity to stand and hold up their very long necks, and they had to use muscles to move their enormous frame! We will discuss how they managed the feat of just living, given their size and proportions. But much of how they managed to do this—and on a plant diet no less—is still a mystery (Figure 9.8). All members of Sauropodomorpha—from the largest to the smallest— were herbivorous. Plants today are a notoriously nutrient-poor food source, so how could these long-necked, massive herbivores take in enough plant matter to maintain their body mass? It has been estimated that even small sauropods would have had to eat at least 100,000 calories a day. If the plants they were feasting on had similar nutritional value to today’s plants, that means they would’ve been eating 1,200– 1,500 tons of plant material every single day of their lives. And how did they take in—let alone process—that much plant material daily? Most sauropods lacked the dentition of food-processing machines like hadrosaurs. Diplodocus, for example, possessed a very small head (and small mouth) with simple, peg-like teeth that could grab plants, but probably not chew them (Figure 9.9). Imagine passing more than 1,500 tons of plants through a mouth not very much larger than your own every day! Even without chewing, it would seem that the task of simply meeting their nutritional needs would be constant and endless.

Figure 9.8  Artist’s depiction of the sauropod Europasaurus. The outline of a

sauropod dinosaur is familiar to children the world over, but many of the details of how they lived—such as how they ate enough food to support their massive body size—is still unclear to paleontologists. (Courtesy of Gerhard Boeggemann https​://co​mmons​.wiki​ media​.org/​wiki/​Sauro​poda#​/medi​a/Fil​e:Eur​ opasa​urus_​holge​ri_Sc​ene.j​pg.)

194

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.9  Diplodocus mouth (cast) showing simple, peg-like teeth that were ill-suited for chewing their food.

(Photographed by K. Tiffany, taken at the Field Museum.)

Because there are known growth series for some members of Sauropodomorpha (i.e., specimens of the same species from various points in their ontogenetic development, such as embryo, juvenile, subadult, and adult), by comparing histological sections of the bone microstructure from these series, we can build hypotheses about how fast individuals grew (see Chapter 18). By some estimates, it is thought that some sauropodomorphs could grow from a tiny (about 18 inches) hatchling to an adult weight of 40–60 tons or more in as little as 20–30 years! That’s about the same length of time it takes humans to reach their adult size, and we have a lot less far to go! There is much we still do not understand about this group, it is important to remember that every single member of Sauropodomorpha is more closely related to living birds than any ornithischian dinosaur—even the bipedal ones, like Iguanodon or Pachycephalosaurus, or the small, early ones, like Eoraptor. So what characterizes the group Sauropodomorpha?

Figure 9.10  Skeletal diagram of the sauropod Notocolossus showing a head length to body length ratio typical of sauropods. The blue line

indicates the actual length of the head (HL) in the diagram. The orange line is 19 times longer than the head length (HL × 19) and indicates how long the body of this animal would be if the head represented 5% (or 1/20) of its total body length. Given that Notocolossus has a body longer than the orange line, its head makes up even less than 5% of its body length. (Adapted from artwork by Bernardo J. González Riga, González Riga, B., Lamanna, M., Ortiz David, L. et al. A gigantic new dinosaur from Argentina and the evolution of the sauropod hind foot. Sci Rep 6, 19165 (2016) doi:10.1038/srep19165.)

All members of Sauropodomorpha share two main characteristics. First, they have a very small skull relative to their body—typically the skull is about 5% of their total body length, or less (Figure 9.10). To put that figure in perspective, the head-to-body ratio of a 6 ft adult human is ~12.5%—that’s a head about 9 inches long (a little longer than the short side of a standard sheet of paper). But if a human were proportioned like a sauropod, the same 6 ft person would have to have a head smaller than 3.5 inches—that’s 1.5 inches shorter than a soda can (Figure 9.11)! Second, sauropodomorphs have at least ten cervical (neck) vertebrae (Figure 9.12) and most have a lot more. Each of these vertebrae can be elongated compared with the cervical vertebrae of other dinosaur

9.2  Sauropodomorpha: Terrestrial Titans

195

Figure 9.11  (A) Human skeleton with normal proportions. (B) Human skeleton with a skull that is only 5% of the total body height.

Figure 9.12  Skeleton of the basal sauropodomorph Plateosaurus engelhardti with the cervical vertebrae numbered. All

sauropodomorphs have at least ten cervical vertebrae. In this picture, the first vertebrae after the skull (the atlas), which in this species is much smaller and differently shaped than the rest of the cervical vertebrae, is not shown. (Adapted from an image taken by FunkMonk, https​://up​load.​ wikim​edia.​org/w​ikipe​dia/c​ommon​s/e/e​1/Pla​ teosa​urus_​panor​ama.j​pg.)

groups. This synapomorphy (derived feature) illustrates an important fact about the paleobiology of sauropodomorphs, and dinosaurs in general. The longest neck of any terrestrial vertebrate today is the giraffe (Figure 9.13). Giraffes have seven cervical vertebrae—the same number as there are in your neck, and the necks of nearly all other mammals, even the tiniest mice or shrews (the exceptions being manatees and

196

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.13  Skeleton of a giraffe with the cervical vertebrae numbered.

Although giraffes have the longest neck of any living terrestrial vertebrates, they still only have seven cervical vertebrae, the same as humans and most other mammals. (Courtesy of K. Tiffany, taken at the North Carolina State University College of Veterinary Medicine.)

some sloths). The giraffe’s neck vertebrae are just much, much larger and longer than your own. In sauropods, it’s not just the relative size of the vertebrae that increase to contribute to neck length (even though each one is much bigger than those of a giraffe), but the number of vertebrae as well. This number continues to increase in species with longer and longer necks, but starts in Sauropodomorpha with a baseline of at least ten.

9.2.1 Basal Sauropodomorphs The earliest record we have of sauropodomorphs is from sediments dating to the latest Triassic, as is the case for many other dinosaur groups. These early sauropodomorphs were bipeds; the immense body size that would require a weight-bearing quadrupedal stance would not develop until much later in this group. These early lineages were diverse, widespread, and were either herbivorous, or in some cases, possibly omnivorous. In fact, with their elongated necks, these basal sauropodomorphs were the first large vertebrates to exploit very tall plants, then abundant on the planet, as a food source. Their tails were also generally longer, relative to the rest of their body, than other early dinosaur groups. Probably the best known basal sauropodomorph is Plateosaurus engelhardti (Figure 9.14). Over 100 specimens are known of this dinosaur, and although most are incomplete, what bones we do have document the unique morphology of early sauropodomorphs: the elongated neck and tails that will become more exaggerated (and more familiar) in sauropods. But unlike later species, Plateosaurus was an obligate biped with a long neck. Even more remarkable (and more informative) specimens of basal sauropodomorph fossils were described from South Africa in 2012. They comprised a nesting site of the Early Jurassic sauropodomorph Massospondylus, which had adult members as well as nests containing eggs, and eggs containing embryos (Figure 9.15). Indeed, this nesting ground is the oldest known for dinosaurs, and show that this species, like its later relatives (including titanosaurs and birds) displayed

9.2  Sauropodomorpha: Terrestrial Titans

197

Figure 9.14  Skeleton of Plateosaurus, a basal sauropodomorph. Like other

basal sauropodomorphs, Plateosaurus had an elongated neck and was bipedal. (Adapted from an image taken by FunkMonk, https​://up​load.​wikim​edia.​org/w​ ikipe​dia/c​ommon​s/e/e​1/Pla​teosa​urus_​panor​ ama.j​pg.)

Figure 9.15  Cast of a Massospodylus nest with embryos, discovered in Golden Gate Park, South Africa.

(Courtesy of Daderot, https​://co​mmons​.wiki​ media​.org/​wiki/​Categ​ory:Mass​ospon​dylus​ _foss​ils#/​media​/File​:Mass​ospon​dylus​_egg_​ clutc​h_wit​h_emb​ryos_​(cast​),_Go​lden_​Gate_​ Natio​nal_P​ark,_​South​_Afri​ca,_E​arly_​Juras​ sic_-​_Roya​l_Ont​ario_​Museu​m_-_D​SC001​ 45.JP​G.)

site fidelity (returning to the same region to lay their eggs year after year) and colonial nesting (many individuals laying eggs together in colonies, like modern penguins) (see Chapter 17). Basal sauropodomorphs such as Plateosaurus and Massospondylus disappear in the Early Jurassic, and thus were the first widespread group of dinosaurs to become extinct. Their worldwide loss left only the more derived sauropods to continue through the Jurassic and into the Cretaceous.

9.2.2 Sauropoda Sauropoda (Figure 9.16) is the group that contains all derived, more familiar-looking members of Sauropodomorpha—the immense quadrupeds with extremely long necks and tails. Members of this group are known from the Late Triassic to the Late Cretaceous, making them a very long-lived, diverse, and widely distributed group. Indeed, the remains of these dinosaurs are found on every continent. What contributed to this widespread dispersal? Sauropods are diagnosed by several derived traits not seen in the more basal sauropodomorphs.

198

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.16  Cladogram of Sauropodomorpha indicating the members of Sauropoda (highlighted) within the group.

Figure 9.17  Neck of the sauropod Barosaurus lentus, which has 16 cervical vertebrae. Although not all

sauropods have as many cervical vertebrae as Barosaurus, they all have at least 12. (Courtesy of the Royal Ontario Museum © ROM.)

Sauropod synapomorphies include: • Twelve or more cervical vertebrae: The number of neck vertebrae increases in sauropods, from the ancestral state of ten to 12—or more (Figure 9.17)! Mamenchisaurus constructus possessed 19 cervical vertebrae. • Increased number of caudal vertebrae: Much like the neck length in Sauropoda increases through the addition of more vertebrae in their neck, the tails of sauropods correspondingly lengthen through the addition of caudal vertebrae. Diplodocus possessed as many as 80 caudal vertebrae! • Retracted nares: In most dinosaur groups (and most animals), the nostrils are at the tip of their snout (Figure 9.18A). In sauropods, they are further back in the skull (Figure 9.18B). At one time, it was thought that this feature might indicate that sauropods had trunks like elephants, since elephants also (convergently) have retracted nares (Figure 9.18C)! • Reduced number of carpals: Sauropods have fewer ossified carpals (wrist bones) than more basal groups. In some derived groups, the carpals are completely lost.

9.2  Sauropodomorpha: Terrestrial Titans

199

Figure 9.18  Skulls of (A) a coyote, (B) Diplodocus, and (C) an elephant, with the nares labeled with a red arrow. In

the coyote, the nares are at the tip of the snout. In Diplodocus, the nares are retracted far back in the skull. In elephants, the nares are also retracted back in the skull, convergently with sauropods. (Courtesy of K. Tiffany. A photographed at the lab of A. Hartstone-Rose, B and C photographed at the Field Museum.)

• Highly pneumatic, complex vertebrae: Sauropods have very complex vertebral morphology, externally and internally, compared with other dinosaurs (see below). The last two traits are related to increases in mass—sometimes to enormous proportions—in this lineage. Let’s look at these a little more closely. The loss of bones in the wrist is part of broader posture changes in sauropods, which help them compensate for their great mass. They adopt a graviportal stance. In graviportal (gravi = gravity, port = to carry) posture, the limbs essentially become weight-bearing pillars; the long bones of the limb are arranged vertically underneath each other (to form a column), and the small bones of the wrist and ankle (which would be weak spots, favoring collapse) are reduced (Figure 9.19). Although elephants—the heaviest living terrestrial vertebrates—have also (convergently) adopted a graviportal stance, sauropods take it to the extreme. Not only do their metacarpals (the bones that form the palm of the “hand”) become vertically oriented as part of the “column”, but in derived sauropods, they even become arranged in a tight semicircle (or full circle). In one group (Titanosauria, see below), they lose their wrist bones completely, as well as all the digits on their manus (i.e., their fingers) (Figure 9.20). Titanosaurs are essentially walking around on the fingerless, wrist-less stumps of their hands! The vertebrae in sauropods are extremely complex in overall morphology. They have thin sheets of “sculpted”-looking bone (laminae), bowl-like indentations or depressions ( fossae), and perforating holes ( foraminae) (Figure 9.21). This type of structure is the result of a systemic process called post-cranial skeletal pneumatization, in which extensions from the lungs lay against or pierce the bone and cause the bone they touch to be resorbed. This can happen on the external surfaces of the bone (giving sauropod vertebrae their unique shapes), or on the internal surfaces of the bone, causing all or part of the vertebrae to look like swiss cheese or honeycomb on the inside (Figure 9.22), particularly in species where this process is more extensive. This bizarre biological phenomenon, and its relationship to the respiratory system and dinosaur phylogeny, is discussed in detail in Chapter 19. Here, it is important to know that post-cranial pneumaticity, as it is expressed in Sauropoda, results in bones that maintain their overall size, surface area for muscle and tendon attachments, and structural strength, but at the same time are significantly lighter than they would be if they were a solid mass. This feature probably made it possible for them to attain enormous sizes, because decreasing bone density reduces the weight of the skeleton without decreasing size. Pneumatization is also thought to contribute to their ability to hold their necks and tails above the ground—a 40 ft neck with hollowed bones would be much

Figure 9.19  Forelimb (cast) of a Brachiosaurus showing adaptations for a graviportal posture. The

humerus, radius and ulna, and metacarpals are arranged in one vertical column. Additionally, the carpals (wrist bones) and phalanges (fingers) have been reduced. (Photographed by K. Tiffany at the Field Museum.)

200

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.20  Forelimb of the titanosaur Patagotitan. In titanosaurs, the carpals

(wrist bones) and phalanges (finger bones) are lost, and the manus comprises only metacarpals. (Photographed by K. Tiffany at the Field Museum.)

Figure 9.21  Sauropod dorsal vertebra with lamina and fossa labeled. These

structures are the result of post-cranial pneumatization, a process where extensions of the lungs invade the bone during development. (Photographed by K. Tiffany at the Field Museum.)

9.2  Sauropodomorpha: Terrestrial Titans

201

Figure 9.22  Cross-sections through the caudal (tail) vertebrae of several different sauropods, showing different patterns of internal pneumaticity. In each cross-section,

the black represents bone, and the white internal air spaces. Tornieria, a diplodocid, has large internal chambers, while Malawisaurus, an ancestral titanosaur, has a honeycomb pattern restricted to the neural spine. Conversely, Saltasaurus, a derived titanosaur, shows the honeycomb pattern throughout the whole caudal vertebrae. (Artwork by M.J. Wedel and M.P. Taylor, doi:10.1371/journal.pone.0078213.)

easier to support, lift, and move than a neck of the same size comprised of solid vertebrae. Derived sauropods split into two main groups: Dipoldocoidea and Macronaria (Figure 9.16).

9.2.3 Diplodocoidea Diplodocoidea (Figure 9.23) include the longest dinosaurs, when measured nose to tail. Despite their great length, most diplodocoids were relatively slender and gracile in their proportions compared with other groups within Sauropoda, and had rather weak, pencil-shaped teeth po-

Figure 9.23  Cladogram of Sauropodomorpha depicting the placement of Diplodocoidea within the group. Diplodocoidea is the sister

group to Macronaria within Sauropoda. It splits into two clades: Diplodocidae and Dicreaosauridae.

202

CHAPTER 9    How Do We Name and Group Dinosaurs?

sitioned mostly toward the front of their snout in their small, elongate heads (Figure 9.9, Figure 9.18B). Biomechanical studies of their long necks show that range of motion in their vertebral joints was restricted, and cervical ribs running down the length of their neck contributed to further limitation on movement. These data have led to the hypothesis that most members of Diplodocoidea held their necks horizontally, roughly parallel to the ground. Further evidence for this comes, from all places, from 3-D reconstructions of their inner ear! The semicircular canals serve as balance centers, because these canals are filled with fluid, and when the head moves, the brain senses the response of those fluids. The semicircular canals are oriented in three dimensions (i.e., horizontal, superior, and posterior). How these canals are positioned in the skull of an animal reflects the angle at which it habitually holds its head. For example, the horizontal canal is oriented parallel to the ground (the horizon). Thus, when we find a skull preserved with enough detail to allow us to reconstruct the horizontal canal, we can align it—and the rest of the skull—with the ground to get an idea of the animal’s habitual posture. In some species of diplodocoids, the orientation of the horizontal canal within the skull shows that their heads were generally held with their snouts tilted more downward than forward. This posture might help explain the very long tail, which probably served as a counterbalance to the neck. Some of the longest vertebrates ever to walk the earth are in a derived group within Diplodocoidea, called Diplodocoidae (Figure 9.23). Diplodocidae include species like Supersaurus vivianae (~112 ft) and Diplodocus hallorum (formerly Seismosaurus) as well as Apatosaurus ajax. Diplodocoidea also includes a separate, strange clade that re-evolved a (relatively) short neck. This group, Dicraeosauridae, includes species like Dicraeosaurus hansemanni and Amargasaurus cazaui (Figure 9.24).

9.2.4 Macronaria Macronaria literally means big nose (macro = large, naria = nostrils). This group is the sister group to Diplodocoidea within derived sauropods (Figure 9.25). They are so named because their nares were as big or bigger than their orbits (eye sockets). In species like Camarasaurus lentus, the nasal bones are even arched to create particularly large nares (Figure 9.26). In many ways, macronarians display features that are “opposite” those observed in diplodocoidea. Whereas diplodocoids have small, elongate skulls, macronarians had bulldog-shaped skulls with more robust, spoon-shaped teeth that would have functioned quite differently than the peg-like teeth of diplodocoids. Whereas the overall morphology of diplodocoids is relatively long and gracile, with a horizontal neck and tail posture, macronarians have more robust skeletons, and skeletal

Figure 9.24  Skeletal mount of the dicraeosaurid Amargasaurus.

Amargasaurus has very long neural spines in its cervical vertebrae. (Adapted from an image taken by Jeffery, https​ ://co​mmons​.wiki​media​.org/​wiki/​Categ​ ory:Amargasaurus_skeletal _moun​ts#/m​ edia/​File:​Amarg​asaur​us_sk​eleto​n.jpg​.)

9.2  Sauropodomorpha: Terrestrial Titans

203

Figure 9.25  Cladogram of Sauropodomorpha indicating the placement of Macronaria within this group. Macronaria includes the group

Brachiosauridae as well as the derived group Titanosauria.

reconstructions and biomechanical studies suggest that they could elevate their neck and heads much more vertically than diplodocoids (Figure 9.27). Additionally, although diplodocoids follow the more ancestral state for sauropods of having hindlimbs longer than their forelimbs, macronarians have a derived trait of elongated forelimbs. In species like Brachiosaurus altithorax, the forelimbs are markedly longer than the hindlimbs (Figure 9.28) and lend support to the idea of a more upright stance in this group.

9.2.4.1 Titanosauria A derived clade within macronarians is Titanosauria (Figure 9.29). Titanosaurs exhibit wide-gauge posture. This means that, instead of their legs being pillar-like columns directly under the body, their femora and humeri are angled slightly outward, so that their feet are planted farther away from their midline (Figure 9.30). This is an adaptation that increases stability when supporting increased weight. In addition to skeletal data, this “bow-legged” posture in titanosaurs is supported by comparison of sauropod trackways found in association with titanosaurs versus those found in association with members of Diplodocoidea. The trackways of titanosaurs are wider. Figure 9.26  Skull (cast) of Camarasaurus, a basal macronarian, illustrating two macronarian features: nares larger than the orbits and robust, spoon-shaped teeth. (Courtesy

of K. Tiffany.)

204

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.27  Skeletal mounts of (A) Barosaurus and (B) Brachiosaurus.

The neck of Barosaurus, a diplodocid, is oriented much more horizontally than that of Brachiosaurus, a macronarian. (A courtesy of the Royal Ontario Museum © ROM; B photographed by K. Tiffany at the Field Museum.)

Figure 9.28  Skeleton (cast) of a Brachiosaurus with an adult woman for scale. Brachiosaurus had forelimbs

markedly longer than its hindlimbs, a derived trait within Macronaria. (Photographed by K. Tiffany at the Field Museum.)

9.2  Sauropodomorpha: Terrestrial Titans Figure 9.29  Cladogram of Sauropodomorpha depicting the placement of Titanosauria within the group.

Figure 9.30  Cranial (anterior) view of limb posture of (A) Apatosaurus, a diplodocoid, and (B) Patagotitan, a titanosaur. When compared with

Apatosaurus, the wide-gauge posture that is characteristic of titanosaurs (in which their feet are planted far apart from their midline) is apparent in Patagotitan. (Photographed by K. Tiffany, taken at the Field Museum.)

Some titanosaurs have also been found with preserved osteoderms, a feature not observed (thus far) in any other group of sauropods. Osteoderms are a convergent trait shared with the ornithischian clade Thyreophora. However, unlike the large vertical plates of Stegosauria, or the extensive armor of Ankylosauria, titanosaurs possessed rounded or oval osteoderms (Figure 9.31). These osteoderms often retained small holes on the surface where the blood vessels would have been housed, and this vascularity might point to a potential role in thermoregulation or calcium regulation. In adult specimens of some species, including Rapetosaurus krausei, the osteoderms were found to be hollow. This has led some researchers to hypothesize they were used as reservoirs for minerals the titanosaurs might not always be able to access in appropriate quantities through their diet. Such a mobile calcium reserve would

205

206

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.31  Osteoderm found from an indeterminate titanosaur (possibly Magyarosaurus) in Transylvania, Romania, in (A) dorsal and (B) lateral view. Titanosaur osteoderms are

typically rounded or oval in shape, and sometimes are internally hollow. (Adapted from Z. Csiki-Sava et al., doi: 10.3897/ zookeys.469.8439.)

have been especially helpful when titanosaurs needed to mineralize their eggshells (Chapter 17). Titanosauria includes some of the most massive sauropods that ever lived. Although Argentinosaurus huinculensis is known from only fragmentary remains, a partial femur discovered from this animal was estimated to measure a whopping ~2.5 m in length (or 8.2 ft!), meaning its upper leg alone was the height of the world’s tallest living human (Sultan Kosen). Patagotitan mayorum, a relatively complete titanosaur from Chubut Province, Argentina, is estimated to have been 37 m (121 ft) long! (Figure 9.32). Interestingly, although the group Titanosauria includes some true titans, it also includes some very small species—at least, small by sauropod standards. Magyarosaurus dacus, for example, was estimated to be only about 6 m (~20ft) long, and just a little over a ton. That’s smaller than a school bus! Other members of the very diverse Titanosauria clade include Futalognkosaurus dukei, Dreadnoughtus schrani (Figure 9.33), and Alamosaurus sanjuanensis, one of the few titanosaurs from North America. Interestingly, titanosaurs are the only group of sauropods that survived to the end of the Mesozoic—so all the Figure 9.32  Skeletal reconstruction of Patagotitan mayorum, an immense titanosaur. (Photographed by K. Tiffany at

the Field Museum.)

9.3  Theropoda: The Carnivores

Figure 9.33  Adult woman inside a full-scale outline of the titanosaur Dreadnoughtus in dorsal (aerial) view. (Courtesy of A. Carter.)

sauropods that still roamed the Earth at the same time as Tyrannosaurus rex were titanosaurs!

9.3 THEROPODA: THE CARNIVORES After reading this section you should be able to… • Draw a simple cladogram showing the relationship of Theropoda clade members. • Describe the synapomorphies of the group Theropoda. • Describe the synapomorphies of the group tyrannosauroidea • Summarize the unique characteristics of each group within Theropoda and name a common species from each group.

The final group of dinosaurs to discuss is a favorite among dinosaur lovers everywhere: Theropoda. Theropods (thero = beast, pod = foot) comprise the sister group to Sauropodomorpha (Figure 9.34), and like all other major dinosaur groups, they arose in the Middle to Late Triassic. All theropods are obligate bipeds, and many theropod lineages were carnivorous (although some very derived groups adopted herbivory lat-

Figure 9.34  (A) Cladogram depicting the placement of the group Theropoda (highlighted) within the saurischian clade. (B) Cladogram of Theropoda. This group contains basal

theropods such as Daemonosaurus, as well as more derived theropod groups such as Tetanurae.

207

208

CHAPTER 9    How Do We Name and Group Dinosaurs?

er). In fact, of the five main dinosaur branches we’ve discussed, Theropoda is the only one that includes carnivores (with the possible exception of very early, very basal members of the other groups). These features (bipedality and carnivory) are plesiomorphic traits this group retained from their ancestors; we know because we can observe them in some of the earliest true dinosaurs, such as Eoraptor and Herrerasaurus. Despite retaining these ancestral traits, theropods comprise an extremely complex and diverse clade, and one persisting longer than any other dinosaur group. In fact, they are so long-lived, they are still alive today, in the form of extant birds! As such, Theropoda is the only dinosaur group that has living descendants. They have the largest brain-to-body ratio of any group, and CT studies of their brain and optic nerve cavities, as well as their eye orbits, show that they had very good visual acuity. Theropods are also exceedingly diverse, filling a variety of ecological niches, and are found (both in the fossil record and as living animals) on every continent, from the equator to the poles. They ranged in size from the extant bee hummingbird (Mellisuga helenae; ~2 inches long and weighing 0.07 oz—yes, it’s a theropod!) to predators in the size range of Tyrannosaurus rex (40 ft long and 8 tons). Despite this diversity, like all clades, Theropoda is united by a set of shared characteristics. Theropod synapomorphies include: • Sharp, recurved, serrated teeth: Theropod teeth are pointed, curve backward (toward the throat), and their margins possess serrations, like a steak knife (Figure 9.35). • Tridactyl foot: The feet of theropods consist of three functional toes. Digits 2, 3, and 4 are the only ones that touch the ground while walking, as digit 1 is reduced. • An expanded and prominent ascending process on the astragalus: Like all members of Avemetatarsalia, theropods possess a planar ankle. In some dinosaurs, a thin sheet of bone rises upward from the astragalus (an ankle bone) toward the tibia above it. In theropods, this bony process is expanded and prominent, and fuses to the tibia (Figure 9.36). This both strengthens and stabilizes the ankle, and is hypothesized to be an adaptation for running. • A furcula: A furcula, or as it is more commonly known, a wishbone, has been found within many groups of both early and derived theropods, and the presence of this bone has been hypothesized to be a unique feature (apomorphy) within Theropoda (Figure 9.37). Figure 9.35  The margins of theropod teeth have serrations (labeled) like a steak knife that make them more efficient at cutting meat. (Courtesy of

K. Tiffany.)

9.3  Theropoda: The Carnivores Figure 9.36  Leg of a Tyrannosaurus rex with the ankle shown in inset.

Theropods have an expanded, prominent bony process (labeled in inset) that rises from the astragalus and fuses to the tibia. (Photographed by K. Tiffany at the Field Museum.)

Figure 9.37  The chest of a Tyrannosaurus rex skeleton. Arrow

indicates the furcula, a bone formed from the fusion of the clavicles. It is found widely throughout the group Theropoda. (photographed by K. Tiffany at the Field Museum.)

• Pneumatic skeleton: Like their sauropod cousins, theropod bones were hollow and thin-walled (relative to their overall diameter) and many were filled with air sacs, which served, in part, to lighten the skeleton without diminishing strength. Let’s look at how some of these bony adaptations are related to important aspects of theropod paleobiology and evolution. First, their blade-like teeth show adaptations for carnivory. They were not only sharp, but most were serrated as well, allowing them to more efficiently cut through and shred muscle, the same way it is easier for you to cut steak with a serrated steak knife than a butter knife (Figure 9.35). In addition to serrations, the recurved nature of their teeth acted like a hook, holding prey more firmly in their mouths and forcing meat back into the throat. The furcula and pneumatic bones that characterize Theropoda also point to their evolutionary relationship with birds, which emerge as a

209

210

CHAPTER 9    How Do We Name and Group Dinosaurs?

derived group within Theropoda. Interestingly, both of these features were once thought to be unique to living birds, and along with feathers, were used to define them. The furcula is formed from a fusion of the clavicles at their midline. Virtually all vertebrates have clavicles, and you can certainly feel your own “collarbones”, but only in theropods do they become fused together. In living birds, this fused furcula stabilizes the thoracic (chest) region to better withstand the enormous stresses of flight, as well as provide increased surface area for the attachment of flight muscles (Figure 9.38). We now know that the presence of a furcula is spread widely across Theropoda, and they have been found in species that we are certain did not fly. Tyrannosaurus rex, for example, had a fused furcula. What selective pressures drove the initial development of the furcula in basal theropods remains a topic of investigation. Although no theropod reached the massive size of their sauropod cousins, pneumaticity is even more prevalent and extensive in theropod skeletons. This pneumaticity incorporates not only their vertebrae, but also their limbs and other elements, resulting in hollow long bones with thin walls relative to their overall diameter, distinctive and easy to recognize even in a hand sample. This makes identification of extinct theropods straightforward, even while still in the quarry (Figure 9.39). In modern birds—living theropods—we can observe the process of pneumatization during development. Through these observations, we know that the hollow bones of birds are the result of invasions of air sacs from the respiratory system into bone tissue. This allows the bones to be lighter (while still retaining their strength) and in birds increases the efficiency of their breathing. Lighter, pneumatic bones in sauropods might have allowed those groups to attain their massive proportions, but in theropods, this feature would eventually become crucial for the development of flight. For more on post-cranial pneumaticity, see Chapter 19.

9.3.1 Coelophysoidea The first division of relatively advanced theropods (i.e., Neotheropoda, or neotheropods) is between Coelophysoidea and members of Averostra (Figure 9.40). Coelophysoids are a group of relatively small theropods Figure 9.38  Skeleton of a pied-billed grebe (Podilymbus podiceps) with the furcula labeled. Furculas were once

thought to be unique to living birds until the discovery of furculas in extinct, nonavian dinosaurs. (Photographed by K. Tiffany at the Field Museum.)

9.3  Theropoda: The Carnivores Figure 9.39  A dinosaur long bone sticking out of an outcrop, broken in cross-section. The large, hollow center

of the bone is characteristic of theropods, allowing us to infer this fossil is from a theropod before we even excavate it. (Courtesy of M. Schweitzer.)

characterized by the particular way in which the premaxilla and maxilla meet; the angled joint creates a toothless gap and a “kink” in their snout (Figure 9.41). Some species of these small carnivores have been found in death assemblages representing a large number of individuals (up to a thousand at one site), suggesting that they may have lived together in groups. Coelophysoidea includes Coelophysis bauri, Zupayasaurus rougieri, and Procompsognathus triassicus, and many other Late Triassic-Early Jurassic species including the compsognathids that had a starring role in Jurassic Park III.

9.3.2 Ceratosauria After coelophysoids branch off, we are left with a clade consisting of all groups more closely related to modern birds than to coelophysids. This clade of remaining theropods is called Averostra, literally “bird nose”. (Figure 9.42). All members of Averostra have lost the “kink” in the snout between the maxilla and premaxilla seen in more basal groups and have a reduced number of teeth in their maxilla. Averostra gives rise to the Ceratosauria and Tetanurae. Figure 9.40  Cladogram of Theropoda depicting the placement of Coelophysoidea within the group.

Coelophysoidea represents a basal group within Neothoropoda, and is the sister group to Averostra.

211

212

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.41  Skull (cast) of Coelophysis, a member of Coelophysoidea, with the flexible joint, or “kink” between the maxilla and premaxilla labeled. (Courtesy of A.

Carter, taken at the American Museum of Natural History.)

Figure 9.42  Cladogram of Theropoda depicting the placement of Ceratosauria within the group.

Ceratosauria is the sister group to Tetanurae within Aveostra.

Ceratosaurs are characterized by a robust skull that may or may not be ornamented, but is increased in height over the flattened skulls of more basal groups, and by a reduction in the size of the manual digits (fingers) (Figure 9.43). In derived ceratosaurs such as abelisaurids, the forearms become very shortened (Figure 9.44). Although other, distantly related groups of theropods would convergently evolve short arms—including Tyrannosaurus rex—these derived ceratosaurs had arms that were both short overall and had a proportionately long humerus compared with their reduced radius and ulna. Carnotaurus sastrei, for example, had forearms only a quarter of the length of its upper arm (Figure 9.45)! If you are ever confronted with a picture of a theropod with short arms and cannot tell what group it belongs to, a good “cheat” is to count the fingers—whereas tetanurans like Allosaurus and T. rex have three or fewer fingers, ceratosaurs still have the ancestral number of four. Other ceratosaurs include Abelisaurus comahuensis and Ceratosaurus nasicornis. The phylogenetic relationship between Coelophysoidea, Ceratosauria, and Dilophosaurus (Figure 9.46), the double-crested dinosaur featured

9.3  Theropoda: The Carnivores

213

Figure 9.43  Skeletal mount (cast) of Ceratosaurus nasicornis, showing the ceratosaur feature of shortened fingers. Ceratosaurus also had an

ornamented skull, including bony, hornlike projections on its snout, as well as very small osteoderms along its spine—a trait unique to this dinosaur within Theropoda. (Photographed by D. Czajka at the Natural History Museum of Utah.)

Figure 9.44  Skeletal diagram of Carnotaurus, an abelisaurid (a derived ceratosaur), showing the relatively short forearms that characterizes this group. (Adapted from artwork by J. A.

Headden, https​://co​mmons​.wiki​media​.org/​ wiki/​Categ​ory:Carn​otaur​us_fo​ssils​#/med​ ia/Fi​le:Ca​rnota​urus_​recon​struc​tion_​Headd​ en.jp​g.)

in Jurassic Park (it was portrayed with both a frill and the ability to spit venom, but there is no evidence to support either feature in their fossil remains), has shifted in recent years. For a time, coelophysoids and ceratosaurs were paired as sister groups, and Dilophosaurus was shuffled between the two. Current thinking places ceratosaurs more closely related to other members of Averostra, but it is still unclear if Dilophosaurus is more closely related to coelophysoids or more derived theropods. Like most phylogenetic mysteries, the discovery of additional, more complete skeletons (and therefore more data) are needed to resolve these relationships!

9.3.3 Tetanurae Within Averostra, the sister group to Ceratosauria is Tetanurae (Figure 9.47), a group that includes all living birds—and a few other critters as well. Tetanurans are grouped together by numerous synapomorphies that are not seen in more basal theropods, but here we will limit the discussion to two of the most basic and easily distinguishable traits. First, all members of Tetanurae have lost the fourth digit on their manus (hand), and therefore have only three fingers (or less). Thus, if you see a dinosaur that has four or more fingers, it is not a member of this group—or is a very inaccurate artistic rendering! Second, although in more basal theropods like Coelophysis, the tooth row can extend fairly far back in the jaw, in tetanurans, the tooth row does not extend posterior to their orbits (Figure 9.48). Tetanurae includes some really big (and really odd) groups of theropods. It was within this clade that theropods first evolved large body proportions, eventually becoming the largest terrestrial predators that have ever walked the earth. In fact, large body size evolved numerous times

214

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.45  Forelimb of a Carnotaurus, showing the relative proportions between the upper arm (humerus), forearm (radius and ulna), and hand (metacarpals) of this species. Whereas other short-armed

theropods like Tyrannosaurus had upperand forearms roughly equal in length, Carnotaurus had forearms only a quarter of the size of their humeri. Scale bar = 5 cm. (Adapted from image by R. Delcourt, doi:10.1038/s41598-018-28154-x.)

Figure 9.46  Cast of Dilophosaurus.

It is currently unclear if Dilophosaurus is more closely related to coelophysoids or more derived theropods. What feature do you see that might unite Dilophosaurs with coelophysids? (Courtesy of S. Bergmann, https​://up​load.​wikim​edia.​org/w​ikipe​dia/c​ ommon​s/e/e​9/Dil​ophos​aurus​_skul​l.jpg​.)

9.3  Theropoda: The Carnivores

within the group, independently appearing in three separate branches: Megalosauria, Allosauria, and Coelurosauria.

9.3.4 Megalosauria Megalosaurs comprise the most basal group of tetanurans (Figure 9.49), and include two main sister groups: Megalosauridae, which includes some Jurassic theropods such as Afrovenator abakensis and Megalosaurus bucklandii, and the Spinosauridae, known for their huge neural spines, which give them a humped silhouette (Figure 9.50). These elongated neural spines are hypothesized to have supported either a large sail (superficially similar to the very early synapsid Dimetrodon) or possibly a hump of fatty deposits (superficially similar to a camel). In addition, spinosaurids had elongated, narrow snouts similar to gavials (gharials) (Figure 9.51), which, together with their narrow teeth, has led to hy-

215

Figure 9.47  (A) Cladogram of Theropoda depicting the placement of Tetanurae within the group. Tetanurae is a very derived group within Theropoda. (B) An expanded cladogram of Tetanurae.

Figure 9.48  A comparison of dental morphology in the skull of (A) Dilophosaurus, a non-tetanuran theropod, and (B) Suchomimus, a member of Tetanurae. In each image,

the yellow line indicates the anterior extent of the orbit, and the blue line indicates the furthest extent of the maxillary tooth row. In tetanurans, the toothrow does not extend posterior to the toothrow. (A adapted from an image taken by S. Bergmann, https​://up​ load.​wikim​edia.​org/w​ikipe​dia/c​ommon​s/e/e​ 9/Dil​ophos​aurus​_skul​l.jpg​; B courtesy of the Royal Ontario Museum © ROM.) Figure 9.49  (A) Cladogram of Tetanurae depicting the placement of Megalosauria within the group. (B) Expanded cladogram of Megalosauria, showing the sister groups Megalosauridae and Spinosauridae.

216

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.50  Skeleton (cast) of Suchomimus, a spinosaurid dinosaur.

The elongated neural spines over the back and hips of spinosaurus have been hypothesized to support either a sail or a hump of fatty deposits. (Courtesy of the Royal Ontario Museum © ROM.)

Figure 9.51  Skull (cast) of Suchomimus, a spinosaurid dinosaur.

The long, narrow snouts of members of spinosauridae, convergent with the morphology of gavials, is one piece of evidence that has led researchers to hypothesize that at least part of their diet consisted of fish. (Courtesy of the Royal Ontario Museum © ROM.)

potheses that at least part of their diet comprised fish. This piscivory (fish-eating) behavior is supported, not just by morphological overlap with other fish-eaters, but also by the presence of fish scales in the abdominal area of the spinosaurid Baryonyx, and by chemical data in the form of calcium isotope studies on its teeth. Spinosauridae includes one of the largest predators ever to live, Spinosaurus aegyptiacus, a spinosaur estimated to have grown up to ~50 ft in length. For reference, most Tyrannosaurus rex specimens were significantly smaller, about 40 ft in length! So, in the battle for dominance, it is quite likely that this spinosaurid might have won, had they lived at the same time! This species was first described in 1915 by German paleontologist Ernst Stromer, but the original material (holotype specimen) was obliterated in the destruction of the museum housing them during the bombing of Munich during World War II. However, the drawings, notes, and descriptions made by Stromer were thorough enough to diagnose and assign new fossils found years later to this species. Let that be a lesson in keeping detailed records in science! Other spinosaurids include Baryonyx walkeri, Suchomimus tenerensis, and Irritator ­challengeri.

9.3.5 Allosauria After Meglosauria, the remaining tetanurans are united in a group called Avetheropoda. Among avetheropods, there are two main groups: Allosauria and Coelurosauria (Figure 9.52A). Allosaurs were widespread and successful, with fossil discoveries dating from the Jurassic to the Early Cretaceous, and from North and South America, to Africa, Europe, and Madagascar. Probably the most well-known member of this

9.3  Theropoda: The Carnivores

217

Figure 9.52  (A) Cladogram of Tetanurae showing the placement of Allosauria within the group. Allosauria is the sister group to Coelurosauria within Avetheropoda. (B) Expanded cladogram of Allosauria, including sister groups Allosauridae and Carcharodontosauridae.

group was the Jurassic King, Allosaurus fragilis (Figure 9.53), but it also includes other large predators, including Carcharodontosaurus saharicus and Giganotosaurus carolini. Although casual dinosaur fans may confuse the many large theropods within Allosauria with Tyrannosaurus rex, all allosaurs possess three fingers (Figure 9.54), the ancestral state for Tetanurans.

Figure 9.53  Skull (cast) of Allosaurus, a Jurassic allosaurid. (Courtesy of K.

Tiffany.)

Figure 9.54  Skeletal mount (cast) of Acrocanthosaurus, a carcharodontosaurid. Although

Acrocanthosaurus and other allosaurs are similar to tyrannosaurids in that they are large, predatory theropods with short arms, their hands have three fingers, not two. (Photographed by K. Tiffany at the North Carolina Museum of Natural Sciences.)

218

CHAPTER 9    How Do We Name and Group Dinosaurs?

9.3.6 Coelurosauria Coelurosauria includes the members of Avetheropoda that are more closely related to birds than to allosaurs (Figure 9.55). There are two main groups of interest within this clade: Tyrannosauroidea (the “tyrant lizards”) and Maniraptoriformes (the “hand stealers”). Members of Tyrannosauroidea are less closely related to living birds that the members of Maniraptoriformes. Basal members of Tyrannosauroidea include Dryptosaurus aquilunguis, a tyrannosauroid first discovered in the 1860s in New Jersey (Figure 9.56), and Dilong paradoxus, a species from the Early Cretaceous of China that was found with evidence of a feather-like (perhaps protofeather?) covering in the form of impressions. Derived tyrannosauroids form the subgroup Tyrannosauridae (Figure 9.57), and it is here that we see the onset of the familiar features we associate with the most infamous tyrannosaurid, the iconic Tyrannosaurus rex.

Figure 9.55  Cladogram of Tetanurae depicting the placement of Coelurosauria within the group.

Coelurosauria contains the sister groups Tyrannosauroidea and Maniraptoriformes.

Figure 9.56  Skeletal mounts of two Dryptosaurus, members of Tyrannosauroidea, in the middle of combat. (Courtesy of L. Lazinsky, taken at

the New Jersey State Museum, https​://co​ mmons​.wiki​media​.org/​wiki/​Categ​ory:Dryp​ tosau​rus_f​ossil​s#/me​dia/F​ile:L​eapin​g_Dry​ ptosa​urus.​jpg.)​

9.3  Theropoda: The Carnivores

219

Figure 9.57  Cladogram of Tyrannosauroidea, showing basal members of the group as well as the derived clade Tyrannosauridae. It is

within the Tyrannosauridae that we see the onset of traits that are generally associated with the iconic Tyrannosaurus rex (e.g., a two-fingered hand), which are also present in other members of this group, such as Daspletosaurus and Tarbosaurus.

Tyrannosaurid synapomorphies include: • Shortened forelimbs: Tyrannosaurids have very short arms relative to their body size; although a Tyrannosaurus rex could grow to be upwards of 40 ft long and 7–8 tons, its arms were not much longer than those of an average human (Figure 9.58). • Reduction of digits: Tyrannosaurids lose yet another digit from the ancestral tetanuran condition of three, leaving them with only two grasping fingers (Figure 9.58). • Expanded skull: Tyrannosaurids possess very large, robust skulls that are wider than other groups (i.e., expanded laterally), allowing the eyes to be oriented straight forward (Figure 9.59) relative to the more side-oriented eyes of more narrow-skulled theropods. Figure 9.58  Model of a T. rex arm showing its relative size compared with the arm of an adult woman, as well as the tyrannosaurid condition of only two fingers. (Courtesy of K. Tiffany,

taken at the North Carolina Museum of Natural Sciences.)

220

CHAPTER 9    How Do We Name and Group Dinosaurs?

Figure 9.59  Skull of Tyrannosaurus rex. The skulls of tyrannosaurids are

laterally expanded, allowing the eyes to be oriented forward. It is hypothesized that because of this skull morphology, T. rex might have had binocular vision, like wolves, cats, and humans. (Photographed by K. Tiffany at the Field Museum.)

It is hypothesized that this trait would have allowed tyrannosaurids to have binocular vision and greater depth perception, like humans (and other predators) have. Thus, the idea that Tyrannosaurus rex had weak vision and wouldn’t be able to see you if you were right in front of its nose, as depicted in Jurassic Park, is not supported by evidence. • Robust teeth: Whereas most theropods have narrow, blade-like teeth that are adapted for slicing, tyrannosaurids have thickened teeth that are oval-shaped in cross-section (Figure 9.60). This type of tooth morphology is better for crushing, and is somewhat similar (convergent) to the tooth morphology of crocodilians. Tyrannosauridae is also the third group within Theropoda to independently evolve very large body sizes. In addition to T. rex, Tarbosaurus bataar, Albertosaurus sarcophagus, and Daspletosaurus torosus could all reach 30 ft—or more—in length. Maniraptoriformes is the group within Coelurosauria that includes birds, as well as dinosaur groups that show increasingly bird-like characteristics (e.g., ornithomimosaurs, the “bird-mimics”). We will cover all the dinosaur clades within Maniraptoriformes in much greater detail in Chapter 19, because it is this group of dinosaurs that we still have with us today, and in great abundance. The evolution of birds within Theropoda and the development of flight is significant in today’s world and deserves its own chapter! Figure 9.60  Comparison of teeth (cast) from Tyrannosaurus rex, a tyrannosaurid (right), and Carcharodontosaurus saharicus, an allosaur (left). Although both species

have large teeth, those of T. rex are much thicker, which are better adapted for crushing rather than slicing. (Courtesy of K. Tiffany.)

9.4 SAURISCHIANS: DEFINITION After reading this section you should be able to… • Define Saurischia. • Draw a cladogram showing the relationship of major Saurischian groups.

9.5  What We Don’t Know

221

Figure 9.61  Cladogram of Dinosauria.

Blue shading indicates members of Saurischia. Red arrows indicate the path to the most recent common ancestor that all groups within Saurischia share with extant birds. Note that all members of Saurischia share this ancestor more recently than any of them share an ancestor with Triceratops.

As you will remember from Chapter 4 (Phylogenetics), the definition of a group is not a list of the traits that diagnose it. Rather, it is a concise statement that identifies the branches of a phylogenetic tree that belong within the group, to the exclusion of all others. In Chapter 8, we defined Ornithischia as: “All dinosaurs more closely related to Triceratops horridus than to Passer domesticus (the sparrow)”. It may not surprise you that the definition of Saurischia—essentially the other half of the dinosaur tree—is the exact opposite. Saurischia is defined as “All dinosaurs more closely related to Passer domesticus than Triceratops horridus”. In other words, all animals that have (or had in their lineage) all the features that diagnose the clade Dinosauria (e.g., asymmetrical fourth trochanter, perforated acetabulum; see Chapter 7) are more closely related to birds than they are to the derived ornithischian Triceratops. By specifying “more closely related to Passer domesticus”, we know exactly where to divide the tree (Figure 9.61). As shown in Figure 9.61, everything to the right of the Dinosauria node has an ancestor in common more recently with sparrows than with Triceratops, while on the left, everything has an ancestor in common with Triceratops more recently than with any bird. Note that it does not matter if the branch bearing Triceratops is furthest left on the page—what matters is the relationship of where the branches meet (see Chapter 4).

9.5 WHAT WE DON’T KNOW 9.5.1 How Did Sauropods Get So Very Large, and in Such a Short Time? The rapid growth of sauropods seems to suggest an elevated metabolic rate—indeed, to support that growth hints that these dinosaurs may have been fully endothermic (see Chapter 18). However, when grown, their surface area to volume ratios would have made it particularly difficult to shed metabolic heat, particularly in the warm environments of the Mesozoic. The massive size of sauropods also leads to many unanswered questions related to their diets.

222

CHAPTER 9    How Do We Name and Group Dinosaurs?

Questions to consider: • How did sauropods avoid cooking? Their relatively small surface area compared with huge volumes would make it very difficult to shed heat, and it would accumulate internally. • How could sauropods get enough nutritive value out of plants (a relatively non-nutritive source of food) to support the level of growth and maintenance required for their massive bulk? • How did they manage to take in and process enough plant material to support their enormous size with such small mouths, relatively weak teeth, and small heads?

9.5.2 What Drove Many of the Unique Evolutionary Features We See in Theropods? While nowhere near as the big as the largest sauropods, many theropods also achieved relatively large sizes. If you think about large predators today (and outside the Mesozoic), most are either quadrupeds (e.g., lions, crocodiles, polar bears) or aquatic (e.g., sharks, killer whales). The presence of feathers is a feature that appears unique to dinosaurs but may also have roots deeper in the archosaur lineage. Recent discoveries have shown that some pterosaurs may also have had feather-like integuments, hinting that maybe feathers originated in archosaurs ancestral to dinosaurs. Questions to consider: • What favored bipedality in large theropods? Why don’t we have massive bipedal predators (or other animals) today? (the biggest is the ostrich, at 300–400 pounds vs. a 7-ton T. rex. • How did T. rex (and other tyrannosaurids) use their tiny, but strong arms? Why was this character selected for in this lineage? • Are feathers an ancestral character for all theropods? For all dinosaurs? What data do we need to address the origin of feathers?

CHAPTER ACKNOWLEDGMENTS We thank Dr. Kristi Curry-Rogers and Dr. Nathan Smith for their in-depth and thorough reviews and suggested improvements to this chapter. Dr. Curry-Rogers is a Professor of Biology and Geology at Macalester College. Dr. Smith is the Associate Curator at the Dinosaur Institute of the Natural History Museum of Los Angeles County.

INSTITUTIONAL RESOURCES Hallett, M., and Wedel, M. J. (2016). The Sauropod Dinosaurs: Life in the Age of Giants. JHU Press, Baltimore. Hone, D. (2016). The Tyrannosaur Chronicles: The Biology of the Tyrant Dinosaurs. Bloomsbury Publishing, London. Klein, N., Remes, K., Gee, C. T., and Sander, P. M. (Editors) (2011). Biology of the Sauropod Dinosaurs: Understanding the Life of Giants. Indiana University Press, Bloomington. Kristi Curry-Rogers. How dinosaurs grow. https://vimeo.com/42592504.

9.5  What We Don’t Know

223

LITERATURE Amiot, R., Buffetaut, E., Lécuyer, C., Wang, X., Boudad, L., Ding, Z., Fourel, F., Hutt, S., Martineau, F., Medeiros, M. A., Mo, J., Simon, L., Suteethorn, V., Sweetman, S., Tong, H., Zhang, F., and Mo, J. (2010). Oxygen isotope evidence for semi-aquatic habits among spinosaurid theropods. Geology, 38(2), 139–142. Brink, K. S., Reisz, R. R., LeBlanc, A. R. H., Chang, R. S., Lee, Y. C., Chiang, C. C., Huang, T., and Evans, D. C. (2015). Developmental and evolutionary novelty in the serrated teeth of theropod dinosaurs. Scientific Reports, 5, 12338. Campione, N. E., and Evans, D. C. (2012). A universal scaling relationship between body mass and proximal limb bone dimensions in quadrupedal terrestrial tetrapods. BMC Biology, 10(1), 60.

Carballido, J. L., Pol, D., Otero, A., Cerda, I. A., Salgado, L., Garrido, A. C., Ramezani, J., Cúneo, N. R., and Krause, J. M. (2017). A new giant titanosaur sheds light on body mass evolution among sauropod dinosaurs. Proceedings of the Royal Society Series B: Biological Sciences, 284(1860), 20171219. Niedźwiedzki, G., Brusatte, S. L., Sulej, T., and Butler, R. J. (2014). Basal dinosauriform and theropod dinosaurs from the mid–late Norian (Late Triassic) of Poland: Implications for Triassic dinosaur evolution and distribution. Palaeontology, 57(6), 1121–1142.

10 HOW DO WE NAME AND GROUP MESOZOIC ANIMALS THAT ARE NOT DINOSAURS?

10

PTEROSAURS, MARINE REPTILES, MAMMALS, AND OTHERS

D

inosaurs were not the only vertebrate players on the Mesozoic stage. There were many niches that dinosaurs did not fill, and this left room for the diversification of other groups. For example, although dinosaurs arose in the Triassic (~230 Ma), they did not fly until Archaeopteryx arrived on the scene in the Late Jurassic (~150 Ma). However, pterosaurs, a group of organisms closely related to dinosaurs, were already abundant in the Triassic skies. Additionally, although it has been suggested that some dinosaurs, like Spinosaurus, could swim, no group of dinosaurs adopted a predominantly aquatic lifestyle until the emergence of penguins, long after the extinction of all non-avian dinosaur groups. That left the entire ocean to be filled with marine vertebrates that were not dinosaurs. So, who were these “other players” that filled the remaining ecological niches of the Mesozoic—niches that still exist. Figure 10.1 shows a cladogram depicting some basic relationships of the groups within Tetrapoda (tetrapods), all of which had representatives alive during the Mesozoic.

IN THIS CHAPTER . . . 10.1 ALIVE AND KICKING: EXTANT MESOZOIC LINEAGES 10.2 TAKING TO THE SKIES: THE FLYING REPTILES (PTEROSAURS) 10.3 TAKING TO THE SEAS: THE SWIMMING REPTILES (MOSASAURS, ICHTHYOSAURS, AND PLESIOSAURS) 10.4 WHAT WE DON’T KNOW

226

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

Figure 10.1  Cladogram of Tetrapoda showing the relationship between dinosaurs and many other tetrapod groups that existed during the Mesozoic. Although members of many

of these groups are commonly mistaken as dinosaurs themselves (e.g., mosasaurs, ichthyosaurs, plesiosaurs), this phylogenetic tree shows that they are diapsids rather distantly related from dinosaurs.

10.1 ALIVE AND KICKING: EXTANT MESOZOIC LINEAGES After reading this section you should be able to… • Identify the lineages of extant vertebrates that were present during the Mesozoic.

Although dinosaurs get most of the attention today, the Mesozoic was full of animals that shared the earth with them—vertebrates like snakes, turtles, mammals, fish, and sharks, as well as a host of invertebrates such as insects and spiders—that still have living descendants today. In this section, we review some of the key extant and extinct groups that roamed the Mesozoic alongside dinosaurs.

10.1.1 Mammals Mammals co-existed with the dinosaurs! In fact, the first true mammal puts in an appearance about the same time as the first true dinosaur, in the Triassic (Figure 10.2). All living mammals descend from therapsid cynodonts (Figure 10.3). After giving rise to mammals, almost all cynodonts became extinct in the great End Permian mass extinction 252 million years ago. Some cynodonts survived, however, and competed with their mammalian cousins. In fact, some have proposed that competition Figure 10.2  Flesh reconstructions of an early mammal, Juramaia sinensis, a very early mammal in our own lineage. (Artwork by N. Tamura,

https://commons.wikimedia.org/wiki/ File:Juramaia_NT.jpg.)

10.1  Alive and Kicking: Extant Mesozoic Lineages

227

Figure 10.3  Triassic therapsid, a mammal precursor, that could have interacted with early dinosaurs.

(Courtesy of Ghedoghedo, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=85​ 27157​.)

with their more efficient mammalian descendants may have led to the extinction of the last remnants of this group at some point in the Jurassic. Nevertheless, although it was proposed in the past that mammals drove the dinosaurs to extinction, that idea is hardly correct, given that these two groups lived side-by-side throughout the entire reign of the dinosaurs—and still do today, as both mammals and avian dinosaurs are abundant in the modern world.

10.1.2 Squamates (Snakes and Lizards) Squamata is a group of diapsids that include extant snakes and lizards, as well as extinct mosasaurs (see below). In fact, it is hypothesized that snakes descended from a lineage of either burrowing or aquatic lizards, and the fact that some living snakes still retain pelvic girdles and tiny limbs supports that the ancestor of this group possessed four legs (Figure 10.4). There is no fossil evidence for snakes before the Jurassic, but their closest relatives, the lizards, preceded or co-existed with the earliest dinosaurs. Unlike dinosaurs, snakes survived the End-Cre-

Figure 10.4  Vestigial limbs (circled) can be seen in some living snakes such as this boa constrictor, testifying to its tetrapod ancestry. (Photographed

by K. Tiffany at the Field Museum.)

228

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

Figure 10.5  Flesh reconstruction of Titanoboa swallowing a crocodile.

Titanoboa is estimated to have grown up to 42 ft (~13 m) long and 2,500 lbs. (~1134 kg)! (Courtesy of R. Quick, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=38​ 43705​0.)

taceous extinction event—and managed to become larger and scarier. Titanoboa cerrejonensis (Figure 10.5), which lived during the Paleocene (~10 Ma after the Cretaceous mass extinction), reached a colossal 42 ft (~13 m) in length and an estimated 2,500 lbs. (1,134 kg) in weight. By comparison, the longest living snake, the reticulated python, reaches only ~30 ft (~9 m) and ~350 lbs. (~159 kg), while the most massive living snake, the giant anaconda, reaches only ~550 lbs. (~250 kg). As large as Titanoboa was, however, it wasn’t the largest squamate to ever live. That honor goes to Mosasaurus (see below). The oldest fossil lizard is Triassic in origin; however, molecular data from living squamates suggests that this lineage began even earlier, before the Permian–Triassic extinction. Diversity in this lineage expanded greatly after this massive extinction event, in no small part because the extinction had wiped out competitors, creating vacancies in niches. Squamates took on many odd forms as they radiated and diversified into new Triassic habitats. One of the strangest is Longisquama insignis (Figure 10.6), which possessed long projections from its ribs that have been proposed to be convergent with feathers. Another is Icarosaurus siefkeri (Figure 10.7), an odd little lizard that had greatly elongated ribs. When skin stretched across these ribs, they acted as airfoils, making these lizards excellent gliders. Squamates are true survivors!

10.1.3 Turtles The earliest turtles have been proposed to have originated near the end of the Permian, thus predating the dinosaurs, or possibly in the Mid- to Late Triassic. The reason for this wide variance in attempts to pinpoint their origin is because the earliest turtles did not look much like today’s versions. Eunotosaurus (Figure 10.8), for example, looks more like a lizard than a turtle. Although all living turtles lack teeth, these early

10.1  Alive and Kicking: Extant Mesozoic Lineages

229

Figure 10.6  (A) The holotype fossil of Longisquama insignis, a Triassic squamate. (B) Flesh reconstruction of Longisquama showing its unusual morphology. (A courtesy of

Ghedoghedo, https://commons.wikimedia. org/wiki/File:Longisquama_insignis_ fossil.JPG; B courtesy of N. Tamura, https://commons.wikimedia.org/wiki/ File:Longisquama_BW.jpg.)

Figure 10.7  Reconstruction of Icarosaurus siefkeri, a Late Triassic lizard that used greatly expanded and elongated ribs covered with skin to glide from tree to tree. (Artwork by N.

Tamura, https​://co​mmons​.wiki​media​.org/​w/ ind​ex.ph​p?cur​id=19​45983​4.)

Figure 10.8  Flesh reconstruction of Eunotosaurus. Eunotosaurus has

been identified as the earliest member of the turtle lineage. Its shell is not fully formed, but its ribs are broad and flat and will eventually fuse to form the plastron, or shell, of later turtles. (Courtesy of Smojeybjb, https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=11​16370​0.)

230

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

forms still possessed small teeth. Similarly, the very earliest identifiable members of the turtle lineage did not have the familiar carapace (shell) or plastron (ventral plate), but rather possessed broad and flat ribs. Turtles, based upon living forms, were once considered to be the only living anapsids, because their skulls are solid and do not display the fenestrae seen in synapsids and diapsids. However, new fossil finds and molecular data combine to place these animals well within diapsids, closer to crocodiles and birds than to lizards and other squamates. This placement, however, is still a bit tenuous, and scientists do not yet agree as to where, exactly, they fall in the phylogenetic tree of vertebrates. Regardless of their ancestry, Mesozoic turtles were extremely diverse and successful, and were significantly larger than today’s turtles. Archelon (Figure 10.9), with its 7.5 ft (~2.2 m) carapace, is the largest marine turtle ever described, and lived right before the mass extinction that ended this era. Another very large Early Cretaceous turtle is Desmatochelys padillai. Desmatochelys is in the same lineage as today’s sea turtles and is the oldest representative of that lineage. By this time, it looked much more like living turtles than Eunotosaurus, and already exhibited key turtle features, including a full bony shell. Fossils of Desmatochelys have been found in association with plesiosaur, pliosaur, and ichthyosaur remains (see below). One specimen has even been found with eggs in the body! In contrast to non-avian dinosaurs, some turtles survived the catastrophic extinction that put an end to the Mesozoic, and rapidly occupied the empty ecosystems. One of these early survivors was Carbonemys (Figure 10.10), a large freshwater turtle that lived in Colombia about 60 million years ago.

10.1.4 Crocodiles Crocodiles are archosaurs, a group nested within the broader group Diapsida (Figure 10.1). As archosaurs, this lineage shares a more recent ancestor with all dinosaurs and pterosaurs than they do with snakes and lizards. Further, because there are still crocodiles (including alligators,

Figure 10.9  Shell of Archelon, an early marine turtle from the Late Cretaceous, with an adult human for scale. (Courtesy of E. Cadena, photo by

Mariano Gonzalez.)

10.1  Alive and Kicking: Extant Mesozoic Lineages

231

Figure 10.10  Carbonemys, a large freshwater turtle that was present in the early Cenozoic ecosystems of present-day Colombia. (Courtesy of

AuntSpray, https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=20​20305​6.)

gharials, caimans) alive today, we can apply much of what we know about them to ancient crocodiles as well. Thus, although crocodiles are not dinosaurs, we refer to them often when studying dinosaurs because of the close relationship between these groups, and their usefulness in setting up the extant phylogenetic bracket (EPB) by which we test many of our hypotheses about dinosaurs (Chapter 4). Archosaurs split into two distinct groups, Avemetatarsalia, which includes dinosaurs, and Pseudosuchia, which includes living crocodiles (Crocodylia) as well as several extinct lineages that roamed the Mesozoic. Rather ironically, “pseudosuchia” means “fake crocodiles”, though don’t be fooled—everything we think of as a “real” crocodile is also in this group. The earliest pseudosuchians appear in rocks ~250 million years old, slightly predating the earliest dinosaurs. However, like the earliest dinosaurs, they were small, terrestrial animals that were at least facultatively bipedal. They were also fast runners, and some show evidence of being herbivorous—certainly different from the crocodylians alive today! At their peak, pseudosuchians were very diverse, widespread and successful, and included lineages such as Phytosauria (phytosaurs) (Figure 10.11), Aetosauria (aetosaurs) (Figure 10.12), and Rauisuchidae (rauischids) (Figure 10.13) in addition to Crocodylomorpha, the group including extant crocodylians. In fact, as a group, the pseudosuchians Figure 10.11  Phytosaurs, such as this Machaeroprosopus mccauleyi, lived primarily in the Late Triassic, and had a global distribution. They

vaguely resemble living gavials and later fossil champsosaurs, with their narrow and sometimes hooked snout. (Courtesy of P. Ranger, https​://co​mmons​.wiki​media​.org/​w/ ind​ex.ph​p?cur​id=16​26826​1.)

232

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

Figure 10.12  Skeletal reconstruction of the aetosaur Stagonolepis robertsoni in (A) dorsal and (B) lateral view. Aetosaurs lived in the Triassic and

had several crocodile-like features that show their shared common ancestry. Although aetosaurs are more closely related to crocodiles than dinosaurs, they share a convergent feature with one particular dinosaur group. Can you identify it? (Courtesy of J. Martz, https://commons. wikimedia.org/wiki/File:Stagonolepis_ robertsoni.png.)

Figure 10.13  Prestosuchus chiniquensis, a Triassic rauisuchid.

With its erect gait (legs directly under the body), this predator dominated the Triassic landscape and likely played a role in keeping the dinosaurs as background players. Rauisuchids went extinct in the Triassic/Jurassic extinction event, which paved the way for the dominance of Dinosauria. (Adapted from R. Somma, https​ ://co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=67​38323​.)

dominated the landscape, effectively keeping dinosaurs as bit players in the shadows during the remaining Triassic. However, during the extinction event that separated the Jurassic and Triassic, most lineages of pseudosuchians mysteriously went extinct. Only one lineage survived, the crocodylomorphs, which we still see today in rather marginal habitats (including Florida golf courses). The extinction of most of the pseudosuchians finally opened the door for the dinosaurs to truly dominate the Mesozoic. Today’s remaining pseudosuchians are very large and powerful, but some members of this ancient group were far more massive. Sarcosuchus imperator, a species from the Early Cretaceous, is estimated to have been about 40 ft (~12 m) in length and about 8–10 tons (~7,250–9,000 m) in weight—its skull alone was over 5 ft (~1.5 m) in length (Figure 10.14)! Why do we see the appearance and unprecedented radiation of so many diverse groups of vertebrates in a relatively short time period? Toward the end of the Triassic, a time roughly corresponding to the emergence of the earliest dinosaurs, the geologic record shows worldwide trends that contributed to the evolution of terrestrial vertebrate fauna. First, atmospheric oxygen showed a slow decline from a high of about 30% in the Late Permian to an estimated low of about 12% by the end of the Triassic. However, a brief spike in atmospheric oxygen interrupted this trend about 220 million years ago, roughly corresponding to the origin of pterosaurs. Today’s oxygen levels are about 21%. How might this have affected the distribution of life? These changes in oxygen levels were accompanied by wide fluctuations in atmospheric CO2. Because of the changing position of landmasses and the supercontinent of Pangea, we also see an increase in aridi-

10.2  Taking to the Skies: The Flying Reptiles (Pterosaurs)

233

Figure 10.14  Sarcosuchus, a crocodylomorph from the Early Cretaceous of Africa, is over a third longer and much more massive than any living crocodile. (Adapted from P.

Janicek, https​://co​mmons​.wiki​media​.org/​w/ ind​ex.ph​p?cur​id=18​52282​8.)

ty, particularly in inland regions, throughout the Triassic period when dinosaurs were beginning to emerge and diversify. The Late Triassic continental rifting, resulting in the breaking apart of Pangea, resulted in huge amounts of greenhouse gasses being released into the atmosphere. Together, these global shifts contributed to a sharp rise in global temperatures. As the climate warmed, the weather became increasingly unstable; tempestite (storm) deposits indicate that storms increased in both duration and intensity. These factors combined to change the planet, contributing to a mass extinction at the end of the Triassic and creating new ecological niches, niches that could no longer be filled by the vanishing pseudosuchians. Now that we’ve discussed the Mesozoic players that are still around today, for the rest of this chapter, we will focus on the Mesozoic reptile groups that lived and died with the dinosaurs, but which have no living descendants.

10.2 TAKING TO THE SKIES: THE FLYING REPTILES (PTEROSAURS) After reading this section you should be able to… • Explain why pterosaurs are not dinosaurs. • List traits that link pterosaurs and dinosaurs more closely to each other than to any other group. • Describe convergent evolutionary traits found in Pterosaurs and other flying vertebrates.

Pterosaurs (pteron = wing; sauros = lizard) were the first vertebrates to take advantage of the many benefits of life in the air, not the least of which is a general lack of competitors. As a group, pterosaurs were extremely diverse and long-lived, emerging about the same time as the dinosaurs, and lasting until the last non-avian dinosaur went extinct at the end of the Cretaceous. As you can see from Figure 10.15, they are archosaurs more closely related to dinosaurs than they are to pseudosuchians, but they were not dinosaurs themselves. This is because although they share with dinosaurs the two pairs of temporal fenestrae that classify them as diapsids, the antorbital fenestrae (at least in basal members) and the fourth trochanter that classify them as archosaurs, and the

234

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

Figure 10.15  Cladogram of Tetrapoda, with the position of pterosaurs highlighted within the group.

Although pterosaurs are archosaurs very closely related to dinosaurs, they are not themselves dinosaurs.

planar ankle that classify them as avemetatarsalians, they do not have the perforated acetabulum that unites all dinosaurs. Thus, although they are closely related to dinosaurs, they don’t share the synapomorphies to justify their common inclusion in the dinosaur group. Pterosaurs were the first vertebrates to attain powered flight, and as a result, some pterosaur traits are convergent with the two other groups of vertebrate fliers, birds and bats, although these groups are only very distantly related. Most obviously, all three groups have wings, and they used them to increase the surface area of their forelimbs, a necessity for gaining lift. However, the bones that make up the wing of each group have been modified in very different ways, and these modifications arise from unrelated evolutionary events. The wings of these groups are thus analogous traits (Figure 10.16), not related through common ancestry. In a pterosaur, the wing membrane is supported by the greatly elongated little finger alone (Figure 10.16A), and in some species, that little finger could be several feet long! For example, the giant pterosaur Quetzalcoatlus (Figure 10.17) had wings that were each 16 ft (~4.9 m). However, its humerus was only 21.5 in (~54 cm), which is about twice the length of an adult human humerus. The remaining 14–15 ft of its functional wing was mostly just its pinky finger! Conversely, the main body of a bird’s wing (Figure 10.16B) is made up of multiple bones, though some have fused together, including those of the wrist and hand, and other bones have been lost. The hand itself is reduced in complexity to only two bones. Using this reduced limb, birds attain lift through their feathers, each of which has a tiny attached muscle that moves the feather to displace air. Pterosaurs and bats, on the other hand, have membranous wings, and achieve lift through the action of these membranes. But even so, bird and bat wing membranes are not evolutionarily similar. In a bat’s wing (Figure 10.16C), the membrane is supported by elongated fingers of the hand. Although the wings of birds and pterosaurs are convergent, these vertebrate fliers also share a different feature that may be homologous—post-cranial skeletal pneumaticity. In post-cranial skeletal pneumaticity (PSP), the bones of the skeleton caudal to the skull are partially hollowed out by extensions of the respiratory system during development (see Chapter 19). As mentioned in Chapter 9, this trait arose at the

10.2  Taking to the Skies: The Flying Reptiles (Pterosaurs)

235

Figure 10.16  Comparison of the wings of (A) a pterosaur, (B) a bat, and (C) a bird. All three of these vertebrates have

a humerus that articulates with the bones of the shoulder. Although the bones in the wings of these animals (e.g., radius, ulna, metacarpals, carpals, and phalanges) are all derived from a common ancestor (and are therefore homologous), the evolutionary modifications these bones underwent to form wings are very different in each of these animals. In the pterosaur, the body of the wing is a membrane that arises from the bones of the fifth digit (little finger). The body of the bat wing is formed by a membrane that arises from and attaches to four fingers of the hand. In the bird, the feathers of the wing form the body, and they insert on the ulna. The bones of the wrist and hand are fused for stability. Each wing is structurally very different, even though they appear superficially similar because the physics of flight highly constrains what morphologies are possible. Thus, although the bones in the wing are homologous between these groups, the wings themselves are analogous traits (homoplasies) that have arisen from convergence. (Adapted from J. Romanes, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=13​24636​.)

base of Saurischian dinosaurs, because we see pneumatized bones in sauropods and theropods as well. This process reduces the mass of the bone, while still keeping it structurally strong. This is advantageous for flying because lighter skeletons (and therefore, lighter bodies) require less energy to move, which is particularly important with the high energy cost of flight. PSP is observed in pterosaurs and saurischian dinosaurs (sauropods and theropods, including birds). In both birds and pterosaurs, the bones are extremely hollow and are often reinforced by bony struts that extend from one internal surface to the other (Figure 10.18). There are more than 200 different species of pterosaurs, which exhibit enormous diversity in size—from the robin-sized Nemicolopterus (~10 in/25 cm, but may not be fully grown), to Pteranodon, which was the size of a hang glider and had a head that measured over 6 ft (1.8 m) alone, to the enormous Quetzalcoatlus (Figure 10.17), which had a wingspan of up to 33 ft (~10 m), more than that of many small personal aircraft! Although these flying giants get most of the attention, the earliest pterosaurs looked quite different. Early pterosaurs were quite small relative to later species, with very long bony tails, and skulls that consisted of thin lacey bones with huge open spaces that were probably filled with air. Their snouts were relatively short, especially with respect to some of the later and more derived pterosaurs, but their mouthful of teeth made them appear much less friendly than the birds that occupy the skies today. Some early pterosaurs, like Eudimorphodon (Figure 10.19)

236

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

Figure 10.17  Fleshed in reconstruction of Quetzalcoatlus, the largest vertebrate to ever attain powered flight, with an adult human for scale.

The wings are proportionate overall to the wrist, but the very long little finger must be folded when not in flight. This animal walked on its wrist! (Courtesy of K. Tiffany.)

Figure 10.18  Post-cranial skeletal pneumaticity in a pterosaur (A, B) and a bird (C). (A) Longitudinal section through

a bone from the wing of a pterosaur shows a honeycomb-like texture of air pockets inter-webbed by thin bony struts. (B) Cross-section through a wing bone of a pterosaur shows an extremely thin cortex wall reinforced by bony struts. (C) Cross-section through the femur of a bird shows a thin cortex and bony struts, very similar to what is observed in pterosaurs. (A and B courtesy of Fastnacht, M. [2005]. The first dsungaripterid pterosaur from the Kimmeridgian of Germany and the biomechanics of pterosaur long bones. Acta Palaeontologica Polonica, 50(2); C courtesy of E. Schroeter.)

10.2  Taking to the Skies: The Flying Reptiles (Pterosaurs)

237

Figure 10.19  Eudimorphodon, a small basal pterosaur from the Late Triassic of Italy. This fossil specimen

preserves sharp pointed teeth in the jaws, and the fingers of the hand can be clearly seen in relation to the very long fifth digit. (Courtesy of Tommy from Arad, https​://co​ mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=28​41394​6.)

show very unusual adaptations, including a mouthful (about 120) of multi-cusped teeth in a small, 3-inch (7.5 cm) jaw. These features have been used to support the hypothesis that these pterosaurs were divers, and perhaps had a diet of fish and invertebrates. However, whether pterosaurs could dive in water is still debated, and it may be that insects formed much of their diet instead. As pterosaurs diversified, they began to increase in size, reduce their tails, and develop extensive head ornamentation. Some had long, spiky teeth that extended from their upper and lower jaws, like a vampire badly in need of braces! Others show even stranger, and enigmatic adaptations, such as tightly packed, hair-like teeth that extended from the lower jaw (Figure 10.20). What they did with these teeth is anyone’s guess, but because they bear a superficial resemblance to baleen whales, it has been proposed that they were filter feeders.

Figure 10.20  Cast of Pterodaustro, an enigmatic pterosaur from Argentina.

Because of the array of long, narrow, and closely packed teeth, superficially similar to the keratinous baleen in whales, it has been proposed that this pterosaur skimmed insects and/or small fish for the majority of its diet. (Adapted from Gadfium at the Museo Argentino de Ciencias Naturales in Caballito, Buenos Aires, Argentina, https​:// co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=17​05717​8.)

238

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

Figure 10.21  Skeleton of Tupuxuara, at pterosaur in which the nares and the antorbital fenestrae merge to form one very large opening in the skull. (Courtesy of https​://co​mmons​.wiki​

media​.org/​w/ind​ex.ph​p?cur​id=10​90952​.)

At the opposite extreme, many derived pterosaurs were toothless—another trait convergent with modern birds. Later pterosaurs seemed to grow their heads and wings at the expense of their bodies, which were very thin, delicate, and fragile-looking, giving them an almost emaciated look. Their heads grew longer, but the overall head mass probably stayed about the same, as they expanded the fenestrae in their skulls. In most of these large and very derived forms (i.e., monofenestratans), the antorbital fenestrae merged with the nares (nostrils) to form one giant opening (Figure 10.21). The huge heads, tiny, slender bodies, and extremely elongated little fingers raises the question—how did these animals move on the ground? After all, they couldn’t fly all the time. What do you do with a 9-ft long pinky finger when it’s not stretched out in the air? Biomechanical studies of the wing elements suggest that they could rotate their wing finger almost 180 degrees, allowing them to fold their wings very tightly to their body. This trait would reduce resistance and drag, making them aerodynamically fit for plunging into the water from great heights. Some could, perhaps, have crawled on all fours, with their body low to the ground (Figure 10.22A) in a splayed posture. Or, they may have had a posture similar to some dinosaurs, as obligate bipeds that walked with their head held horizontal and their tail counterbalancing the weight (Figure 10.22B). Perhaps they walked upright and erect, like humans, with their wings tucked in close to their sides, or they could have walked on all four feet, arms splayed slightly with that elongate pinky tucked into the body, somewhat like the erect stance of quadrupedal dinosaurs. However they moved on the ground, their gait had to accommodate a pinky finger that extended far past the length of their hind legs. This question of posture was hotly debated among pterosaur workers for many years, as each posture had its pros and cons. They all look, from our perspective, very awkward. A series of models were proposed, and from these, footprint patterns were generated to match each model. Despite these efforts, it was once thought that this aspect of their biomechanics would remain forever unknown, because it seemed highly unlikely that we would recover footprints from animals that spent much of their time in the air. But in 1995, trackways were reported that were suggested to be made by pterosaurs, because they retained features consistent with the bony anatomy of pterosaur feet. This interpretation was supported by the finding in 1998 of an articulated pterosaur foot, showing that indeed, it walked plantigrade (i.e., flat-footed, with the heel on the ground). In addition to showing a plantigrade foot posture, the trackways also showed a four-toed, clawed hindfoot, and an odd, tri-

10.2  Taking to the Skies: The Flying Reptiles (Pterosaurs)

239

Figure 10.22  Skeletal mounts of the pterosaur Dimorphodon posed in (A) quadrupedal and (B) bipedal posture.

(A courtesy of F. Kovalchek, https​://co​ mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=33​49594​9; B courtesy of D. Peters, https​ ://co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=49​81474​.)

Figure 10.23  Depiction of quadrupedal walking in pterosaurs as indicated by trackways, showing plantigrade foot posture. (A) Depiction

of a pterodactyloid pterosaur walking, showing their wrists turned so that their fingers point outward to tuck their pinky finger supported wing in close to their body. (B) Depiction of a rhamphorhynchid pterosaur, with their manus turned fully forward. (Courtesy of M. Witton.)

point handprint in front, just as was predicted if pterosaurs walked on all fours, resting their weight on their wrists and extending the little finger behind them (Figure 10.23). Now, most agree that pterosaurs, even the earliest ones, were probably quadrupedal, very different from the obligate bipedal stance of the earliest dinosaurs. However, that does not mean we aren’t still discovering and learning new things about the posture and locomotion of this group. For the last few decades, all the pterosaur trackways that were known had been made by pterosaurs within the derived group Pterodactyloidea. The handprints of this group showed that, in addition to being quadrupedal, pterodactyloids rotated their wrists when walking, with their fingers pointed sideways and their pinky tucked in toward their body (Figure 10.23A). Without trackways of pterosaurs outside of Pterodactyloidea, it was uncertain if other, more basal pterosaur groups walked the same way—or if they even walked at all. However, a new trackway from a rhamphorhynchid pterosaur discovered in 2019 showed that these basal pterosaurs

240

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

certainly did walk, and they too were quadrupedal. However, unlike the pterodactyloids that rotated their wrist to tuck their wing, digits of the manus in rhamphorhynchids pointed fully forward, while their pinky was tucked backward at a perpendicular angle (Figure 10.23B). Although we can place pterosaurs as close relatives to dinosaurs, there is nothing alive today that resembles many aspects of these weird organisms, so understanding their evolutionary history and the origin and distribution of some of these characters is difficult. We do, however, have some specimens of pterosaurs that are preserved almost perfectly, allowing us to see not only all the bony parts, but also to get a close look at their wings. This is how we know that they flew with a wing membrane that was anchored to one, elongate finger, which would have had to support their weight during flight as well as for take-off and landing. How could a thin and apparently poorly anchored membrane support such weight, even with their lightened skeleton? Fossil finds have long suggested that pterosaurs employed an intricate system of stiffening rods within their wing tissues, sandwiched between the layers of skin (Figure 10.24). There is nothing quite like this in living creatures today, so it is hard to say for certain what they were comprised of, but some have proposed that these rod-like reinforcements were thin bands of interwoven elastic and collagen fibers, partially mineralized for stiffness. In addition to these stiffening, strut-like features, pterosaurs showed another surprising trait; some have been found with a fuzzy, fur-like covering. Although hair is restricted to mammals, filamentous, thin, downlike structures are present in some of these first fliers. The only animals that have coverings like this in living organisms are birds and mammals, both of which are endothermic. Because of the extreme energetic costs of flight, it has been proposed that pterosaurs had higher metabolic rates than today’s cold-blooded lizards and snakes. If pterosaurs and dinosaurs both show features we can consistently link to higher metabolic rates, it supports the idea that an elevated metabolism was ancestral for at least the avemetarsalians, and perhaps all archosaurs. Knowing that pterosaurs had a wing membrane that extended from an elongated wing digit is only half an answer to the question of wing structure in these animals. Where and how did this membrane attach to the rest of their body? There are numerous ways the wing membranes could be attached to the body for flight, and Figure 10.25 shows what the wings would look like in each case; membranes could attach to various locations on the hip, ankle, or thigh. How these long and fragile wings attached to the body, as they must have done for flight, is yet another pterosaur mystery. Figure 10.24  Stiffening rods (arrow) can be seen in the wing membrane of this small Rhamphorhynchus muensteri specimen (cast). (Courtesy of

R. Somma, https://commons.wikimedia.org/ wiki/File:Rhamphorhynchus_muensteri_cast. jpg.)

10.2  Taking to the Skies: The Flying Reptiles (Pterosaurs)

241

Figure 10.25  Possible sites of attachment for pterosaur wing membranes. (A) A very bat-like

In addition to possible variation in the attachment of wing membranes, different groups of pterosaurs may have used different attachments for membranes between their hindlimbs (uropatagia). These membranes shed light on the biomechanics of flight, which differed in different pterosaur groups. A primitive, small pterosaur with a long tail, called Sordes pilosus, was exceptionally well preserved in very fine-grained lacustrine (i.e., lake) sediments. These sediments preserved the specimen in fine detail, enough to reveal an extra membrane between its hindlimbs and pelvis, a little like penguin legs (Figure 10.26). These have been used to suggest that when they walked, they probably looked a little like they had their shoelaces tied together! However, later and larger pterosaurs, equally well preserved, show this membrane is reduced or missing altogether, allowing the freedom of movement and independent motion of each leg.

configuration, with the wing attached to the pterosaur ankle. (B) Possible attachment of the membrane that doesn’t involve the legs or tail. (C) The membrane is attached to the knee; a compromise from the two previous versions with more freedom of movement for the feet, but more stability than B. (D) A more recent interpretation of a bat-like model. The exact nature of the wing attachment to the body is still a matter of debate because few fossils show the attachment points, even though many have wing membranes preserved. (Courtesy of Elgin, R. A., Hone, D. W., & Frey, E. (2011). The extent of the pterosaur flight membrane. Acta Palaeontologica Polonica, 56(1), 99–111.)

In addition to shedding light on the physiology of pterosaurs, the fossil record has also produced information on their reproduction (Figure 10.27). In 2004, eggs containing pterosaur embryos were found in China and Argentina. The preservation of these eggs was exquisite, and allowed researchers to propose that pterosaur eggs were not well-mineralized like bird eggs, but more leathery with a thin shell, like crocodile eggs. Furthermore, some hypothesized that the eggs were buried—again,

Figure 10.26  Flesh reconstruction of Sordes, showing the membrane connecting its hindlimbs (arrow).

(Courtesy of D. Bogandov, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=28​ 64318​.)

242

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

Figure 10.27  Depiction of a Pterodaustro embryo folded up in its shell. (Courtesy of Mark Witton.)

more typical of crocodiles and turtles than birds. Burial would restrict the amount of oxygen that could diffuse to the embryo. While most birds sit on their eggs to keep their unhatched young warm, maleos bury their large eggs in underground nests, letting heat from geothermal sources, the sun, or decaying vegetation do their work for them. Burial of eggs also indicates that pterosaurs did not brood their eggs, a behavior that, when observed, implies that the mother has body heat to contribute to the nest (see Chapter 17). If buried, these fossil eggs would suggest that pterosaurs were perhaps more like crocodiles in their metabolism. This, however, seems to directly contradict both evidence from the bones that they grew faster than today’s ectotherms, and the fact that metabolic demands required for sustained, powered flight are greater than what ectothermic animals can sustain. Pterosaurs had to have used more metabolic energy than is available to living lizards and snakes to attain loft for flight. Clearly, we have much yet to learn about the pterosaurs! This is not the only case of exceptional preservation of non-dinosaurian remains. In southern Germany, there is a region known in the 1800s for its production of lithographic limestone—very fine-grained deposits used in the printing industry. The region is named for a small village called Solnhofen, and around this little town are many small quarries where these fine-grained sediments have been quarried for centuries to use for high-quality printing. When choosing rocks for these early

10.3  Taking to the Seas: The Swimming Reptiles (Mosasaurs, Ichthyosaurs, and Plesiosaurs)

243

Figure 10.28  A specimen of a tiny Rhamphorhynchus that has been snatched out of the sky by a large fish, called Aspidorhynchus. Close

inspection shows a small fish, trapped in the throat of a pterosaur. When visualized with ultraviolet light, exceptional detail of soft tissues is seen in panel C. (Courtesy of Frey, E., & Tischlinger, H. (2012). The Late Jurassic pterosaur Rhamphorhynchus, a frequent victim of the ganoid fish Aspidorhynchus? PLoS One, 7(3).)

printing presses, some individuals noticed that the rocks also contained exquisitely preserved remains of creatures never seen before. Not long after Darwin first proposed his theory of evolution by natural selection, a specimen came to light that gave great credence to Darwin’s new theory; the first specimens of Archaeopteryx, identified as the earliest true bird. At first, the skeletal remains had been confused with small dinosaurs that were also observed in the same sediments. Only with the discovery of exceptionally preserved feathers, identical in morphology to feathers of modern birds, was Archaeopteryx accurately identified. Many other lifeforms are preserved in similar detail, in some cases preserving examples of behavior caught in an instant and frozen in time. In these fine-grained rocks, we see what happened when little pterosaurs got too close to the water, where the hungry marine reptiles and large fish could snatch them out of the air. Figure 10.28 captures the death of such a little pterosaur—and, of course, the fish that caught it, which seems to have bit off more than it could chew! When illuminated using UV light, the detail is astonishing.

10.3 TAKING TO THE SEAS: THE SWIMMING REPTILES (MOSASAURS, ICHTHYOSAURS, AND PLESIOSAURS) After reading this section you should be able to… • Explain why the marine reptiles were not dinosaurs. • List and describe features that marine reptiles evolved for a life in water, features that are convergent with other aquatic organisms.

244

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

• Compare and contrast the morphology of mosasaurs, plesiosaurs, and ichthyosaurs. • Summarize the features that separate ichthyosaurs and plesiosaurs from mosasaurs.

As seen in Figure 10.1, dinosaurs and their pterosaur cousins were not alone in the Mesozoic world. These aerial and terrestrial vertebrates crossed paths often with other vertebrates when their niches overlapped, just as various species interact today. If pterosaurs were the first terrestrial vertebrates to master the skies with powered flight, what about the oceans? Who occupied the deep marine waters before whales and dolphins? Based upon fossil evidence, life in Mesozoic oceans was exceedingly diverse, and we estimate that, just as on land, only a small percentage of the creatures that actually lived in these waters were preserved as fossils. In addition to a wide range of invertebrates (clams, oysters, and squid-like creatures), the seas were filled with a wide variety of fish, as well as other, massive vertebrate life that arose from terrestrial ancestors. Unlike today’s oceans, vertebrate life in the Mesozoic seas, besides fish and sharks, consisted mainly of marine reptiles, which can generally be classified into three main groups: ichthyosaurs, plesiosaurs, and mosasaurs. Just like bats, birds, and pterosaurs show convergent features because of the constraints of flight, these marine-adapted vertebrates expressed convergent traits required to exploit a watery niche. Terrestrial animals have, at some point in their history, left the land and returned to the sea many times in many lineages. Mammals that have secondarily adapted to life in the ocean include dolphins, whales, sea lions, walruses, and seals. Within Aves, penguins “fly” underwater. Similarly, several groups of terrestrial reptiles also returned to the seas to fill various aquatic niches. Thus, mammals, birds, and reptiles exhibit traits that adapt them for swimming, and these traits converge on each other despite the evolutionary distance between them. That is the importance of phylogenetic analyses: using similar appearances to group organisms, rather than grouping them by shared derived traits, results in trees that do not necessarily reflect evolutionary lineages and/or processes (Chapter 4). What might have driven these organisms to return to the water? One factor probably was the ocean itself. In the Late Triassic and earliest Jurassic, Pangea began to slowly break apart into smaller landmasses. At this time, the continents were still close together, meaning that most of the world was covered by a huge ocean, interrupted only by shallow seas between the still-close continental landmasses. Without barriers formed by continents, the oceans provided a large range of habitat for these animals to occupy, reducing the competition they would have faced on land—a strong driver of evolutionary change. Global sea levels were also rising during the Mesozoic and peaked during the Cretaceous due to warm temperatures (water expands when warm) and rapid seafloor spreading associated with the separation of Pangea. When ocean basins are growing quickly, it leads to very broad mid-ocean ridges that force water up onto the continents. This would have created lots of warm, shallow oceans covering continental shelves that would create ideal habitats for these creatures to fill. Three major groups of marine reptiles dominated the Mesozoic oceans: ichthyosaurs, plesiosaurs, and mosasaurs (Figure 10.29). Ichthyosaurs have left no extant relatives, and their relationships to other marine

10.3  Taking to the Seas: The Swimming Reptiles (Mosasaurs, Ichthyosaurs, and Plesiosaurs)

245

Figure 10.29  Cladogram of Tetrapoda, with the various groups of marine reptiles (mosasaurs, ichthyosaurs, and plesiosaurs) highlighted. Although

many of them look superficially similar, not all of them are closely related to each other, and none of them are closely related to dinosaurs.

groups are also unclear, as is the identity of their specific diapsid ancestor. Plesiosaurs, which also include the shorter-necked pliosaurs (see below) are an extinct group that shares extreme adaptations of their shoulder girdle that fit a swimming lifestyle. Mosasaurs are squamates, and their closest living relatives are varanid lizards like the Komodo dragon. Figure 10.29 shows a simplified cladogram of where the different marine reptiles fit in the phylogenetic tree of tetrapods, and more specifically, where they fit in relation to other diapsids. Recall that diapsids are characterized by two pairs of holes (temporal fenestrae) behind their eye socket (Chapter 7). Living diapsids include everything we think of as a “reptile” (e.g., lizards, snakes, crocodiles) as well as birds, which are descendants of dinosaurs. In this cladogram, you can see that, in addition to not being dinosaurs, no lineage of marine reptiles are even members of Archosauria. Clearly, these swimming reptiles are not themselves closely related to one another, but they share a few convergent features—some of which are also found within living dolphins and whales, mammals that are evolutionarily far removed from these ancient reptiles. What are some of these convergent traits? Convergent traits that are (variably) found in extant and extinct secondary swimmers regardless of ancestry: • Streamlining: A streamlined body shape reduces drag in the water when swimming. • Modified vertebral columns: Individual vertebrae become shorter, and surfaces between them increase, to form a stable “beam” that can be pushed against for forward motion in the water. This is important for animals that use the spine for swimming. • Additional digits (polydactyly) or additional bones in their digits (hyperphalangy): Sometimes, the manus and pes of many swimming vertebrates can have extra digits, known as polydactyly. In others, the number of digits is reduced, and the number of phalanges (finger bones) increases; thus, although there are fewer digits, the digits are longer. Both of these adaptations function to expand the surface area of their swimming “paddles” (i.e., flippers), making movement through the water more efficient (Figure 10.30).

246

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

Figure 10.30  The paddle of a large mosasaur, found in ocean sediments (Pierre Shale) in central Canada.

The many extra bones in each digit is an example of hyperphalangy, a swimming adaptation that expands the surface area in contact with water, much like scuba divers wear fins to expand the surface area of their feet. (Courtesy of M. Schweitzer at the Canadian Fossil Discovery Centre, Manitoba, Canada.)

Figure 10.31  Full mount of a whale skeleton showing remnants of small pelvic bones (inset), testifying to their tetrapod and terrestrial ancestry.

(Photographed by K. Tiffany at the North Carolina Museum of Natural Sciences.)

• Reduction or loss of hind limbs: Although this has occurred frequently in lineages of living and extinct mammals that returned to the sea (Figure 10.31), the marine reptiles do not show this trend as much, testifying not only to different evolutionary origins of these groups, but also to the different mechanics of swimming. Marine mammals gain forward motion by using their tails and posterior body, but their spines are stiffer than most terrestrial mammals. Similarly, ichthyosaurs and mosasaurs used their stiffer backbones to push against the water. Plesiosaurs, on the other hand, used their limbs to generate lift, essentially “flying” underwater.

10.3.1 Ichthyosaurs Ichthyosaurs, or “fish-lizards” (ichthy = fish; sauros = lizard) (Figure 10.32), are strikingly similar in morphology to living dolphins (Figure 10.33), despite the fact that they are not closely related. Based upon functional morphology, these may have even occupied similar niches to dolphins during the Mesozoic. However, as with plesiosaurs, the ancestral group that gave rise to the ichthyosaurs is still debated. We do know that, like the other marine reptiles discussed here, ichthyosaurs are diapsids. They fall within Ichthyopterygia, an extinct group that has no living representatives.

10.3  Taking to the Seas: The Swimming Reptiles (Mosasaurs, Ichthyosaurs, and Plesiosaurs)

247

Figure 10.32  Cladogram of Tetrapoda, depicting the placement of ichthyosaurs (highlighted) within the group. Although they look strikingly similar

to living dolphins, they are very distant from mammals (synapsids) phylogenetically.

Figure 10.33  Although they are not closely related, dolphins (A) and ichthyosaurs (B) have very similar, convergent morphologies. (Courtesy of

K. Tiffany, ichthyosaur photographed at the Field Museum.)

The first ichthyosaurs are known from sediments about 250 million years old, almost immediately after the greatest extinction our planet has ever known. They thrived throughout much of the Mesozoic, reaching their peak diversity and distribution in the Late Triassic to Early Jurassic, expanding to include about 50 distinct genera. Ichthyosaurs were the top predators of the Mesozoic oceans until the emergence of the very successful Plesiosaurs. Ichthyosaurs could never have been food for T. rex, even if T. rex could swim, because they died out long before T. rex or Triceratops ever lived. The most recent ichthyosaur skeletal material was found in sediments dating to 90 million years ago, showing that they co-existed, at least for a short time, with the other predatory reptiles, mosasaurs and plesiosaurs. Although ichthyosaurs show a gradual decrease in diversity from the Middle Jurassic to Cretaceous, they still maintained a worldwide distribution until their final demise. It is thought that their decline and eventual disappearance may have been due in part to the arrival on the scene of more efficient competitors, but evidence is lacking to state this definitively.

248

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

Multiple exceptionally preserved specimens of ichthyosaurs have been found in the Posidonia Shale deposits of Holzmaden. Many show associated soft tissues, allowing us to determine their overall body shape—especially the outline of the tail fin, which sheds light on the biomechanics of swimming in this group. The Holzmaden strata also preserve many juvenile ichthyosaurs, and at least one specimen shows a young ichthyosaur emerging from the birth canal of its mother, indicating that they gave live birth. In fact, fossil evidence shows that these babies were born tail first, as are those of living whales! These observations have led some to propose that the Holzmaden represents a communal birthing ground/nursery for these animals, shedding light also on aspects of ichthyosaur behavior. The exceptional morphological preservation observed in Holzmaden specimens includes, in some cases, internal organs as well as skin. Recently, a cross-disciplinary study employing a host of specific and sensitive methods was able to show that this exceptional morphological preservation extends to the molecular level. The preserved skin, when sectioned and visualized under the microscope, shows the presence of pigment-containing cells and cellular layers, like the ones seen in the skin of living animals. This specimen also showed folds and wrinkles that are remarkably similar to those seen in degraded dolphin skin. Multiple methods confirmed the presence of proteins, lipids, and pigments associated with the liver and skin, and in-depth chemical analyses of this specimen served to confirm, for the first time, the presence of blubber in an extinct species. This is important because blubber is only found in animals with elevated metabolic rates, so its presence in this ichthyosaur lends strong support to the hypothesis that this very ancient group of vertebrates returned to the ocean with elevated metabolic rates, making it not just morphologically, but also molecularly, similar to endothermic dolphins! These data support earlier studies that used stable isotope ratios and fast growth rates to suggest endothermy in this group. Morphological traits and global distribution also lend support to endothermy in this lineage, in that the skulls and skeletons of ichthyosaurs show features that are consistent with a high-speed, highly maneuverable locomotion style. If upheld, these would be the earliest animals for which we have evidence of a metabolic rate approaching endothermy. Additionally, some forms are thought to have been able to dive to depths exceeding 500 meters! They exhibit both polydactyly and hyperphalangy, helping the flipper to act as a hydrofoil for increased maneuverability. Additionally, ichthyosaurs had very large eyes—in fact, they had the biggest eyes (proportionately) of any animal, living or extinct (possibly only rivaled by the extant giant squid), and many specimens show the presence of a sclerotic ring (Figure 10.34) in their orbital (eye socket). A sclerotic ring is a ring of bones inside the eyes of some vertebrates. One function of this ring is to help the eyeball hold its shape. Ichthyosaur eyes, in addition to being really big, were also flattened, and the water pressure against the eyeball of fast swimming and deep diving ichthyosaurs would be offset by the added support of this bony ring. Thus, this structure would help to maintain visual acuity underwater. Sclerotic rings are also found in living birds of prey, including owls, as well as some non-avian dinosaurs, but they are not known to be present in any mammal. The excellent vision implied by these large eyes may have been an adaptation to their deep-water swimming abilities, but may also have been an adaptation for observing large predators, made necessary by the emergence of aggressive plesiosaurs and mosasaurs.

10.3  Taking to the Seas: The Swimming Reptiles (Mosasaurs, Ichthyosaurs, and Plesiosaurs)

249

Figure 10.34  Skull of ichthyosaur Shonisaurus, showing the bony sclerotic ring within the orbit. This

structure is convergent with that seen in some birds and other vertebrate organisms. (Adapted from Kumiko, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=42​ 12814​3.)

Figure 10.35  Cladogram of Tetrapoda, depicting the placement of plesiosaurs (highlighted) within the group. Plesiosauria consists of

two main groups: Pliosaruomorpha and Plesiosauromorpha.

10.3.2 Plesiosaurs The order Plesiosauria includes two main body shapes, or morphotypes (Figure 10.35): the short-necked, large-headed, streamlined Pliosauromorphs and the long-necked, small-headed Plesiosauromorphs. There are no living members of either of these groups. Pliosauromorph plesiosaurs, with their shorter necks and proportionately longer skulls, had large conical teeth and have been interpreted as the top predators of Mesozoic oceans (Figure 10.36). The robust form, large teeth, and heavy-duty skulls seen in most pliosauromorphs made them well suited for taking down large prey, a hypothesis that is supported by the presence of small ichthyosaur bones in the stomach contents of some specimens. These diverse and successful marine predators were first found in Late Triassic to Early Jurassic marine sediments (~ 200 Ma). Plesiosaur vertebrae were the first evidence of this group and were described by a Belgian naturalist named Richard Verstegan in the 1600s, though he mistakenly attributed them to fish. The first scientific description of a partial

250

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

Figure 10.36  A full skeleton mount of the pliosauromorph. Pliosauromorphs

are differentiated from plesiosauromorphs by their relatively short neck and robust skull with large teeth. This pliosauromorph does not show a loss or reduction in hindlimbs as in some other marine vertebrates (e.g., whales) but does share the trait of hyperphalangy. (Photographed by M. Schweitzer at the Canadian Fossil Discovery Centre, Manitoba, Canada.)

Figure 10.37  Skeleton of Elasmosaurus, a plesiosauromorph.

Plesiosauromorphs differ from pliosauromorphs by having a longer, more gracile neck, a long tail, and a smaller more delicate skull. (Courtesy of E. Howard at the Milwaukee Public Museum, https​://co​ mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=64​19371​7.)

skeleton was not published until the 1820s. Thus, despite this delay in the correct assignment, plesiosaurs are among the first extinct reptiles to be scientifically recognized. In contrast to the pliosaurs, plesiosauromorphs have a broad, flattened body, and because some show bony reinforcements on their ventral skeleton, they are vaguely reminiscent of a turtle. They are distinguished from other marine groups by their very long necks, small heads, and extreme polydactyly (Figure 10.37). Their teeth are smaller, and their skulls more delicate, than the closely related pliosauromorphs, making them better suited for a diet of fish and smaller prey. Some, however, may have preferred a diet of ammonites and mollusks, based upon preserved stomach contents. Like mosasaurs (below), bone histology and isotope ratios of some plesiosauromorph specimens suggest they had a metabolic rate somewhat elevated over fish, but whether they were fully endothermic is not known. An articulated specimen was recently described as having a rather large embryo within its body cavity, supporting the hypothesis that like ichthyosaurs, these too gave live birth. Pliosaurs achieved lengths of up to 50 ft (~15 m), the size of some living humpback whales. Because of their longer necks, some plesiosauromorphs were longer, attaining lengths of about 60 ft (~18 m). It has been suggested that the two groups had different swimming modes, and thus different predation styles. However, both groups were well-adapted swimmers, using their long and robust limbs to swim, rather than the backbone like ichthyosaurs and marine mammals do. They also possess expanded bony plates on the underside of the body to house the large and powerful swimming muscles (Figure 10.38).

10.3  Taking to the Seas: The Swimming Reptiles (Mosasaurs, Ichthyosaurs, and Plesiosaurs)

251

Figure 10.38  Ventral view of a plesiosaurimorph, showing expanded bony plates to anchor powerful swimming muscles. (Adapted from

Ra’ike, taken at the Museum am Löwentor, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=45​48762​.)

Figure 10.39  Cladogram of tetrapods, showing the placement of mosasaurs (highlighted) relative to other groups.

Although superficially similar in morphology to ichthyosaurs and plesiosaurs, mosasaurs are phylogenetically very distant from these groups, more closely related to snakes.

Both pliosauromorphs and plesiosauromorphs radiated widely in the Jurassic, but all became extinct at the end of the Cretaceous, at the same time non-avian dinosaurs disappeared.

10.3.3 Mosasaurs The last group of giant marine reptiles we will consider are the mosasaurs (Figure 10.39). Like pterosaurs, mosasaurs (and the other marine reptiles) are not dinosaurs, although they are often grouped with them in movies and coloring books (Figure 10.40). But even more, these animals are not even archosaurs, and far more distantly related to dinosaurs than are crocodiles! However, the presence of two pairs of fenestrae behind their eye sockets makes them diapsids, and thus we can infer a common ancestor with dinosaurs at some point in the very distant past. Unlike the icthyosaurs and plesiosaurs, for which direct ancestors are not known, analyses of features in the bones and skeleton of mosasaurs show that these massive sea creatures fall into the group Squamata (Figure 10.39), and are more closely related to varanid lizards, such as the Komodo dragon, than they are to dinosaurs. Their terrestrial ancestry is

252

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

Figure 10.40  Mounted skeleton of a mosasaur. These massive, widespread

ocean predators are known from many specimens and divide into several groups. Although they show similarities with ichthyosaurs and plesiosaurs, including a sclerotic ring, they are much more closely related to Komodo dragons than they are to other groups of swimming reptiles. (Photographed by M. Schweitzer at the Smithsonian Institution, with permission.)

shown by their somewhat robust hindlimbs, which had expanded “paddles” for efficient swimming. Mosasaurs came to the attention of scientists at least 50 years before the first dinosaur was discovered and described. The first documented Mosasaurus find, in 1770, was found in an underground quarry near Maastricht, The Netherlands, and the name Mosasaurus is derived from “Mosa” (for the river Meuse, which flowed near the quarry where it was discovered), and “sauros” for lizard. Mosasaurs are relatively recent, compared with the plesiosaurs and ichthyosaurs, both of which originated just after the Permian–Triassic extinction. Mosasaurs first put in an appearance in the early Late Cretaceous, after the extinction of the ichthyosaurs. Their streamlined body, fin-like extremities, and two-lobed tail fin made them efficient swimmers, well adapted for an obligate marine lifestyle. Biomechanical studies suggest that they swam by moving their tail and posterior body from side to side (i.e., used their backbone for propulsion) more like a fish than a whale, which propels itself by moving its tail up and down. Their large eye sockets suggest that they hunted using sight and the bones housing their auditory organs indicate that their underwater hearing was acute. They also had double rows of teeth, extending far back into the roof of the mouth. So what did these top predators eat? The evidence from tooth shape and stomach contents indicates that different forms had different diets, ranging from other vertebrates to shelled invertebrates. Even as late arrivals, mosasaurs diversified rapidly, and were global in distribution—by any measure one of the most successful of Mesozoic lineages. At least 38 genera are known for this group, ranging in size from small, lizard-like creatures not much over 3ft (~1 m), to the massive leviathans that dominated the End-Cretaceous seas, and which reached 45 feet (~13 m) in length. Like whales and dolphins, they breathed air, and like whales and dolphins, there is evidence that these top predators may also have given birth to live young, rather than having to return to land to lay eggs, as sea turtles do. In fact, with their greatly adapted skeletons, it would have been almost impossible for them to crawl onto beaches to lay eggs. To support this idea, in 2001, an exceptionally well-preserved mosasaur skeleton was reported to have evidence of three embryos retained within its abdomen. In addition to giving live birth, other data suggest that at least the more derived mosasaurs may have possessed an elevated metabolic rate, regulating their body temperatures to be consistently warmer than the water surrounding them. Stable isotope studies, conducted on the teeth and bones of large mosasaurs and compared with fossil fish (assumed to be ectothermic) and seabirds (likely endothermic), suggest that they could maintain their internal body temperatures above that of the surrounding ocean waters. This was somewhat surprising, given that their closest relatives, the varanids, are fully ectothermic.

10.4  What We Don’t Know

When first discovered, mosasaurs were thought to be slender animals with paddle-shaped tails; however, new evidence from mosasaurs that preserve soft tissues, including scaly skin, show otherwise. These skin outlines shed light on the size and shape of the tail flukes, and indicate that they were streamlined and powered by a two-lobed tail fin, suggesting that these organisms experienced evolutionary pressures comparable with the preceding ichthyosaurs and the whales that followed them. In more advanced mosasaurs, skin impressions suggest that the scales appear to diminish in size, perhaps because smaller scales enhance streamlining and reduce drag. This is similar to some marine turtles that have also lost the scaly skin of their ancestors. At least one mosasaur has also preserved evidence of osteocytes (bone cells) and others preserve pigment-containing cellular organelles, suggesting that at least some of these animals may have been counter-shaded. This means that they were likely darker on the dorsal side, and pale on the underside, similar to the vast majority of living tetrapods that have returned to the seas. Indeed, mosasaur lineages are one of the best examples of both macroevolution and convergence in vertebrates.

10.4 WHAT WE DON’T KNOW 10.4.1 What Is the Evolutionary History of Pterosaurs, and What Behaviors Did They Exhibit? There are no extant animals alive today that are similar to pterosaurs, and this makes it especially hard to understand their evolutionary history as well as the origin and use of the many strange characters they exhibited. The mysteries surrounding pterosaurs are numerous, including what they ate, how they obtained food, why they evolved such large sizes, how their wing membranes attached to their body, and how they moved on land. Hopefully new pterosaur fossil discoveries will continue to shed light on these odd, but marvelous creatures. Questions to consider: • How could a thin wing membrane support the weight of the more massive pterosaurs like Quetzalcoatlus? • Were pterosaurs capable of diving into water or skimming the surface to catch fish? Or was their diet mainly composed of insects or something else entirely? • What type of metabolic strategy did pterosaurs employ? • Did pterosaurs have feathers or feather-like structures, and are feather-like features ancestral in Avemetatarsalia (the clade including dinosaurs and pterosaurs)?

10.4.2 Where Did the Three Main Groups of Marine Reptiles Come From, and Why Did They Go Extinct? Marine reptiles were exceedingly successful and diverse, but their ancestral relationships are not clear and Plesiosauria, Ichthyopterygia, and Mosasauria all had different ancestors. It is evident that although some of the marine reptiles were driven to extinction at the same time as the dinosaurs, animals that live in water are generally buffered somewhat from ecological factors that affect terrestrial animals. The factors that drove these successful vertebrates to extinction are unknown. In particular, the extinction of the ichthyosaurs remains a mystery. Failure to compete with emerging mosasaurs has been proposed, and bony evidence in some ichthyosaurs suggests multiple incidents of “the bends” (i.e., decompression

253

254

CHAPTER 10    How Do We Name and Group Mesozoic Animals That Are Not Dinosaurs?

sickness). Perhaps the more efficient predators that displaced them required them to swim in areas to which they were not optimally adapted. Questions to consider: • What were the terrestrial animals that gave rise to Plesiosauria, Ichthyopterygia, and Mosasauria? • Why don’t we have marine reptiles today? If whales and dolphins could have returned to the sea from terrestrial form since the extinction event at the end of the Cretaceous, why did the same selective pressures not lead to terrestrial reptiles returning to the sea? • Many fish and sharks survived the End-Cretaceous extinction (Chapter 20), so why did the marine reptiles go extinct?

CHAPTER ACKNOWLEDGMENTS We thank Dr. Brian Andres and Dr. Johan Lindgren for their generous reviews and suggested improvements to the pterosaur and marine reptiles sections, respectively. Dr. Andres is an Assistant Professor in the School of Geosciences at the University of South Florida. Dr. Lindgren is a Senior Lecturer in the Department of Geology at Lund University in Sweden.

INSTITUTIONAL RESOURCES Everhart, M. J. (2017). Oceans of Kansas: A Natural History of the Western Interior Sea. Indiana University Press, Bloomington. Hone, D. W., Witton, M. P., and Martill, D. M. (2018). New perspectives on pterosaur palaeobiology. Geological Society, London, Special Publications, 455(1), 1–6. http://pterosaur.net/. Pterosaurs: Flight in the age of dinosaurs from the American museum of natural history. https​://ww​w.amn​h.org​/exhi​bitio​ns/pt​erosa​urs-f​l ight​-in-t​he-ag​e-of-​dinos​aurs. Witton, M. P. (2013). Pterosaurs: Natural History, Evolution, Anatomy. Princeton University Press, Princeton, New Jersey.

LITERATURE Cleary, T. J., Moon, B. C., Dunhill, A. M., and Benton, M. J. (2015). The fossil record of ichthyosaurs, completeness metrics and sampling biases. Palaeontology, 58(3), 521–536. Fleischle, C. V., Wintrich, T., and Sander, P. M. (2018). Quantitative histological models suggest endothermy in plesiosaurs. PeerJ, 6, e4955. Lindgren, J., Sjövall, P., Thiel, V., Zheng, W., Ito, S., Wakamatsu, K., Hauff, R., Kear, B. P., Engdahl, A., Alwmark, C., Eriksson, M. E., Jarenmark, M., Sachs, S., Ahlberg, P. E., Marone, F., Kuriyama, T., Gustafsson, O., Malmberg, P., Thomen, A., Rodríguez-Meizoso, I., Uvdal, P., Ojika, M., and Eriksson, M. E. (2018). Soft-tissue evidence for homeothermy and Crypsis in a Jurassic ichthyosaur. Nature, 564(7736), 359–365. Liu, S., Smith, A. S., Gu, Y., Tan, J., Liu, C. K., and Turk, G. (2015). Computer simulations imply forelimb-dominated underwater flight in plesiosaurs. PLoS Computational Biology, 11(12), e1004605. Parker, W. G. (2016). Revised phylogenetic analysis of the Aetosauria (Archosauria: Pseudosuchia); assessing the effects of incongruent morphological character sets. PeerJ, 4, e1583.

Upchurch, P., Andres, B., Butler, R. J., and Barrett, P. M. (2015). An analysis of pterosaurian biogeography: Implications for the evolutionary history and fossil record quality of the first flying vertebrates. Historical Biology, 27(6), 697–717. Wang, X., Kellner, A. W., Jiang, S., Cheng, X., Wang, Q., Ma, Y., Paidoula, Y., Rodrigues, T., Chen, H., Sayão, J. M., Li, N., Zhang, J., Bantim, R. A. M., Meng, X., Zhang, X., Qiu, R., and Li, N. (2017). Egg accumulation with 3D embryos provides insight into the life history of a pterosaur. Science, 358(6367), 1197–1201. Witton, M. P., and Habib, M. B. (2010). On the size and flight diversity of giant pterosaurs, the use of birds as pterosaur analogues and comments on pterosaur flightlessness. PLoS One, 5(11), e13982. Yang, Z., Jiang, B., McNamara, M. E., Kearns, S. L., Pittman, M., Kaye, T. G., Orr, P. J., Xu, X., and Benton, M. J. (2019). Pterosaur integumentary structures with complex feather-like branching. Nature Ecology & Evolution, 3(1), 24–30.

11 HOW DO WE KNOW HOW DINOSAURS BECAME PART OF THE FOSSIL RECORD?

11

TAPHONOMY AND FOSSILIZATION

I

f we want to understand dinosaurs, we are limited to those body parts that become incorporated into the rock record. But when we compare the bones from a dinosaur quarry with those of a freshly killed deer, it is obvious that these differ significantly in size, texture, completeness, color, and other factors. Much of the original information that was once present is lost. So how can we go about reconstructing it? To understand what was lost, we must understand the processes that lead to that loss. What happens to an animal after it dies? What changes occur in an animal’s body after death? After burial? During fossilization? For that matter, what even is a fossil?

IN THIS CHAPTER . . .

11.1 ENTERING THE ROCK RECORD: A HOW-TO GUIDE

11.1 ENTERING THE ROCK RECORD: A HOW-TO GUIDE

After reading this section you should be able to… • Define the term fossil.

Before we drill down into the process of fossilization in all its complexity, we need to define the term “fossil” and discuss the stages of how something goes from a living animal to a preserved specimen on display in your local museum. Defined simply, a fossil is any evidence of past life. Fossilization can occur in many different ways, but there are a few basic steps that are vital to the process.

11.2 TAPHONOMY AND TAPHONOMIC LOSS 11.3 DEATH TO DIRT: BIOSTRATINOMY 11.4 DIRT TO DISPLAY: DIAGENESIS 11.5 DIFFERENT TYPES OF FOSSILS 11.6 A CASE STUDY 11.7 WHAT WE DON’T KNOW

256

CHAPTER 11    How Do We Know How Dinosaurs Became Part of the Fossil Record?

To become a fossil, you must: 1. Die: Without exception, the first step on the path for a living animal to becoming a fossil is to die, regardless of how that death occurs. There is no such thing as a still-living fossil. Although you may have heard some animals, like a fish called a coelacanth, referred to as a “living fossil”, this simply means that they are part of a very old lineage of lobe-finned fishes, a group of which most members are long extinct. 2. Become buried: While there are some exceptions, in order to prevent total destruction of an organism after its death, the remnants of its body must be physically protected by burial in some type of medium. This is not limited to burial with sediment; fossils can also be “buried” in ice or amber. 3. Preserve: Even once they’re buried, the vast majority of animals that have ever lived on this planet do not persist into the rock record. Rather, would-be fossils must be subjected to a chemical environment that slows or arrests typical degradative processes long enough for the tissues to become stabilized, rather than completely breaking down. This usually occurs when minerals from the environment become incorporated into the degrading tissues. This association with minerals allows them to persist over millions of years. Also, once these steps have occurred, it becomes a matter of luck and timing (and a bit of skill) whether a fossil will be found by a scientist and added to a museum or university collection. Just as most animals will never become fossils, most fossils that are currently out there, buried in the rock record, will never be found! The circumstances surrounding each of the above three steps on the path to becoming a fossil have a profound effect on the final product, and it is imperative to take them into account when interpreting fossil specimens. If the processes involved in fossilization are not considered each time we study any fossil, our interpretations can be misleading, or wrong. The rest of this chapter will discuss the nature and variety of the changes animals may undergo after death, and how we learn about them from the fossils they leave behind.

11.2 TAPHONOMY AND TAPHONOMIC LOSS After reading this section you should be able to… • Define the two phases of taphonomy and give examples of each.

We know about ancient life, and the progression of organisms that inhabited our world, only because of the fossils they leave behind. But how exactly does this happen? When you think about it, degradation is the norm! It is rare indeed when organisms don’t degrade to completion. In almost all cases, processes of degradation, dissolution, and rot are active and enormously efficient—if not, we would be knee-deep in dinosaur carcasses to this day! Thus, it is exceedingly rare for an organism to become a fossil. Indeed, it is a one in a million (0.000001%) chance that a once-living organism will enter the fossil record. So what factors increase the chance of an organism becoming a fossil? As discussed above, death, burial, and preservation profoundly change an organism on its path from life to fossil. The scientific study of all changes an organism undergoes, from the moment its life processes cease until it is on display in a museum, is called taphonomy.

11.2  Taphonomy and Taphonomic Loss

Taphonomic processes are broken into two main phases (Figure 11.1): 1. Biostratinomy: All the processes an organism undergoes from the moment it dies to the moment it is buried. These include (but are not limited to) processes like bloat, scavenging, and trampling. Once burial occurs, these processes are either arrested or greatly reduced—thus, rapid burial is a friend to paleontologists! 2. Diagenesis: All the processes an organism undergoes after burial. These include processes like mineral recrystallization, or distortion from geological pressure of overlying rocks. Look carefully at the starting and ending points of the little turtle in Figure 11.1. What is missing at the end of the process, when the fossil is compared with the living animal? How is the fossil different from a freshly killed organism? The result of every taphonomic process, no matter what they are or when they occur, is taphonomic loss; the loss of information critical to our understanding of the once-living organism. These can include things like its color, presence of soft tissue appendages (like an elephant’s trunk), diet, metabolic and reproductive strategies, body temperature, speed, or genetic information. Depending on the preservational environment, many aspects of an animal’s life are progressively less “knowable” the more time passes from its death.

257

Figure 11.1  Schematic depicting the processes encompassed in taphonomy. All processes that occur to an

organism from the moment it dies until it is buried constitute biostratinomy. Once an organism is buried, biostratinomic processes cease, and diagenesis occurs. Diagenesis continues until the organism, now a fossil, is discovered and removed from the natural environment. (Image of living turtle courtesy of Wildlifeppl, https​://co​mmons​.wiki​media​ .org/​w/ind​ex.ph​p?cur​id=16​72778​7; image of fossil turtle courtesy of R. Sylvestersen, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=25​03295​8.)

Let’s look at this concept up close. Figure 11.2 is a photograph of a modern deer that was found along a running trail. What do you observe about this animal? What is still present? What has been lost? What has been altered or rearranged? If you had never seen a living deer, what might you conclude about the structure of one, based on these remains? Figure 11.2  The skeleton of a small, winter-killed deer (center) shows early biostratinomic processes. A closer

inspection of the skull (left) illustrates one of the “players” in taphonomy (arrow). The hindquarters (right) illustrate another huge source of taphonomic loss—disarticulation. (Courtesy of M. Schweitzer.)

258

CHAPTER 11    How Do We Know How Dinosaurs Became Part of the Fossil Record?

Look closer at the enlarged image of the skull (left). What else do you learn about this animal? What other information, now lost, would you need to reconstruct the living animal? Can you tell anything about possible interactions with other organisms? Now, look at the enlarged view of the animal’s hindquarters. What is surprising to you? What is missing? Given just these remains, how much can you tell about the age of the animal? The color? How fast it ran? What tissues do you think are most likely to preserve in the fossil record? With all this information loss then, how can we say anything about the lives and deaths of dinosaurs that have been extinct 65 million years (or more)? We start by applying the Principle of Uniformitarianism (see Chapter 2). As a refresher, this principle states that processes we can observe today also happened in the past, and our knowledge of modern processes can therefore be applied to past events we cannot directly observe. In short, “What we observe in the present is key to understanding the past”. This doesn’t just apply to geological processes like sediment deposition and mountain building, it also applies to life/death processes like scavenging or predation. Thus, processes that result in certain patterns today, such as those we observed above in the deer, are probably implicated when we see similar patterns in fossils like dinosaurs. Only by keeping these patterns in mind can we accurately interpret the fossils of dinosaurs when we find them.

11.3 DEATH TO DIRT: BIOSTRATINOMY After reading this section you should be able to… • Explain the difference between articulated and disarticulated skeletons. • Describe key biostratinomic processes that can occur after the death of a dinosaur. • Predict how a biostratinomic process will affect the fossilization of a dead dinosaur.

Biostratinomic processes begin the moment an animal dies. Thus, the way an animal dies is an important variable in its taphonomic pathway to fossilization. Some ways of dying can eliminate the possibility of an animal even becoming a fossil—animals that fall into extremely hot flowing lava will disintegrate long before the lava flow solidifies, and dinosaurs at ground zero of an asteroid impact would be obliterated rather than fossilize. However, there is a great variety of (more mundane) ways to die, all of which will affect the fossils left behind, and the interpretations we make from them. Let’s imagine a scenario in which an old, sick animal wanders off by itself, to a place where a scavenger doesn’t find it. After it dies, its body undergoes bloat (Figure 11.3) and other processes that distort its soft tissues, perhaps leading to partial disarticulation of limbs and other elements— that is, its bones become unattached from each other. Unless something else happens, though, there is little movement, and the skeleton remains mostly articulated (i.e., still hooked together). If we were to find these bones fossilized millions of years later, the bones might still be attached in partial articulation, and the ones that have become disarticulated are usually found lying near or associated to the rest of the skeleton—this conveys that they are part of the same skeleton, but are now unattached to it in a way they would have been when the animal was alive—more information loss! How would the results in Figure 11.3 be different if an animal were killed by a large predator? How would you predict that would affect the

11.3  Death to Dirt: Biostratinomy

259

Figure 11.3  Carcass of a pig going through various stages of biostratinomic changes. (A) Bloat occurs

state of the skeleton in the moments after death? What if the same animal is instead the victim of a pack of predators? How might its remains look different after they are gone compared to how they would look after being taken down by a single predator (Figure 11.4)? Regardless of how an animal dies, it will usually go through well-understood stages early in taphonomy that are both predictable and that have an effect on their eventual entry into the fossil record.

shortly after death and is temperaturedependent. The gasses within the body, coupled with the stiffening of rigor, cause the fore- and hindlimbs to straighten. Additionally, the skin thins and begins to discolor. When the pressure increases from the accumulating internal gasses, the skin ruptures and the inner organs spill out. (B) Organisms of decay are active, and extensive mass loss occurs. (C) After some time, these processes slow down, but continue to proceed. (D) Eventually, skeletonization occurs. What implications does the progress of these decay stages have for how we look for and interpret dinosaur fossils? (Courtesy of Hbrenton19, A: https://commons.wikimedia.org/wiki/ File:Exam​ple_o​f_a_p​ig_ca​rcass​_in_t​he_bl​ oat_s​tage_​of_de​compo​sitio​n.jpg​; B: https:// commons.wikimedia.org/wiki/File:Exam​ ple_o​f_a_p​ig_ca​rcass​_in_t​he_ac​tive_​decay​ _stag​e_of_​decom​posit​ion.j​pg; C: https:// commons.wikimedia.org/wiki/File:Exam​ ple_o​f_a_p​ig_ca​rcass​_in_t​he_ad​vance​d_dec​ ay_st​age_o​f_dec​ompos​ition​.jpg;​ D: https:// commons.wikimedia.org/wiki/File:Exam​ ple_o​f_a_p​ig_ca​rcass​_in_t​he_dr​y_dec​ay_st​ age_o​f_dec​ompos​ition​.jpg.​)

11.3.1 Rigor Soon after death, a process called rigor (i.e., rigor mortis) sets in, usually within hours. Rigor is preceded by other recognizable stages, including algor mortis, pallor mortis, and livor mortis, but these processes are not directly discernible on skeletal remains, and so we won’t discuss them here. Rigor mortis is the stiffening and contraction of body muscles caused by changes in chemistry within the body after death; the chemicals responsible for contracting muscles can continue to be produced for a while after an animal stops breathing because they can be made anaerobically (without oxygen). The chemicals required to relax muscles require oxygen, thus, they can no longer be produced in tissues after an animal stops breathing. As a result, rigor initially causes all the muscles in a dead body to contract, which distorts the overall position the body parts were held in by the animal during life (Figure 11.5). These forceful muscle contractions can realign skeletal elements, causing the limbs to stiffen or the spine to curl and contract. These contortions of the body can result in an overall appearance suggesting that an animal died in

Figure 11.4  (A) Lionesses taking down a water buffalo. (B) A wedge-tailed eagle scavenging from roadkill. How

do you think the manner of death affects entry into the fossil record? That is, in what ways do you think an animal that has undergone predation and scavenging prior to burial such as the ones above, and one that has been left to decay without interference (e.g., Figure 11.3), might leave different remains? Predation and scavenging are frequent in today’s environments, and undoubtedly were in the age of dinosaurs as well. These processes were part of the reason that most of our dinosaur finds consist of only part of a skeleton. (A courtesy of Corinata, https​:// co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=80​52349​; B courtesy of Djambalawa, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=39​53856​.)

260

CHAPTER 11    How Do We Know How Dinosaurs Became Part of the Fossil Record?

Figure 11.5  The state of rigor mortis is illustrated in this extremely wellpreserved human mummy. Oetzi

the iceman was found partially frozen in a glacier, and it is estimated that these remains date to ~5,300 years ago. Rigor caused contraction of his arms, and then he became encased in ice, leaving his arms permanently displaced in this awkward position. (Courtesy of bastiaan, https​://pi​ xabay​.com/​photo​s/%C3​%B6tz​i-hum​an-mu​ mmy-2​77986​/.)

pain even if it died painlessly in its sleep—a perfect example of why we must be careful in our interpretations of fossils, and ground them in observations of modern processes. Eventually, the chemicals that cause these contractions break down and the muscles relax again, but if burial happens quickly while the animal is still in rigor, as in this Gorgosaurus (Figure 11.6), it will fossilize in this contorted position. Because we can observe and estimate the timing of rigor in extant animals today, when we find a dinosaur in such a pose, it gives us an estimate of how quickly after death burial occurred—in this case, within hours of death.

11.3.2 Bloat If an animal is not dismembered, but left relatively intact after its death, gasses build up fairly rapidly within its body cavities, causing the carFigure 11.6  Rigor can result in some spectacular dinosaur poses as well.

The muscles holding the neck upright (in both human and dinosaur) are stronger than those pulling it to the chest. Thus, in full rigor, the dorsal neck muscles often win this tug-of-war. If a researcher is not aware that this is a natural process, fossils such as these could be—and sometimes were—interpreted as the result of disease. (Courtesy of Traumador the Tyrannosaur (https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=53​09921​.)

11.3  Death to Dirt: Biostratinomy

261

Figure 11.7  Depiction of the “bloat and float” biostratinomic process that led to the preservation of a hadrosaur, Kamuysaurus japonicus, in marine sediments of Japan. The

fact that this dinosaur was found in ocean sediments does not mean it lived in the ocean; rather it is the result of taphonomic processes that transported it after death. However, the proximity of this animal to the ocean at the time of its death may mean that the natural habitat of this dinosaur was similar to today’s coastal plains. (Courtesy of M. Hattori, https://commons.wikimedia.org/ wiki/File:Carcass_of_Kamuysaurus.jpg.)

cass to swell, or bloat. The combination of swelling (bloat) and rigor results in substantial distortion of the body’s original shape—until the gasses are released and the carcass collapses in on itself. This collapse can disarticulate parts of the body, making the pieces easier to be transported elsewhere by other physical forces. During this process of bloat, a carcass is so full of gasses that it can actually float. Thus, if an animal dies near water, it can float a very long distance from the site of its death. This can include being carried off down a river, out into a lake, or even out into deep ocean environments (Figure 11.7). We call this phenomenon (somewhat morbidly) “bloat and float”, and it's the key to interpreting fossils that we find in marine environments that clearly didn’t live there. Dinosaurs, for example, were not marine animals—no species of dinosaur had flippers or were morphologically adapted to live in the ocean. But we do sometimes find the skeletons of dinosaurs in ocean sediments, where they couldn’t possibly have lived, and these can be explained by “bloat and float” taphonomic processes. Again, without awareness of these processes, we could be very wrong about the environments inhabited by dinosaurs.

11.3.3 Scavenging and Predation Predation and scavenging can result in substantial taphonomic loss. Scavenging, in particular, can occur at any point before an animal gets buried—before or after rigor and bloat, whether an animal dies naturally or was already the victim of predation. Both predators and scavengers pick apart the body and can carry parts off (Figure 11.8) or swallow them, so that they end up far removed from the rest of the body’s original position. Scavenging and predation can also leave tell-tale marks on the bone, including tooth scars and gnaw marks (see Chapter 15), tooth punctures (Figure 11.9), and drag marks. Whether in recent or fossil bones, the bites of a toothy predator (lion, tiger, or velociraptor) or scavenger (small rodents, hyenas, or vultures) leave an indelible mark that can change the rate and degree of degradation, because they disrupt the integrity of the bone. Sometimes, they can even leave a whole tooth (Figure 11.10)! These taphonomic indicators can also tell us much about ecological interactions. In this case, we know the tip of a T. rex tooth is not likely to end up buried in the vertebra of a hadrosaur (duckbill) dinosaur by being carried downstream in a

262

CHAPTER 11    How Do We Know How Dinosaurs Became Part of the Fossil Record?

Figure 11.8  Scavenging and predation are important taphonomic causes of disarticulation and information loss.

This hawk has dismembered a rodent. How might that influence how (and if) this rodent enters the fossil record? (Courtesy of S. Jurvetson, https​://co​mmons​.wiki​media​ .org/​w/ind​ex.ph​p?cur​id=11​05819​.)

Figure 11.9  This shows tooth marks in a pedal phalanx (i.e., toe bone) of a Tyrannosaurus rex. The size, shape, and

serrations of the tooth marks on this bone match most closely to another T. rex. These tooth marks are evidence that T. rex may have practiced cannibalism, and are also part of the taphonomic history of this bone. (Adapted from N.R. Longrich, J.R. Horner, G.M. Erickson, P.J. Currie, https​://do​i.org​ /10.1​371/j​ourna​l.pon​e.001​3419.)

river. Instead, a find like this is very strong evidence that a T. rex made a meal of this dinosaur.

11.3.4 Transport Many of the processes described above result in transport, or the movement of some or all parts of the animal to a location different than the site of its death. Thus, when coming to conclusions about dinosaur habitats and ecologies, it is vital to keep the basic principles of transport in mind! Additionally, understanding transport patterns is of practical importance, because if we find a single dinosaur bone, like a piece of the skull or a tail vertebra, understanding the different ways transportation occurs can affect how we search an area for the rest of the skeleton. In skeletal elements that have undergone water transport, we see some general patterns. Heavier bones are usually transported over the least amount of distance, while lighter ones can travel relatively farther. Additionally, similar elements move in a similar manner; for example, if five cows die in a storm and their bodies all come to rest at the same place,

11.3  Death to Dirt: Biostratinomy

263

Figure 11.10  The tip of a tyrannosaur tooth was found embedded in the vertebral body of an Edmontosaurus.

Because the bone shows signs of healing, we can say two things: first, this was not a killing blow—this lucky hadrosaur got away and lived long enough to start healing. Second, this bite was an act of active predation, not scavenging. (Adapted from image courtesy of D.A. Burnham and R. DePalma.)

say in the bend of a river after a flooding event, all the limb elements will move about the same distance from their original position. In fact, sometimes in bonebeds with multiple individuals, we see piles of similar bones together (e.g., ribs, limb bones), where the water has “sorted” them based upon size, shape, or mass. In terms of skeletal elements themselves, the pattern observed in modern examples is that lighter, more porous bones, such as vertebrae, sacra, phalanges (digits), and patellae (kneecaps), are transported over greater average and total distances downstream than heavier, denser bones like limb bones and mandibles (jaw bones). The small bones at the tip of the tail and the forelimbs are often the first to be removed and tend to be carried the furthest distances. Of course, porosity isn’t the only factor at work, so things aren’t quite that simple; the shape of bones also has partial control over their transport. For example, let’s consider the ribs. Ribs are lightweight and porous, so you might predict they would be carried easily and removed some distance from the body. However, because they are long and slender, in natural systems they start moving end-over-end (i.e., spinning). This causes them to get caught up and buried earlier, and therefore move a shorter distance than you might otherwise predict. Another factor that must be considered in bone transport is the flow of the water and the shape of the channels. A meandering river has lots of bends and that greatly affect transport, and can decrease the energy of the water as well. Indeed, many bones are often found at bends of river channels known as point bars (Figure 11.11), where the water slows and no longer has the energy to carry the heavier elements such as sand and bones. Thus, they get trapped and are deposited on these relatively shallow turns. Conversely, in areas of the river where the water flows faster, and the energy in the system is higher, bones carried by the water can be moved much farther from their point of origin. What does all of this have to do with dinosaurs? Suppose you are out walking in the badlands of Montana, and you come upon what you think is a femur of a dinosaur. There aren’t any other bones exposed, just this one. How will you know where to start looking for other bones that

264

CHAPTER 11    How Do We Know How Dinosaurs Became Part of the Fossil Record?

Figure 11.11  (A) Diagram of a meandering river, showing how current speed is different at different locations of the bend. When water goes around the many curves of a meandering river, the fastest current is on the outside of the bend, and the slowest current is on the inside. Because the water on the outside of the curve is moving fast, it can pick up and carry sediment, and it erodes the riverbank on that side, resulting in a cut bank. Because the water on the inside of the curve is slowed, it drops the sediment it is carrying. This deposition results in a point bar. (B) Shows real-life examples of a point bar and cut bank. What implications do

the dynamics of water flow and sediment deposition have for what might happen to a dinosaur that falls in a fast-moving river? Where in the river might it be deposited? (A adapted from Helgi, https​://uk​.wiki​pedia​ .org/​wiki/​%D0%A​4%D0%​B0%D0​%B9%D​ 0%BB:Meanders.png; B courtesy of H. Steve and the US Fish and Wildlife Service.)

might belong to the same individual? Because you have taken some basic geology classes, you know that the type of rocks surrounding your bone indicates a stream channel, and from grain size and other characteristics, you can estimate flow direction and energy. Using this knowledge, you can follow the channel sediments in the direction that would have been “upstream”, and look for the same rock layer as the one in which you found the first bone. As you can see, understanding the patterns of transport in modern systems is critical to your quest to find the rest of the skeleton!

11.3.5 Trampling and Weathering Beyond being chewed on and moved around, there are a wide variety of ways biological and environmental factors can affect a bone before burial. Bones and skeletons scattered on the ground can be trampled on by other animals, leaving characteristic striations on the bone. When bones are exposed on the ground surface for a long time before burial, they are also subjected to weathering by wind, rain, sun, and heat (or cold), and the length of time they lie out in a given environment can generate different and distinct patterns of weathering. For example, bone laying on a surface that is exposed to the sun and wind can result in deep cracks (Figure 11.12A) that eventually break the bone into smaller pieces that are more easily carried away. Even plants can modify bones, because growing roots can penetrate or even move and break apart bones, and the acids produced by plant roots or in soil itself can act to demineralize and dissolve bone surfaces (Figure 11.12B). Likewise, if a bone has passed through the digestive tract of an animal, the acids work to alter the surface of the bone. Finally, the action of microbes, including fungi, either in the soil, or as part of the decay process, can also alter the bone in characteristic ways, resulting in most cases in complete dissolution. All of these processes contribute to disarticulation, rounding of surfaces, and loss of information

Figure 11.12  Markings observed on the bones of a woolly mammoth (Mammuthus primigenius) discovered in Poland that have been interpreted as (A) cracking from weathering and (B) root etching. Scale bars

represent 5 mm. (Courtesy of B. Kufel from A. Krzemińska, K. Stefaniak, J. Zych, P. Wojtal, G. Skrzypek, A. Mikołajczyk A. Wiśniewski. (2010). A Late Pleistocene woolly mammoth from Lower Silesia, SW Poland. Acta Zoologica Cracoviensia— Series A: Vertebrata. 53. 51–64. 10.3409/ azc.53a_1-2.51-64.)

11.4  Dirt to Display: Diagenesis

about the bones, including muscle scars and the shape of bone surfaces at joints. These can affect our interpretations of biomechanics (how the animal moved) as well as community interactions.

11.4 DIRT TO DISPLAY: DIAGENESIS After reading this section you should be able to… • Describe basic diagenetic factors, and explain how they might impact the preservation of a dinosaur.

As soon as organic material is fully buried, biostratinomic processes are arrested or greatly reduced. At that point, diagenetic processes take over the fossilization pathway. Like biostratinomy, these processes result in taphonomic loss and alteration from the original structure and composition of the tissues. Below, we discuss some diagenetic factors, and how they affect the fossilization process.

11.4.1 Speed of Burial The sooner an organism is buried after death, the earlier biostratinomic processes are slowed or restricted, and the less taphonomic loss they cause. Thus, for paleontologists, the sooner something was buried after death, the more we can learn, because it is more likely to carry information about the organism into the fossil record. For example, if an animal is completely buried soon after death and before its soft tissues have rotted away, the more likely it is to remain articulated, shedding light on the actual structure, morphology, and biomechanics of the animal as a whole.

11.4.2 Ground and Pore Waters The amount, acidity, and mineral content of ground and pore waters can profoundly affect the preservation of a fossil. The mineral comprising bone and teeth is hydroxyapatite, and it will dissolve in acidic environments. Therefore, bones that lie in water, or which are buried in sediments that have groundwater with a pH below seven moving through them, will likely dissolve before they can become fossils. The mineral content of that water is also important; bone has many small pores that get bigger as acidic waters slowly dissolve them. However, if the water that moves through the bone is saturated with minerals, those minerals will precipitate in porous bone in a process called permineralization (Figure 11.13), contributing to increased density and thus increased resistance to breakdown. This process can be facilitated in the presence of microbes that may make the pH of the bone, or the groundwater, more favorable to precipitation. When people think about fossils, many say that the bones have been “turned into rock”. This is not fully accurate, because in most cases the bone tissues remain, maintaining original microstructure and mineral type, but the precipitation of mineral in the pore spaces can change the look and feel of the bone into something more similar to rock than the fresh bone we’re familiar with.

11.4.3 Type of Sediment The type of sediment surrounding a dead organism also plays a role in its fossilization. As you probably know from walking in muddy terrains, muds can be easily compressed, and this can cause distortion of the bones/fossils encased in muds as well. A fine-grained, well-sorted sandstone is good for preserving the detail of things like muscle scars on the bone, and preserving the overall shape of the bones. Conversely,

265

266

CHAPTER 11    How Do We Know How Dinosaurs Became Part of the Fossil Record?

Figure 11.13  Schematic of the process of permineralization acting on a bone buried in sediment. As water

moves through the overlying sediments, it dissolves minerals. It then precipitates those minerals within the bone matrix, in small pores where organic structures used to reside. This gives bone added resistance to degradation and provides information on the environmental conditions to which the bone has been subjected. (Fossil image courtesy of M. Schweitzer. Conglomerate adapted from image taken by Geolina163, https://commons.wikimedia.org/wiki/ File:Wiki​Proje​kt_La​ndstr​eiche​r_Geo​top_E​ istob​el_47​.jpg.​)

if a bone is deposited with sediment bearing large, gravel-sized grains, breakages will occur to the bone during transport and burial as they are smashed against these rocks. On the other end of the spectrum, clay sediments, which represent fine grains and low energy, can result in the preservation of things as delicate as eggshell, and sometimes even the impression of feathers, skin, or other soft tissues. But because clay grains are small, they can also distort the bony fossils they hold, causing it to alter its original proportions.

11.4.4 Microbial Activity Microbes participate in decay, which can cause taphonomic loss. If you recall from Chapter 6, all bone is a composite material, made of both organics and mineral. Microbes contribute greatly to bone destruction most of the time, because they can produce an acidic “slime” that causes bone mineral to dissolve, liberating non-mineralized tissues like collagen, blood vessels, and cells for microbes to access. They can also produce enzymes that break down the collagen and other organics as well. But in some cases, the bacteria and the slime they secrete are chemically reactive, with a strong negative charge, and in the right environmental conditions, they can actually trigger the deposition of positively charged minerals on the surface of organic substances before they degrade. This not only arrests the ability of the microbes to produce acidic slime and degrading enzymes, but adds protection to the bone through this layer of minerals. In fact, this layer can act as a seal, preventing outside influences from acting on the bone, and again, adding to the stability of the organism over time. Because the effects of microbial activity can be so diverse, the specific details of the type, extent, and nature of microbial activity can lead to very different modes of fossilization.

11.4.5 Amount of Oxygen Oxidation causes the destruction of many molecular components of an organism, while reducing conditions usually promote preservation. The more rapid and deep the burial, the less oxygen is available for organisms of decay to use and for chemical reactions that result in the destruction of bone components, like proteins and cells.

11.5  Different Types of Fossils

11.4.6 Burial Environment and Conditions Which do you think is most likely to preserve organisms as fossils? A desert (aeolian environment)? A river channel (fluvial environment)? A lake (lacustrine environment)? An ocean (marine environment)? Within marine environments, which do you think are likely to yield the best fossils—a deep marine environment, or continental shelf? In addition to the amount of available oxygen, as discussed above, think about things like the energy of a system. Lake environments or deep ocean environments are usually lower in energy when compared with rivers or shore deposits; therefore, an organism is more likely to sink slowly to the bottom, remain articulated, and get buried without much disturbance. On the other hand, shoreface environments, with continual action of waves against the shore, or aeolian environments where winds can drive sand grains into remains, result in scouring and destruction, and do not usually favor good preservation. Low energy, low oxygen environments where organisms are likely to be rapidly buried by sediment load will usually result in the best preservation.

11.4.7 Organismal Factors Factors inherent to the organism may also facilitate preservation. For example, compare two ocean creatures, a starfish and a jellyfish. Which is more likely to preserve? Hard parts contribute greatly to the likelihood of preservation—thus, there is a taphonomic bias working against the preservation of animals composed solely of soft, labile tissues. This is why fossil shells are so (relatively) abundant, and extinct sharks, whose skeletons are made of cartilage and not bone, are generally known from only their teeth. If one does not understand this bias, it might lead to an incorrect supposition that only animals with shells and other hard parts lived in the past. What implications does this have for how we reconstruct past ecologies? Past food webs? An animal’s size might also affect its preservation potential. As a general rule, big, dense bones are more durable than tiny hollow bones, like those of birds, so they may be less likely to be destroyed by processes like trampling or transport. However, on the other hand, tiny bird bones are easier to bury rapidly, whereas gigantic femora, like those from a giant sauropod, take a lot longer and a lot more sediment to cover. Think of a sparrow and an elephant. A sparrow’s bones are much less durable than the elephants, and more easily smashed apart. However, a dozen sparrows could be buried rapidly in an instant with much less sediment than it would take to cover even a small single elephant, leaving the elephant exposed longer, and thus subject to more biostratinomic processes. Thus, size is a tradeoff, and its effect on preservation will depend on other circumstances. Remember though, that all taphonomic processes result in a loss of information about the animal you are studying. Based upon that and the above discussion, it becomes apparent that finding any fossil is a rare event. Finding a dinosaur or other large vertebrate fully articulated as in life is even rarer. It happens, but not often. Paleontology rests on interpretations of what we do find, and often we don’t have much to go on. Understanding the present world, and the life we can observe, is critical to understanding the past, and life we will never see.

11.5 DIFFERENT TYPES OF FOSSILS After reading this section you should be able to… • Define the two broad fossil categories. • Describe the different types of fossils.

267

268

CHAPTER 11    How Do We Know How Dinosaurs Became Part of the Fossil Record?

• Summarize the five types of altered fossilization.

Now that we’ve come this far into how something becomes a fossil, it’s time to talk a little more specifically about what “counts” as a fossil. Fossils aren’t just limited to bones, but can include footprints, skin, egg/ eggshell, and plants—and that’s only for starters. The simplest definition of a fossil is: “Any evidence of past life”. This can include leaf impressions, microbial colonies, bones and teeth, skin and feathers, eggshell, tracks and footprints, boreholes and tracks left by invertebrates, burrows from insects that backfill and are preserved, or even chemical fingerprints that are unique to life processes. We generally put fossils into two broad categories: • Body fossils: Remains that were once part of an organism’s body. These include bones, teeth, skull, claw sheaths, or internal parts like intestines (if they preserve). • Trace fossils: Remains that were made or left behind by an organism, but were not themselves part of the organism’s body. These include footprints and trackways, boring traces, burrows, gastroliths (stomach stones), coprolites (fossilized feces), nests, and eggs or eggshells. Body fossils can reveal a great deal about the paleobiology of an organism, as well as evolutionary trends experienced by its lineage. Trace fossils, on the other hand, can shed light on paleoenvironments organisms experienced (e.g., substrates in which footprints were made can tell if they were swampy or arid, muddy or sandy); behavior and paleoecology (e.g., discerning whether an animal was walking or running, whether it dragged its tail or walked more upright); or paleoecological interactions (e.g., borings in fossil wood indicate insect interactions, or tunnels into coprolites can indicate the presence of dung beetles). There are a wide variety of ways that fossils might enter the rock record. For the rest of this section, we’ll go over some of the most common types.

11.5.1 Unaltered Fossils “Unaltered” doesn’t mean these fossils are totally unaltered from their living state, but rather that they still contain many original characteristics of the living organism. Examples include mammoth remains Figure 11.14  A rare, mummified young mammoth, recovered from permafrost deposits in Siberia. Soft

tissues including the skin, trunk, and stomach contents are preserved virtually intact. Fossils like this are sometimes referred to as “unaltered”, although clearly all fossil organisms are altered from the living state to one degree or another. (Courtesy of Ben2, https://commons. wikimedia.org/wiki/File:Jeune_mammouth_ IRSNB.JPG.)

11.5  Different Types of Fossils

269

preserved in permafrost that retain hair, guts, and other components (Figure 11.14), animals preserved in tar pits or deserts that essentially mummify them, or insects preserved in amber. The rest of the fossil types we talk about in this section are considered altered, and it is how they are altered that they are defined and differentiated.

11.5.2 Impression Fossils Impression fossils are patterns in the sediment that retain features of the organism, but not the actual organism or any of its parts, making them a type of trace fossil. A good example of impression fossils are preserved footprints (Chapter 16). When making footprints, no part of the foot remains within the print, and yet, a perfect, three-dimensional shape of the foot is left behind. If you were to cut through an impression fossil from top to bottom, you would see sediment grains throughout, but no preserved tissue. Beyond just footprints, we can find many impressions in the fossil record from places where dinosaurs sat, leaned, or rested, which leaves good evidence of their scale patterns on different parts of the body (Figure 11.15).

11.5.3 Carbon Films/Compression Fossils Carbon films, or compression fossils, occur when the original organics of an organism have been highly compressed and (usually) heated. All that remains is a very thin film of carbon, derived from the carbon in proteins and other components of the original tissue (Figure 11.16). It often results in preservation of labile components, like skin, hair, or feathers, that don’t usually preserve. In fact, carbon films are the most common Figure 11.15  Skin impression found in association with the hadrosaur specimen known as “Dakota”. The

regularity of the scale patterns reflects the original pattern of the dinosaur skin. (Adapted from Kabacchi, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=10​ 83459​3.)

Figure 11.16  Plants and insects are often preserved as carbon films or compression fossils. They differ visually

from impression fossils because they exhibit different colors than the surrounding sediment. Though flattened, compression fossils can preserve great detail. This dragonfly fossil (Cordulagomphus) (A) shows the pattern of veins in the wing, and structural fibers can be seen in the petals of this fossil flower (Chaneya tenuis) (B). (A courtesy of T. Tude, https://commons. wikimedia.org/wiki/File:Cordulagomphus_ fossil.JPG; B courtesy of National Park Service, https​://ww​w.nps​.gov/​fobu/​learn​/ natu​re/im​ages/​chane​ya.gi​f.)

270

CHAPTER 11    How Do We Know How Dinosaurs Became Part of the Fossil Record?

way that feathers are preserved. Compression fossils, like impression fossils, are preserved in only two dimensions, but there is a contrast in color and texture from the surrounding sediments. Compression fossils can preserve features of extinct organisms in exquisite detail; delicate veination patterns in insect wings or plants and branching of feather barbs from the rachis have been observed in compression fossils.

11.5.4 Mold-and-Cast Fossils Mold-and-cast fossils are made when an organism, such as a mollusk, is buried in sediment. The sediment hardens around the organism, and then the organism subsequently dissolves, leaving the hardened sediment behind. That shell-shaped vacancy in the sediment is a mold (or mould). Nothing remains of the original organism, but its three-dimensional shape is retained with varying degrees of fidelity. Sometimes, this natural mold can later fill up with mineral precipitate, and that mineral in-fill takes on the shape of the original organism. However, this is only a mineral cast of the organism, as no actual piece of the organism is left behind. Although this mode of preservation is more common for shell fossils, like ammonites or clams (Figure 11.17), other parts can be preserved this way, including (rarely) small bones. It is thought that fossils that retain parts of digestive tracts, like those preserved in the little Italian dinosaur Scipionyx, might be preserved as a natural cast.

11.5.5 Permineralization Sometimes, the original mineral “scaffolding” of a bone remains, but where there were once pores, cells, or blood vessels, those spaces become filled with mineral from external sources, which has precipitated from saturated waters moving through the bone. This mode, called permineralization, is the most common way dinosaur remains are preserved, and also produces “petrified” wood. Permineralization results in the retention of three-dimensional morphology, surface patterns, size, internal structures of original hard parts, hard part mineralogy, and usually, original microstructural patterns (Figure 11.18). Bone usually permineralizes with a carbonate mineral, but wood and plants are infiltrated with a silicate bearing mineral.

11.5.6 Recrystallization

Figure 11.17  These ammonites illustrate different modes of fossilization. (A) An ammonite mold. The

original tissues have degraded, leaving a mold that retains the inverse (or “negative”) of the original three-dimensional shape of the organism. (B) An ammonite cast. Sediment has infilled a mold similar to the one shown in A, replicating the threedimensional shape of the original organism. (C) A permineralized ammonite. Notice the difference in texture and color between this fossil and the mold and cast, which are the same in color and texture as the sediments that form them. The permineralized form retains much more of the original information in comparison. (C courtesy of Pexel, https​://ww​w.pex​els.c​om/ph​oto/a​ mmoni​te-ce​phalo​pod-f​ossil​-mine​raliz​ed-16​ 08606​/.)

In recrystallization, the minerals that are present in mineralized tissues (e.g., bones, shells) undergo changes to their crystal structure. Recrystallization can sometimes be hard to recognize at first glance, because the mineralogy of the original hard parts remains the same. For example, the aragonite in mollusk shells has the same chemical formula as the carbonate that results from recrystallization (CaCO3). However, the geologically altered carbonate often forms larger crystals. When larger crystals replace the original ones, much fine detail can be lost (Figure 11.19).

11.5  Different Types of Fossils

271

Figure 11.18  Permineralization of (A) fossil wood and (B) dinosaur bone. In

both cases, mineral has been carried in on pore waters and deposited in the spaces of porous organic structures. Note that the original structure is still easy to see; layers of woody tissue (i.e., tree rings) in the tree and primary and secondary osteons in the bone. Even at the microscopic level, permineralized fossils retain some scaffolding of the original tissue (e.g., mineral and/or organics). (A courtesy of Retallack, https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=48​04458​3; B courtesy of E. Schroeter.)

Figure 11.19  Comparison of ammonite shells. In (A), the shell and its

open spaces have been permineralized with exogenous mineral. The shell itself and its chambers can be observed in fine detail. In (B), the ammonite fossil has undergone recrystallization. The newly formed crystals are so large they have obliterated much of the fine detail of the original shell, leaving only the spiral and indication that this was originally an ammonite. (Courtesy of E. Schroeter.)

11.5.7 Replacement Finally, the original minerals that made up the hard parts of the organism in life can be totally replaced by a different mineral. When this replacement occurs, the original material and microstructure of the tissue are lost. Bone is not normally replaced, but rather permineralized, as described above. However, in rare cases, bones can be buried in environments that are saturated with silicate minerals. Silicates precipitate in slightly acidic environments, but bone mineral (hydroxyapatite) is basic. Thus, the overall shape of the bone can be retained, but the microstructure is lost. In bone, this can result in opalization—the replacement of carbonate-bearing minerals with opal silicates (Figure 11.20). At an even finer scale, functional groups that are part of the original mineral can be replaced with other parts. For example, bone and teeth are comprised of the calcium phosphate mineral hydroxyapatite, which has a chemical formula of Ca10(PO4)6 (OH)2. In life, some portion of the OH groups is substituted with CO3 or F2. But most of these functional groups in bone can be replaced, changing bone composition to increases in Si, U, Mg, Mn, or Fe. The three-dimensional shape of the bone stays the same, but the composition changes. In fact, you don’t have to be a fossil for this to happen. If you live in an area with fluoridated water, many of the OH groups in your bone have been replaced with F, because it is more stable. Thus, the type and degree of replacement in fossils can inform on certain aspects of the environmental effects to which it was exposed over time.

272

CHAPTER 11    How Do We Know How Dinosaurs Became Part of the Fossil Record?

Figure 11.20  This plesiosaur vertebra, like all vertebrate bone, was comprised of collagen (and other bone proteins) and the mineral hydroxyapatite in life. After its death

and burial, the geochemical environment the bone was encased in favored the dissolution of the original hydroxyapatite, and its replacement with another mineral— opal, which is essentially quartz with water inclusions. (Courtesy of J. St. John, https:// commons.wikimedia.org/wiki/File:Opal​ized_​ fossi​l_ple​siosa​ur_ve​rtebr​a_(Au​stral​ia).j​pg.)

Commonly, fossils can undergo three types of replacement. Silicification occurs when the apatite mineral in bone (or aragonite in some invertebrate shells) that was original to the fossil is replaced with silica. Pyritization occurs when calcite, or sometimes soft tissues, are replaced with pyrite minerals. Phosphatization may occur when phosphate minerals invade and deposit upon soft tissues, a very rapid process resulting in exceptional preservation. This process is so rapid, in fact, that the phosphatization is referred to as “the Medusa effect”, because it can happen before an organism is completely dead. Another type of phosphatization occurs when a low phosphate mineral is replaced by one containing higher concentrations of phosphate. This process can tell us a lot about the depositional environment. Pyrite, for example, forms in reducing environments with abundant iron and sulfur, while silicification requires a lower pH than carbonate. And, while replacement or recrystallization results in the preservation of the three-dimensional shape, surface information, and of course overall size, all the original microstructure is lost.

11.6 A CASE STUDY After reading this section you should be able to… • Discuss how some findings may change how we think about fossilization.

Recently, we discovered something that shows, despite all the studies on different aspects of taphonomy, there’s still a lot we really don’t understand how once-living organisms, including dinosaurs, enter the rock record. As discussed throughout this chapter, we’ve thought it happens as shown in Figure 11.21: • A dinosaur happens to die in an environment where it can be buried rapidly, before biostratinomic processes like bloat, scavenging, or disarticulation could occur.

11.6  A Case Study Figure 11.21  Common understanding of the fossilization process is illustrated here. A dinosaur dies in an

• Their skin, muscles, and other tissues are covered with sediment and decay slowly. • The small vessels and cells in bone degrade, leaving empty spaces, and all proteins and other organics are lost. • Sediment continues to accumulate, and water moves through the tiny pore spaces of the bones. The water carries minerals that are re-deposited in the pore spaces left by the degraded organics, turning the bone into “rock”. • Geological processes of erosion and uplift remove those sediments, revealing the altered bone. But is this always the case? What if fossilization doesn’t always progress in exactly this way? This typical framework for fossilization doesn’t seem to have been the case for one particularly well-preserved Tyrannosaurus rex. As mentioned previously in Chapter 6 (Bones and Anatomy), bone is a composite of hard minerals for strength, and organics (e.g., collagen and other proteins, vessels, cells) for flexibility. To study modern bone at high resolution, it is often necessary to remove some of the minerals, which can visually obscure the microstructure of other components within the bone. Theoretically, if the fossilization process outlined above were complete, there should be no organics left in dinosaur bones, only mineral. Thus, dissolving the mineral of fossil bone as we do to study modern bone should leave nothing behind, so paleontologists frown on this practice. When preparing the bones of this T. rex, scientists noted an unusual bony tissue lining the medullary cavities of the long bones of this animal. This tissue resembled a bony reproductive tissue, found only in living birds. Because of the close relationship between birds and dinosaurs, scientists had predicted that dinosaurs might have this unique tissue as well, but this was the first time a likely candidate had been seen. To test the idea that this was indeed dinosaur reproductive tissue, they took small pieces of the fossil and placed them in a mild acid solution, as is done to study medullary bone in birds. The scientists expected the acid etching to reveal the orientation of the minerals around where collagen fibers used to be. However, much to the surprise of the observers, when the mineral was dissolved, a pliable, stretchy material still remained! Looking closely at other pieces of bone, small transparent branching tubes, hollow inside except for small round red particles (Figure 11.22) were seen to emerge from the dissolving bone. These looked very much like blood vessels contained within the dense cortical regions of modern bone.

environment where some, or all, aspects of predation, scavenging, and degradation have been slowed or arrested. Then, the dinosaur is buried rapidly so that its body parts remain articulated. Sediments accumulate on top of the dinosaur, and when water passes through these sediments, soluble minerals are carried into and deposited on the porous dinosaur bones, filling in any spaces left behind by degradation of collagen and/or blood vessels with minerals. Geological processes such as uplift, mountain building, and erosion result in the exposure of some of the buried bone, and then paleontologists trace the bone remnants back to the layer where the rest of the dinosaur is buried. (Courtesy of X. Murelaga and E. Fundazioa (https://commons.wikimedia.org/wiki/ File:Fossilization_process.jpg.)

273

274

CHAPTER 11    How Do We Know How Dinosaurs Became Part of the Fossil Record?

Figure 11.22  Dinosaur cortical bone after being placed in a solution to dissolve the minerals. After a few days,

microscopic, transparent, flexible, hollow, and branching structures (arrow) began to emerge. These are both morphologically and chemically consistent with blood vessels! Scale bar represents 5 mm. (Courtesy of M. Schweitzer.)

After 65 million years in the ground, the fact that these materials looked like blood vessels was not enough to conclude they actually were. Remember from Chapter 1 that real science investigates all other possibilities, and in this case, plant fibers and bacterial products had to be eliminated as a source for these structures. So, chemical tests were conducted, and the results showed that their composition was more similar to vertebrate tissues than any other alternative. This was not expected, or even thought possible, given what we thought we knew about bone taphonomy! Clearly, there is still a lot about taphonomic processes that we have yet to understand. Since this discovery, many more exceptionally preserved materials have been found with dinosaurs, and such finds are changing what we think about fossilization processes. This type of preservation is not accounted for by current theories of how organisms transition to the rock record, but through detailed chemical analyses and carefully designed taphonomic experiments, we are beginning to understand conditions where this type of preservation might occur. We have a lot more to learn about how organisms become fossils, and in the process of understanding this, we can learn a lot about the chemistry of ancient environments, the microbes and other creatures that inhabited the world of the dinosaurs, the biology of the dinosaurs, and maybe even about the biological and chemical conditions that affect life on this planet today.

11.7 WHAT WE DON’T KNOW 11.7.1 How Do Features Like Dinosaur Skin and Feathers Preserve and Become Part of the Fossil Record? Soft tissues like skin can be preserved with dinosaurs, but how it preserves is not well understood. We don’t know for sure if different burial environments affect preservation differently. Skin can preserve as impressions, compressions, mold and cast, or as permineralized remains. We also don’t know how long various tissue types might survive in dinosaur remains. In living animals, muscle usually rots before skin, and mammal skin generally rots faster than reptile skin. Questions to consider: • Is skin more likely to preserve under some conditions, while feathers might preserve better under others? How would you test this idea?

11.7  What We Don’t Know

275

• Are any chemical remnants of the original material left in preserved skin or feathers, and if so, how can we best interpret them? • Why are the most preserved skin specimens from hadrosaurs? Was their skin thicker or unique in some way from other dinosaurs?

INSTITUTIONAL RESOURCES How Bones Fossilize…or Don’t from the National Museum of Natural History: https​: //na​tural​histo ​r y.si​.edu/​e duca​tion/ ​teach​ing-r​e sour​ces/p​aleon​tolog ​y /how​ -bone​s-fos​siliz​e -or-​dont Tar Noir: Paleoforensics at the La Brea Tar Pits: https://youtu.be/0tgVXTNiQOM

LITERATURE Behrensmeyer, Anna K. (1978). Taphonomic and ecologic information from bone weathering. Paleobiology, 4(2), 150–162. JSTOR. www.jstor.org/stable/2400283. Accessed 21 Feb. 2020. Davis, M. (2012). Census of dinosaur skin reveals lithology may not be the most important factor in increased preservation of hadrosaurid skin. Acta Palaeontologica Polonica, 59(3), 601–605.

Kobayashi, Y., Nishimura, T., Takasaki, R., Chiba, K., Fiorillo, A. R., Tanaka, K., Chinzorig, T., Sato, T., and Sakurai, K. (2019). A new hadrosaurine (Dinosauria: Hadrosauridae) from the marine deposits of the late cretaceous hakobuchi formation, Yezo Group, Japan. Scientific Reports, 9(1), 1–14.

12 HOW DO WE INTERPRET THE ECOLOGY OF DINOSAURS?

12

THE RELATIONSHIP OF DINOSAURS TO THEIR PHYSICAL AND BIOLOGICAL ENVIRONMENTS

N

o animal can be completely separated from the influences of its environment, and the same is true of dinosaurs. But how can we understand the environment of animals that are long extinct—and that lived in habitats long gone—from our perspective 65 million years in the future (Figure 12.1)? And what can we learn about today’s world by studying dinosaur environments?

12.1 WHAT IS ECOLOGY? After reading this section, you should be able to… • Define ecology. • Define paleoecology and give examples of features that comprise the physical and biological environment.

Ecology is, simply put, all interactions between an organism and its environment. At their core, “ecological interactions” can be reduced to just two things: what an organism has to do to eat and what an organism has to do to reproduce. These two factors are the primary driving force behind all ecological interactions—and, subsequently, evolutionary change as well. Paleoecology, then, is the science of reconstructing ecological dynamics of extinct organisms in their ancient environments. However, just like there is taphonomic loss of information during the transition from a living animal to a fossil (Chapter 11), there is also information loss that affects how we interpret ancient environments, and that must be accounted for when building our hypotheses.

IN THIS CHAPTER . . . 12.1 WHAT IS ECOLOGY? 12.2 THE GEOSPHERE: PHYSICAL ENVIRONMENT 12.3 THE BIOSPHERE: BIOLOGICAL ENVIRONMENT 12.4 AN ECOLOGICAL CASE STUDY: TYRANNOSAURUS REX 12.5 WHAT WE DON’T KNOW

278

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

Figure 12.1  This is a reconstruction of the ecosystem preserved in the Dinosaur Park Formation (Alberta, Canada). How can we make such a

hypothesis about environments that existed 65 million years (or more) in the past? (Courtesy of J.T. Csotonyi, https://commons. wikimedia.org/wiki/File:Dinosaur_park_ formation_fauna.png.)

“The environment” can be broken down into two components: • The physical environment: All the physical/abiotic factors that comprise the environment. These include things like temperature, climate, water chemistries, the amount of light to which an organism has access, relative humidity, and the substrate with which it interacts. • The biological environment: All the biological/biotic factors that comprise the environment. This includes everything from plants to microorganisms, members of the organism’s own species, and members of other species that live in the same area. In order to interpret dinosaur biology, we study the biomechanics, histology, and morphology of living organisms, and to interpret past conditions on Earth, we study the geology, hydrology, and geochemistry of modern Earth systems. Similarly, to interpret data from the fossil and rock records in an environmental context, we can study modern ecologies (Figure 12.2.).

Figure 12.2  This fossil comes from the Green River Formation in Wyoming.

What can you infer about the physical and biological environments of the Green River Formation by looking at this fossil? (Courtesy of J. St. John, https://flic.kr/p/ pEe9hL.)

12.2  The Geosphere: Physical Environment

12.2 THE GEOSPHERE: PHYSICAL ENVIRONMENT After reading this section, you should be able to… • Describe the physical parameters of the environment, and discuss the effects they may have on the biological environment. • Describe proxies that can be used to reconstruct ancient physical environments.

An organism’s physical environment is the sum of a great number and variety of conditions. Each of these, from the amount of sunlight to the availability of water, affects the ability of an organism, or a population, to thrive. When their physical environments undergo significant changes, populations too must adapt, or perish. Many physical parameters act together to shape a given environment. Here we briefly discuss a few of them that are important to think about when trying to reconstruct ancient environments. We will also look at examples of how these factors shaped ecosystems and the organisms that inhabit them.

12.2.1 Temperature The temperature of a terrestrial environment can vary with the season, with latitude from the equator, and even with the time of day—desert environments, for example, can go from very hot to very cold with the setting of the sun. Whether an environment is hot, cold, or temperate can have evolutionary implications regarding animal physiologies. • Effect: Animals that live in warmer climates are generally smaller than animals that live in colder ones, even if they are members of the same species or genus. This is because an organism’s ability to retain or lose heat is determined in part by its surface area to volume ratio. In very large animals, heat is retained because this ratio is small. The smaller the animal, the more easily heat is lost. In colder climates, heat must be retained, and this is favored by an increase in overall size, a concept known as Bergmann’s Rule (in general, body size increases with latitude).

12.2.2 Oxygen The amount of oxygen in an environment can vary greatly in aquatic environments with depth, salinity, currents, and temperature, but terrestrial environments can also vary in oxygen levels. For example, oxygen is low in subterranean burrows and at different heights of elevation above sea level (e.g., at the beach vs. the at the top of Mt. Everest). However, it is also important to remember that the overall level of oxygen in the atmosphere has itself changed dramatically throughout Earth’s history, and so must be considered when reconstructing an ancient environment. Researchers estimate that the percentage of oxygen in early Mesozoic atmospheres may have been lower than today’s levels. • Effect: Levels of oxygen in the atmosphere have an effect on the metabolism and activities of animals. Although oxygen hasn’t fluctuated in our lifetimes significantly, researchers posit that high oxygen levels in the Carboniferous may have favored the origin of flight in the huge flying insects of that time. How might correspondingly lower levels have influenced dinosaur ­evolution?

279

280

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

12.2.3 Light In terrestrial environments, the amount of light that an organism’s environment does (or does not) receive can be affected by the season, the climate, or even extremely localized factors like the thickness of the tree canopy. It can also be affected by the latitude of the landmass on which an organism lives. Regions above the arctic circle or below the Antarctic circle experience periods of constant darkness or constant sunlight each year—and would have in the Mesozoic as well. • Effect: The broad effect of increased or decreased light is most obviously reflected in the type of plants that can grow in different regions. So, even though global temperatures were warmer throughout the Mesozoic, light levels at the poles and in northern regions would still be significantly less during certain times of the year, influencing herbivore populations, migratory patterns, and the size of populations that could be maintained.

12.2.4 Substrate Substrate refers to the surface or material with which an organism interacts during life. For example, some types of plants thrive in hard, rocky soils, while others are adapted to soft muds or sand bars. While it is tempting to think that substrate is more important to plants or invertebrates than vertebrates, the rock-climbing ability of mountain goats and the sand-friendly feet of camels (Figure 12.3) show how substrate can drive evolution in vertebrate populations. • Effect: Certainly, the type of plants living on different substrates will have a direct effect on the characteristics of the animals that eat them, as was noted by Darwin in his study on island finches and their beaks.

12.2.5 Precipitation/Water The amount of freshwater in an environment, and the way it moves through that environment, can vary greatly, from ever-wet rainforests to the driest deserts—both hot deserts, where all the water evaporates, and cold deserts, where all the water freezes. • Effect: The availability of liquid water in an environment, as well as the humidity or aridity of a region, can also have profound effects on an area’s geology, climate, substrate, and plant life. Very

Figure 12.3  The feet of a mountain goat (A) are adapted to climbing. Conversely, the feet of a camel (B) are flexible enough to grip sandy surfaces. We can use such morphological

features of vertebrate organisms to inform on the ecological niche they inhabit. (B courtesy of 3268zauber, https://commons. wikimedia.org/wiki/File:Vorderfu%C3%9F_ eines_Trampeltiers.JPG.)

12.2  The Geosphere: Physical Environment

different life forms occupy the Gobi Desert, as compared with the swamps of South Florida. These are just a few of the physical factors that both characterize and constrain modern-day environments. But how can we reconstruct them for environments that existed hundreds of millions of years ago? We cannot measure these parameters directly, so we must rely on ecological proxies.

12.2.6 Proxies for Physical Parameters of Ancient Environments As we’ve seen in previous chapters, the rock record retains the marks of many abiotic and biotic forces. We can look to both for clues on the physical conditions that prevailed in the past.

12.2.6.1 Depositional Environments At grand scales, rock layers themselves will indicate the depositional environment that was present when the sediment was being laid down (Chapter 2). Very fine-grained sediments (e.g., clay and silt) that form very thin layers, or laminations, may correlate to low energy environments such as lake bottoms, very slow-moving streams, or flood plains. On the other hand, larger-grained, well-sorted, cross-bedded sandstone results from sand moved by faster currents, or blown by wind in a desert, depending on scale.

12.2.6.2 Paleosols Although rocks can indicate the type of environment, more accurate reconstructions of conditions in those environments can be created by studying paleosols, ancient soils that have been preserved in the rock record. Paleosols can shed light on past environments, and, as in most things paleo, we understand these by comparing them with characteristics of soils formed in a variety of modern environments. Climate proxies that are found in paleosols include the following, some of which are relatively new to reconstructing paleoenvironments: • Shrink-swell features: Features preserved in paleosols, like wedgeshaped structures and desiccation cracks, can inform us about the presence and intensity of seasonal precipitation. Wedges and desiccation cracks form during dry seasons when soil dries out and contracts, and features called slickensides can form during wet seasons when clay mineral expands and moves past each other. • Stable isotopes: As we saw in Chapter 2, elements can vary in the number of neutrons they contain in their atomic nuclei, and hence, their atomic mass. These variants are called isotopes. The ratio of light (12C) versus heavy (13C) carbon can shed light on the types of plants that were present, and in turn, environments they occupied. Similarly, water temperatures can be estimated by measuring the ratio of “heavy” oxygen (18O) to the much more common “light” oxygen (16O) isotope in fossils or marine sediments. • Magnetism: Magnetic minerals form naturally in soils. By studying present-day environments, we know that the amount of certain magnetic minerals found in the soil is dependent on the amount of water available as these minerals form when iron or iron oxides react with water. Measuring the ratio of magnetic minerals like goethite and hematite can provide clues to the relative amount of precipitation that may have been present in past environments since more soil water results in a higher proportion of goethite. Just like we can use abiotic components of the rock record to inform us about paleoecology, remnants of once-living organisms can contribute

281

282

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

to our understanding of ancient physical environmental factors as well. Although these fossils themselves constitute part of the “biological environment”, because of the close relationship between organisms and the environment, we can glean information about past climates and ecosystems studying the animals that lived in them.

12.2.6.3 Pollen Palynology is the study of fossil pollen and spores. These can preserve quite well in some environments, and these grains are unique to each plant type from which they derive. When the size and shape of fossil pollen grains are compared with those known from living taxa, the presence of certain plants, or at least plant types, can be inferred from pollen preserved in sediments. Knowing what plants lived in an area gives a strong indication of what the climate, substrate, temperatures, and humidity values were.

12.2.6.4 Phytoliths These are small silica minerals that form inside plant tissues (Figure 12.4). When the plant dies, these phytoliths (phyto = plant, lith = stones) can remain part of the soil and sediment even after the plant decomposes. Different families of plants produce different shaped phytoliths, and these microscopic fossils can provide information about the types of plants that existed and characterized the environment. In more recent sediments, phytoliths have contributed to our understanding of the timing and evolution of true grasses, documenting long-term or short-term vegetation (and hence, climate) change, plant-animal co-evolution patterns, and inform us of the diets of extinct animals! The amount and intensity of sunlight can affect cell size and shape, and this in turn is reflected in phytoliths, allowing them to serve as a proxy for the amount of sunlight an area received!

12.2.6.5 Plant Fossils Microscopic features of plants (pollen and phytoliths) preserve in the rock record, but sometimes, the macroscopic parts like leaves, trunks, and roots also survive (Figure 12.5). In most cases, fossil plants can be compared with living plants, and through modern ecological studies, we know that there are certain features of plants that are correlated with specific environmental conditions. Thus, we can make inferences about

Figure 12.4  This is a scanning electron micrograph (SEM) showing a phytolith. When silica is carried into

the plant tissues, it replicates the internal structures of the once-living plant in three dimensions. Phytoliths can be diagnostic to plant type, and so help inform our reconstructions of paleoenvironments. (Courtesy of B. Gadet, https://commons. wikimedia.org/wiki/File:Phyt​olith​es_ob​serv%​ C3%A9​s_au_​Micro​scope​_Elec​troni​que_%​ C3%A0​_Bala​yage_​01.jp​g.)

12.2  The Geosphere: Physical Environment

283

Figure 12.5  This massive tree trunk (left) was found in the Judith River Formation in Montana (USA), going back into the hill behind it. On the

ancient environments based upon the types of plants we observe in the rock record. In addition to the presence or absence of certain plant types, plant fossils also give us clues about environmental factors through specific features of their anatomy. For example, Figure 12.6 shows fossil leaves that are similar in overall shape, but have different margins. We know from measuring and observing plants in living ecosystems that smooth-margined leaves are more likely to be found in regions with high average temperatures. When we see these same features in ancient leaves, then, we can assume that temperatures were equivalent at least to those observed today with similar plants. If the majority of leaf fossils we find have serrated margins, the temperature of that region was likely to be relatively cooler. Data like these allow us to propose that although today northern states like Montana have cooler climates, in the past, it was likely much warmer than the present in these areas. Fossil plants are good indicators of past climate change!

right is a leaf from a deciduous angiosperm, or flowering plant. Angiosperms were relatively new to the scene, appearing for the first time worldwide about the time these sediments were laid down. Fossils like these can shed light on the type of trees (or other plants) that existed in the same environment as the dinosaurs preserved there. How do you think the diversification of angiosperms might have driven the evolution of the dinosaurs that fed off them? (see Chapter 15 Diets). (Courtesy of M. Schweitzer.)

Humidity, aridity, and paleo-atmospheric data can also be obtained through well-preserved fossil plants, and thus can validate conclusions drawn from other data, like isotope studies, on physical environments. There are three other important morphological features of plants that can allow us to estimate paleoecology and paleoclimate. In plants that live in present-day humid environments, the leaves often possess what is called a “drip tip”, so that water doesn’t accumulate on the leaf surface where destructive microbes can thrive, but instead is drained away. Fossil leaves with similar features can be used to infer a more humid environment than those preserving plants without them (Figure 12.7). At the opposite end of the spectrum, some plants show features that adapt them to arid environments. In very dry environments, plant leaves are often small, and covered in a wax-like material called a cuticle (Figure 12.8). The cuticle is waterproof and acts as a seal to hold water in the leaf and protect it from desiccation. The hydrophobic (“water-hat-

Figure 12.6  (A) This maple leaf has serrated, or “toothed” margins, indicating that it lived in a relatively temperate to cool region. Conversely, the sycamore leaf (B) has smooth margins, and probably came from warmer climates. (A courtesy of Daderot,

https://commons.wikimedia.org/wiki/ File:Acer​_subu​kurun​duens​e_(fo​ssil_​leaf)​ _-_Na​tiona​l_Mus​eum_o​f_Nat​ure_a​nd_Sc​ ience​,_Tok​yo_-_​DSC06​789.J​PG); B courtesy of Kevmin, https://commons.wikimedia.org/ wiki/File:Macginitiea_gracilis_01.jpg.)

284

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

Figure 12.7  (A) The narrow elongate tip on modern plants, or “drip tip”, is a way for them to shed excess water. This is important in wet or humid environments, as shedding water prevents the growth of destructive bacteria and fungi. Thus, when we see this same feature in fossil plants (such as in B), we can infer a relatively wet environment. (A courtesy of W. Djatmiko,

https://commons.wikimedia.org/wiki/ File:Scorod_borneen_20110125-11679_aip. JPG; B courtesy of M. Heaton, https​://ww​ w.fos​siler​a.com​/foss​ils/3​-8-un​ident​ified​-foss​ il-le​af-gl​endiv​e-mon​tana.)

Figure 12.8  In (A), the water-shedding ability of the waxy cuticle of a modern leaf is visible. The cuticle is punctuated by stoma, the organ of gas exchange in plant leaves. (B) Preserved cuticle in a fossil ginkgo leaf, also punctuated with stoma. (A

adapted from Tyanna, https://commons. wikimedia.org/wiki/File:Cuticle_of_leaf_ under_microscope.JPG; B adapted from J. Watson, S. J. Lydon, N. A. Harrison, https:// flic.kr/p/xeA8AP.)

ing”) property of cuticles makes it highly likely to preserve, and also increases the potential of the plant it surrounds to preserve. In fact, fossil leaves with thick cuticles may preserve in three dimensions, so that they can be sectioned, and their fine microstructure can be observed under the microscope for comparison with living plants.

Figure 12.9  Stoma visualized using electron microscopy on (A) a fresh leaf, and (B) a leaf of Ginkgo biloba harvested from Hortus Augustinus (Amsterdam, Netherlands) in 1929.

These SEM images show small openings (arrows) on the underside of leaves that provide a means of exchanging gasses with the environment. When a thick cuticle is present, these stoma puncture it so the plants can “breathe” without losing too much moisture. (A adapted from CNX OpenStax, https://commons.wikimedia. org/wiki/File:Figure_30_04_04abc.jpg; B courtesy of G. Retallack.)

In cases where fossil leaves are so well preserved that we can see them in three dimensions, not just as carbonized “films”, we can find even more informative features that compare directly with those found in living plants. The number and density of stoma (or stomata) (Figure 12.9), small pores through which gasses are exchanged into the leaf, are correlated with aridity as well as levels of atmospheric CO2. By calculating the density of stomata on fossil leaves, we can estimate how CO2 levels changed over time in a particular region. In fact, stomatal densities in fossil leaves have been used to support global climate change through geological time.

12.3  The Biosphere: Biological Environment

12.2.6.6 Fossil Invertebrates In addition to plants, fossilized insects and other invertebrates can shed light on both climate and other aspects of paleoenvironments. For example, beetles (Order Coleoptera) are very diverse, and also very sensitive to changes in temperature. Their lineage is also far older than dinosaurs, dating all the way back to the Carboniferous (~320 Mya), and their exoskeleton is resistant to degradation, allowing them to be preserved in the fossil record. Chitin, the major component of their hard shells, can also be analyzed for stable isotope values, which are direct indicators of paleotemperatures. Thus, because they are highly mobile, we can track changes in insect distribution over time in response to changing temperatures. Bivalves (e.g., mollusks or clams) also fossilize well. Their overall morphology and shell thickness can be used to determine if they lived in fresh, brackish, or marine waters, and thus they can inform us about environments of dinosaurs found nearby. In Montana’s Hell Creek formation, which is the home of Tyrannosaurus rex, there are many beds of freshwater clams in the same geographical area that contain dinosaurs, leading to the interpretation that there were freshwater streams and nearby shallow lakes in the T. rex’s environment. Some fish species are also restricted to certain environments; their distribution varying with water temperature, salinity, and depth of water. If we find their fossils close by, it tells us about the local environments, as well as giving us constraints on the age of the sediments. This is why it is vital to take a census of all fossils in the area of a dinosaur quarry, and not just focus on the dinosaur bones that are most obvious. The sediment and any minute fossil traces it contains will help to complete the picture of dinosaur biology. There are, then, a variety of abiotic and biotic proxies that we can use to estimate the climate parameters of an ancient physical environment. The types of fossils, rocks, geochemical signals, and data from preserved soils provide us very good data for making inferences about what the physical environments were like in the past, and how these changed over time. Remnants of fossil organisms, including invertebrates and plants, contribute greatly to our understanding of paleoenvironmental indicators as well. Comparing types of plants, stomatal size and densities, leaf morphology, and indicators of cuticles sheds light on ancient climates, and thus ecology. Knowing these things is important to dinosaurs because just like living animals today, dinosaurs shaped, and were shaped by, their local and global environments.

12.3 THE BIOSPHERE: BIOLOGICAL ENVIRONMENT After reading this section, you should be able to… • Correctly order the hierarchical levels of Earth’s biosphere. • Distinguish between a habitat and a niche and give examples of each. • Draw an example food web with labeled trophic levels. • Explain how niches don’t really change over time, but the organisms that fill them do.

When we consider the ecology of an organism, whether modern or ancient, we place it within a hierarchical framework. Ecological studies are ordered, from smallest (or narrowest), and most specific to placing

285

286

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

study organisms in an increasingly greater or more inclusive context. This hierarchy describes biological organisms in relation to other organisms, and to their environment, at various levels. Levels of ecological hierarchy, from narrowest to broadest, include: • Organism: A single individual (e.g., you, a bacterium, a dinosaur, your dog, etc.). This is the simplest, narrowest level, and certain features that contribute to an organism’s overall fitness are selected for and maintained across generations. • Population: A group of individuals of the same species (e.g., a pack of wolves, a herd of deer). Life doesn’t happen in a vacuum, and neither do evolutionary changes. A vertebrate organism, by itself, doesn’t reproduce—it takes two! Similarly, a single organism does not evolve. It is only when a trait is passed to succeeding generations that it becomes an evolutionary force. Populations, not individuals, have diversity and variation on which selection can act; thus, populations are the unit of evolutionary change. It is at the level of a population that determines if a trait is maintained or lost. • Community: All the organisms that interact with each other, across all species. A deer population acts upon trees and brush and the flowers in a garden, and are acted upon by wolves and coyotes and ticks and biting flies. All of these organisms, together, form a community. Our understanding of extinct communities is somewhat compromised by taphonomic loss (see below), but there is much that can be inferred from all fossils at all levels recovered from a single locality. • Ecosystem: Includes all the organisms that interact with each other in the context of their physical (or abiotic) environments. For example, a forest ecosystem might include pine trees, deciduous trees, brush and browse, ferns, snails, butterflies, deer, elk, coyotes, etc., in a closed system with reduced light and high seasonal moisture; or an artic ecosystem may include frigid temperatures, low humidity, icy substrate, large polar bears, and seals with abundant blubber. • Biome: Similar to an ecosystem, but describes these interactions on a much larger scale—such as that of an entire geographical area. A biome can be thought of as a grouping of ecosystems, and there can be many ecosystems within a single biome! For example, an aquatic biome can contain a kelp forest ecosystem and a coral ecosystem. An alpine biome can consist of both forest and tundra ecosystems, and each ecosystem contains different organisms. • Biosphere: The collective parts of the Earth where life is found. The biosphere is planet-wide and is the most inclusive, most all-encompassing level of ecological hierarchy. It even includes the subsurface of the earth, where worms or microbes exist, and the lower atmosphere, where pollen, spores, and bacteria live— anywhere on the planet that life exists. The relationships between these hierarchical rankings are summarized in Figure 12.10. Of course, these hierarchical rankings are not limited to the present. The evolution of ecosystems in the past is vital to predicting future environmental trends, and it is important to realize that ecosystems today are in a sense inherited from past interrelationships. An example can be seen in Figure 12.11, which represents an ecological reconstruction of Jurassic organisms.

12.3  The Biosphere: Biological Environment

287

Figure 12.10  Diagram of ecological relationships in perspective. The lion

(an individual organism) interacts with members of its own species (a population). The lion pride interacts with organisms of other species in the local environment (a community). These can be prey, other predators, plants, or even microbes. The communities live on substrates and respond to the physical environment (an ecosystem). Multiple ecosystems comprise large-scale biomes (not pictured), and all the organisms in all the biomes that operate on earth, wherever life is found, together form the biosphere. (Image credits are as follows: single lion courtesy of K. Pluck, https:// en.wikipedia.org/wiki/File:Lion_waiting_ in_Namibia.jpg; lion pride courtesy of GinaFranchi, https://commons.wikimedia. org/wiki/File:PZ_lion_pride.jpg; community courtesy of rcrhee, https://commons. wikimedia.org/wiki/File:A_lion_hunting.jpg; biosphere courtesy of NASA.)

Two other ecological concepts that are important to understand are habitat and niche. The habitat of an organism is its home—the surroundings in which it lives. It can be a forest canopy or a blade of grass, pond scum, or an open prairie. It would encompass the area an organism covers to attain food, find and select a mate, and reproduce. For example, the habitat of a squirrel might be backyard trees and ground between them, while the habitat of a lion would be grasslands with tree cover. A niche is the sum of physical, chemical, and biological limits on an organism, and the role it plays in its habitat. It describes how organisms respond to resource distributions, and primarily describes behaviors. A single habitat can host many different types of organisms—think of how many organisms might occupy a tree in the rainforest—each playing many different roles in the same space. When different populations with similar needs occupy the same habitat, this often results in niche partitioning. That is, each population occupying the niche eat slightly different things, require different amounts of light, etc. This reduces competition between the populations, allowing them to survive and thrive in the same space. As an analogy, you might think of the different roles people play aboard, for example, a starship in a fictional tv show. A 100-person crew will not comprise 100 captains, or 100 doctors, or 100 security officers—there would simply not be enough space or tasks to keep 100 people busy doing the exact same job. Meanwhile, while 100 people are competing for the resources of one first officer, a multitude of

288

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

Figure 12.11  The hierarchy of ecological relationships applied to dinosaurs. An individual Camarasaurus (an

organism) interacted with other individuals of Camarasaurus (a population), as shown from multiple bones of one species discovered in a bonebed. Members of other species, including plants for food and other dinosaurs living in the same environment, formed a paleo-community. The environments in which these communities lived and interacted (ecosystem) can be determined from sedimentary and/or isotope data. Finally, just like today, the physical and biological environments were part of the ancient biosphere. (Image credits are as follows: Camarasaurus by J. St. John, https://flic.kr/p/paYmJ4; population adapted from National Park Service; community (vertebrates) adapted from J. Lallensack, https://commons.wikimedia. org/wiki/File:Dinorama_price.jpg; fossil cycad courtesy of G.R. Wieland, https:// commons.wikimedia.org/wiki/File:Amer​ ican_​fossi​l_cyc​ads_(​1906)​_(179​59823​810).​ jpg; fossil ginkgo courtesy of U.Name. Me, https://commons.wikimedia.org/wiki/ File:Ginkgo_NHM_fossil.jpg; ecosystem courtesy of ABelov2014, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=64​ 76477​0; biosphere courtesy of NASA.)

other tasks go ignored. Instead, all the responsibilities of operating the ship are divided into roles that are filled by people with the appropriate skill set. This is similar to niche partitioning, except in ecosystems, it is geological forces and evolution that partition the niches and determine which organisms are most suited to them. Niche partitioning is a strong evolutionary driver, and may have contributed to the different stances of diplodocids and macronarians (see Chapter 9). We can see other examples of niche partitioning in the fossil record. For example, we occasionally see the bones of different kinds of herbivores together in the same bonebed. How can populations of massive plant-eating ceratopsians live in the same environments as massive plant-eating hadrosaurs? We know from studying the morphology of these different dinosaurs and comparing the structure of their skulls and jaws, these dinosaurs were eating very different types of plants (Chapter 15). This is a way of reducing competition, allowing them to live and thrive side-by-side (Figure 12.12). As mentioned earlier, eating is a primary driver of ecology. Thus, we can also frame ecological interactions or organisms by the trophic level they occupy. This hierarchy categorizes organisms according to the distance the food they eat is removed from the sun’s energy (the origin of all energy in the ecosystem) (Figure 12.13). The trophic levels of an energy pyramid include: • Primary producers: These organisms both produce their own food and provide that energy to the rest of the ecosystem. They are also called autotrophs, or “self-feeders” (auto = self, troph = eat). The vast majority of biomass on the planet is made up of autotrophic organisms, and so we say that this group forms the base of the pyramid. Primary producers include plants, photosynthesizing bacteria, and lithotrophic (litho = rock) microbes that break down rocks for nutrients.

12.3  The Biosphere: Biological Environment

289

Figure 12.12  This reconstruction of the ancient habitat of what is now the Dinosaur Park Formation in Canada is based upon the type and distribution of fossils of all kinds recovered from these sediments. The fossils, together, support that this was once a diverse habitat, filled with a variety of plants, insects, mammals, and dinosaurs, both herbivores and carnivores. (Courtesy of J.T. Csotonyi,

https://commons.wikimedia.org/wiki/ File:Dino​saur_​park_​forma​tion_​fauna​_(cro​ pped-​01a).​png.)​

Figure 12.13  Pyramid of trophic levels. This pyramid is organized by

how far an organism is removed from the primary source of all energy on the surface of our planet—the sun. At the base are the primary producers that utilize sunlight directly to produce biomass. These producers, or “autotrophs” (selffeeders), are the group upon which all other life depends. The next three levels are heterotrophs (other eaters), which obtain the energy to grow and reproduce through the breakdown of tissues of other organisms. Herbivores (primary consumers) eat the producers. Carnivores (secondary consumers) eat the herbivores. At the top of the pyramid, the tertiary carnivores (tertiary consumers) eat from all levels of consumers (i.e., herbivores as well as other carnivores), but are not typically eaten themselves. (Courtesy of Thompsma, https://commons. wikimedia.org/wiki/File:Trophiclevels.jpg.)

• Primary consumers: These are the organisms that directly eat the primary producers. While you might be tempted to think of this group as synonymous with herbivores, there are more autotrophs than just plants, and so there are more types of primary consumers than just herbivores. They come in all shapes and sizes, from grasshoppers and microbes, to mealworms and cows—and of course, hadrosaurs and Triceratops. • Secondary consumers: These are the organisms that eat the primary consumers. These include most carnivores; for example, a wolf that eats a deer. But this can also include insectivores, such as a bird that eats a grasshopper. Secondary consumers usually exist in smaller populations than primary consumers—you’ve seen more cows than you have wolves or mountain lions—and thus take up a smaller portion of the energy pyramid.

290

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

• Tertiary consumers: These are the organisms that eat secondary consumers (and sometimes additional levels of predators in between). These would include examples like a hawk that eats a snake that ate a mouse. Because no one eats them (usually), they occupy the top-most level of the energy pyramid, and thus are sometimes called apex predators (apex = peak). Of all these levels, where do you think humans fit? Primary, secondary, and tertiary consumers are together called heterotrophs (hetero = other; troph = eater; “other eaters”). These relationships between consumers aren’t always linear, and in reality, ecosystems are always much more complicated than a pyramid diagram. For example, omnivores, which eat both plants and meat (e.g., pigs, bears, and humans), can function as primary, secondary, or tertiary consumers, depending on what they happen to be eating. So how can we apply trophic levels to dinosaurs? Unfortunately, it isn’t so simple as sampling modern ecosystems for a distribution of animals on different trophic levels. As you have seen in Chapter 11 (Taphonomy), much information is lost in the transition to the fossil record. Some organisms that may be present and which fill important roles in original communities are less likely to preserve than others. For example, jellyfish and crabs are both found in nearshore communities, but soft-bodied jellyfish are much less likely to preserve than crabs. In this way, a fossil “community” is almost certainly missing some of the original players. Such taphonomic biases can also result in the fossils that do persist becoming overrepresented, relative to their position in their original ­habitat. Another issue to contend with is that fossils of different populations that lived in an area over a rather long period, but which never actually interacted, can become mixed together within the sediment layers, making it appear as if they had. This is called time averaging, because it gives you an “average” of what was present over a time range, but not what exactly was present at any one time. However, while this can be problematic if you are trying to investigate which species directly interacted with each other, time averaging has an upside as well, in that it allows us to sample ecological systems differently than we sample current ones. If you think about it, any one species in an ecosystem today may be actually quite rare—think about how often you might see a bear or mountain lion in a forest compared with how often you might see a deer, or how often you might see deer compared with how often you might see trees. A fossil assemblage that represents the average of an ecosystem over time is more likely to capture these less abundant species than any “snapshot” could. Thus, time averaging can allow us to observe more subtle changes in an ecosystem over time, even if it can’t give us an accurate picture of the paleoenvironment at any one time. If conditions are exactly right, however, we can tell a lot about the interactions within ancient ecosystems. For example, sometimes we can find evidence of predation on plants, where the margins of leaves are altered and look “chewed”, or where worm traces or forms of disease can be seen. These types of fossils also illustrate why taphonomy becomes so important in interpreting the fossil record. Has the leaf in Figure 12.14 been eaten, thus reflecting ancient ecological interactions? Or is that taphonomic alteration? What might you look for to determine which it is? We can define autotrophs and heterotrophs in living ecosystems and extinct ones, but there are some organisms that have specialized even beyond this, and almost certainly this was the case for dinosaur ecosystems as well. Scavengers are carnivores, but specialized ones that eat organisms that are already dead, rather than hunting and killing fresh prey. Many carnivores—even those we think of as “prime examples”

12.3  The Biosphere: Biological Environment

291

Figure 12.14  These two fossil leaves were recovered from Fossil Butte National Monument, representing a 50-million-year-old lake ecosystem.

The leaves are very similar, but the one on the right shows a central hole. Is this the result of disease? Predation by insects, thus reflecting ecological interactions between producer (leaf) and primary consumer (insect)? Or is this the result of taphonomic processes? (Adapted from the National Park Service (https​://ww​w.nps​.gov/​fobu/​plany​ ourvi​sit/i​mages​/inte​racti​on.gi​f.)

of hunters—tend to exhibit some scavenging behavior (why pass up a free meal?), so classification as a scavenger is generally a question of frequency and preference rather than a hard distinction between these two behaviors. Hyenas can hunt and kill when they must, and lions will scavenge, given the opportunity. Non-vertebrate organisms can also be specialized to eat dead things. Fungi, molds, and microbes that participate in degrading organic matter do so through enzymes and slime they secrete; they digest outside their bodies and take the broken-down substances in after they are digested. These are called saprophytes. Detritivores (or bottom feeders) obtain nutrients from forest floor litter or seafloors, taking this detritus into their bodies and breaking it down within. Crayfish and earthworms fall into this category. In reality, however, relationships between organisms on different trophic levels are rarely linear and can better be depicted as a food “web”, as many organisms can operate on different levels. In Figure 12.15, you can see a food web depicting relationships in a modern ecosystem. The tree (producer) supports fungi, various bugs, and worms and insects at its base. These in turn provide food for the frogs and birds and squirrels that occupy its branches. But these are eaten by secondary consumers (snakes) which can be eaten by foxes, who also eat squirrels. This is much more of a web-like interaction than a straight “chain”. So now that we have the roles established, we can begin to design dinosaurian food webs! Remember, the question is, to eat or be eaten! This is one of the major evolutionary drivers of all organisms. Thus, figuring out who eats who is a window into how organisms relate to others in their local environments. It is a little harder to reconstruct these relationships between dinosaurs, but sometimes we can. For example, one dinosaur bone bed preserves abundant dinosaur remains, all from a single species of hadrosaur called Maiasaurus. Some are clearly adult, but some are smaller, and some nests and eggs have been found with hatchling and embryonic remains. Scattered among the bones and eggs were irregular “rocks” with differing textures and densities. These “rocks” were uniformly black (Figure 12.16), with a strange texture. Microscopic examination of these odd fossils clearly showed tiny chunks of plant parts—xylem and phloem from a gymnosperm (a type of non-flowering plant), a kind similar to a conifer (like a pine tree). A closer look showed that woven throughout this structure were small tunnels, providing evidence of a Mesozoic food web! (See Chapter 15 for a more complete discussion of these fossils.)

292

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

Figure 12.15  This simplified chart represents possible interactions between organisms within the habitat of a tree. The tree is the producer.

Beetles survive on tree tissues and are eaten by frogs and squirrels. In this diagram, into what trophic level does the snake fit? What about the millipede? Which animal shown is the tertiary consumer? (Adapted from Thompsma, https://commons.wikimedia. org/wiki/File:TrophicWeb.jpg.)

Figure 12.16  This diagram represents a dinosaur food web. As primary

consumers, the hadrosaurs eat the conifers (primary producers) in their local environments. The hadrosaurs “process” this plant material, producing dung in which we can find remnants of undigested plant tissues. The dung is then colonized by dung beetles. What trophic level does the dung beetle fill? (Image credits are as follows: artwork of hadrosaurs courtesy of P. Riha, https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=43​32510​; dung beetle courtesy of LiquidGhoul, https://commons. wikimedia.org/wiki/File:Dung_beetle.jpg; coprolite macro and histological images courtesy of K. Chin.)

Paleoecology is also useful for testing hypotheses. Take, for example, the infamous Tyrannosaurus rex. Of course, everyone “knows” it was the fiercest predator to ever walk the Earth…right? But how well supported is this hypothesis? Let’s look at the evidence.

12.4 AN ECOLOGICAL CASE STUDY: TYRANNOSAURUS REX After reading this section you should be able to… • Evaluate the evidence for Tyrannosaurs rex as a predator or a scavenger.

12.4  An Ecological Case Study: Tyrannosaurus rex

293

One thing we can say for certain about T. rex is that it ate meat. Whereas the teeth of herbivores have expanded surfaces to grind hard plant material, T. rex teeth are similar to known carnivores today; they were sharp and pointed, recurved, and highly serrated (see Chapter 15). Knowing that it ate meat, however, doesn’t exactly tell us how it ate meat. Did it hunt down prey and kill it? Did it lie in wait, still and hidden, until some unsuspecting hadrosaur walked past, then jump out and take it down with its massive bulk and huge head? Or did it simply wait for some poor dinosaur to die another way, and then happily munch on a free meal? Figure 12.17 depicts both of these scenarios. Obligate scavengers, carnivores whose diets consist mainly of food sources that have died by other means, are very rare. But among living vertebrates, only vultures and their close cousins fit that definition— thus, all extant obligate scavengers are dinosaurs! So, what adaptations can we see in these living dinosaurs which fit them for a scavenging niche? Whether scavenging is obligate or a preference, organisms whose diet is mainly scavenged meat typically have specialized digestive tracts that prevent them from becoming sick from consuming rotten, decayed flesh full of various microbes. This can include adaptations like extremely acidic digestive acids, or in the case of vultures, the lack of feathers on their face and head so that they don’t get contaminated by microbes of decay while eating (Figure 12.18).

Figure 12.17  Was T. rex a fierce, active predator, like the ones in the background chasing down an unlucky hadrosaur? Or, as proposed by paleontologist Jack Horner, was this much-feared dinosaur really an obligate scavenger, like the one in the foreground, chewing on already dead, gooey dinosaur remains? (Courtesy of

Luis Rey.)

Figure 12.18  One feature of living dinosaurs that are obligate scavengers such as the vulture (A) is that they lack feathers on their head, differentiating them from non-scavenger avian relatives (B).

This adaptation fits them for a diet made up of bacteria-rich, and/or disease-carrying carrion. Rotten organics and their bacterial load cannot stick to the bald head of a vulture, as they would with feathers on the head and around the mouth. (A courtesy of Dori, https​://co​mmons​.wiki​media​.org/​w/ ind​ex.ph​p?cur​id=94​39241​; B courtesy of bs-matsunaga.)

294

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

Additionally, although most birds rely primarily on sight for hunting, and have a rather poorly developed sense of smell, vultures can smell carrion up to a mile away. The part of the brain dedicated to olfaction, or smell, dictates the ability to smell over long distances. In a vulture, this lobe is greatly enlarged relative to other birds, indicating that it has more brainpower for detecting and interpreting odors (Figure 12.19). Of course, as mentioned in Chapter 11 (Taphonomy), soft tissues like the brain have an exceedingly low likelihood of preserving, but the space where the brain was housed can sometimes be filled in secondarily by mineral, creating a rough approximation of the shape of the brain as an endocast. When an endocast of the brain of a T. rex was examined in the same way as the vulture (Figure 12.20), it was shown that the olfactory lobe was much enlarged compared with the rest of the brain, making it clear that T. rex interpreted its world primarily through its sense of smell. This evidence seems to support a hypothesis of scavengery. However, the orbits (eye socket) and optic nerves were also relatively large in T. rex, suggesting the possibility of good vision as well. In fact, the eyeball itself was probably bigger than any terrestrial animal alive today; it is only because T. rex had such a massive head to start with that its eye and brain look relatively small in comparison (see Figure 12.20C). But what about other senses? What else does the brain of a T. rex show? When the endocast of an adult T. rex brain was examined, it revealed features that might shed light on the ecological niches this massive dinosaur filled. CT data produced by WitmerLabs at Ohio University showed another feature that is important in determining the niche occupied by T. rex: balance. Predators need to have good balance because they need to be able to twist and turn quickly to take down evasive prey. And in addition to good visual acuity, they also need binocular vision, in which their two eyes have an overlapping field of vision that allows them to

Figure 12.19  A computed tomography (CT) image of the brain of a turkey vulture, which relies strongly on a good sense of smell to locate carrion.

The olfactory lobes (labeled “olfactory bulb”) of these birds are large relative to the overall size of the brain. (Courtesy of L. Witmer, WitmerLab at Ohio University.)

12.4  An Ecological Case Study: Tyrannosaurus rex

295

Figure 12.20  (A) Endocast of the cavity that would have held the brain of a Tyrannosaurus rex. The space for

the two olfactory lobes at the left in this image is greatly expanded relative to the rest of the brain. (B) CT reconstruction of the brain that would have occupied the cavity represented by the endocast in (A). Yellow represents the cranial nerves, dark blue and bright red are part of the vascular system feeding the brain, and pink is the bony labyrinth (see below). The two olfactory bulbs (OB) of the brain dedicated to smelling are enlarged relative to the rest of the brain. (C) Reconstruction of the skull of a T. rex, showing the relative size and placement of the brain. AW = airway, with a red arrow indicating air passage. OLF = olfactory sinus, with the smaller arrow indicating the passage of odorous molecules to the brain and the olfactory bulb. Scale bar in B = 4 cm. (A courtesy of M. Martyniuk, https://commons.wikimedia. org/wiki/File:Tyrannosaurus_brain_aus. jpg; B and C courtesy of L. Witmer and WitmerLabs, Ohio University.)

perceive depth. Vertebrates that employ binocular vision hold their head so that the eyes are forward-facing, allowing them to focus their eyes to accurately follow prey. How can we possibly know how T. rex habitually held its head, or whether it was agile? The brain endocast scans, in addition to showing enlarged olfactory lobes, also revealed the size, shape, and orientation of a small bony region referred to as semicircular canals, which house the organs responsible for balance. Humans have them as well! These tiny, fluid-filled canals are oriented in two separate planes—one horizontal and two vertical—and they sense acceleration or change in direction of the head. How these canals were oriented—in particular, how they were oriented with respect to the plane of the ground—correlates to how a dinosaur held their head, just as in living vertebrates. When these canals are oriented so that the horizontal one is parallel to the ground, it allows determination of the position in which the head was habitually held. A careful comparison of the semicircular canals of different dinosaurs, including T. rex, with living crocodiles and birds, shows that T. rex was more similar to birds than to crocodiles (Figure 12.21). It held its head with the chin lowered, and the eyes pointed straight forward, implying binocular vision. All of these features are consistent with active predation! What about T. rex arms? We know that for many active predators, arms are very important (Figure 12.22), and many dinosaurs, particularly the more derived maniraptorans that we interpret as fierce predators, also have long arms. That the arms of T. rex are so tiny (each T. rex arm was

296

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

Figure 12.21  High-resolution CT images show the location and position of the brain in the skull of an adult Tyrannosaurus rex (top). When

the brain endocast is enlarged to show detail (bottom), the location and orientation of the semicircular canals are visible. When the semicircular canals are oriented as they would have been in life (aligning the horizontal canal with the horizon as on the right), it indicates that T. rex had forwardoriented eyes that allowed for good binocular vision—characteristics generally associated with predation. (Courtesy of L. Witmer and WitmerLabs, Ohio University.)

about the size of an adult human arm) relative to its 7-ton, 40 ft body (Figure 12.23) is one of the great mysteries of dinosaur science. Although these arms have been portrayed as useless, biomechanical studies show that they were relatively strong, capable of lifting hundreds of pounds (see Chapter 13). But because they couldn’t touch their arms together, and because they only had two tiny fingers, not exactly designed for grasping, it is a pretty safe bet they didn’t use their arms to catch prey. Then again, with a mouth like that, did they need to? Additionally, living dinosaurs have no need of arms to catch prey. Their arms, in fact, are otherwise occupied—with flight (Figure 12.24)! So perhaps the “small arms indicate scavenging” argument is not so strong either!

Figure 12.22  Many active predators, especially mammals, use their forelimbs to take down prey. For (A) domestic cats, (B) foxes, and (C) tigers, as well as bears, wild cats, and other predators, forelimbs play an important role in securing their food.

(A courtesy of MagAloche, https://commons. wikimedia.org/wiki/File:Catch_cats.JPG; C courtesy of K. Burkett, https​://ww​w.fli​ckr.c​ om/ph​otos/​kevin​wburk​ett/2​93322​7072.)

The ability to run fast is also important for most active predators. We know that animals adapted for running generally have a longer tibia (relative to the length of their femur) (see Chapter 13). The biomechanics of T. rex running are not definitive, but, looking at the relative length of its leg bones, it probably could not run very fast. Its body size and proportions favor its interpretation as a relatively slow mover, at least as an adult; its legs were massive, its body heavy, and it probably took a lot of energy for this big beast to move faster than a walk. However, it probably had great endurance and could follow prey for long distances. These features are more consistent with either a scavenger (whose prey is already dead, thus not likely to run away) or an ambush predator (who lies in wait for prey). On the other hand, active predation only requires that a predator be able to run a little faster than its lunch! In addition, there was, according to models, a lot of power behind those legs. So, the biomechanics of T. rex legs doesn’t shed definitive light on this question. Finally, however, there is some evidence to suggest that T. rex was at least occasionally acting as a predator. A tail vertebra from an Edmontosaurus was preserved with a T. rex tooth inside (Figure 12.25). This tooth could be definitively assigned to T. rex by the number and size of serrations on the tooth. Although evidence of carnivory in the form of tooth marks and embedded teeth can sometimes be found in the bones of dinosaurs (Chapter 15), oftentimes, it is impossible to tell how long the

12.4  An Ecological Case Study: Tyrannosaurus rex

297

Figure 12.23  The arms of a Tyrannosaurs rex are roughly the size of an adult human arm—only they’re attached to a 40 ft (12.2 m) body! However, despite their relatively tiny size, the muscle attachments on their forelimbs indicate that they were very strong, and the relative robustness of these bones suggests that these were more than useless vestigial appendages. (Courtesy of K.

Tiffany, photographed at the North Carolina State Museum of Natural Sciences.)

Figure 12.24  Arms are not so important for predatory birds— they trap and carry their prey with feet! How does this complicate the discussion about what the small arms of Tyrannosaurus rex imply about its predation habits? (Courtesy of S.

Bhardwaj, https://flic.kr/p/bwk3Ji.)

Figure 12.25  A tail vertebra from an Edmontosaurus was found with a tooth embedded in it. By comparing

the size of the tooth and the number and spacings of the serrations, the tooth was definitively assigned to Tyrannosaurus rex. However, the vertebra showed signs of healing, indicating that the hadrosaur was definitely alive when the T. rex tried to take a bite out of it. (Courtesy of D. Burnham and R. DePalma.)

298

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

Figure 12.26  So what do you think? Scavenger, predator? Or false dichotomy? (Courtesy of R. North,

Dinosaur Comics.)

animal was dead when it happened. Was it freshly killed by the carnivore that left the marks, or did the carnivore come along later to gnaw on its bones? In this case, we know for certain this Edmontosaurus was alive when the T. rex tried to take a bite out of it, because the bone tissue of the vertebrae shows signs of healing! This could only happen if the Edmontosaurus escaped and lived long enough for its wounds to start closing. In this section, we’ve discussed how we evaluate competing hypotheses in paleontology—was T. rex a fearsome predator or an obligate scavenger? Taking all data available into account, there was some support for both hypotheses. But, what about a third option? What if T. rex, as a tertiary consumer, ate whatever it wanted (Figure 12.26)? Could it have eaten already dead organisms when they presented themselves, but also have taken down prey when it needed to, much like living hyenas? This illustrates a nuance in how we frame our hypotheses. The hypotheses of “T. rex was only a predator” and “T. rex was only a scavenger” could potentially be falsified; if definitive evidence of scavengery is found, it falsifies the hypothesis T. rex never ate dead things. Conversely, a T. rex tooth lodged in a healed Edmontosaurus vertebrae falsifies the idea that T. rex never hunted. The hypothesis that T. rex did both things occasionally, but one more than the other, is incredibly hard to test or falsify—even if it’s more likely to be true. So, what do you think? Scavenger or predator? Or a false dichotomy?

12.5 WHAT WE DON’T KNOW 12.5.1 How Might Changes in Earth’s Atmospheric Composition Have Driven Organisms to Exploit New Habitats? We know that our atmosphere has changed drastically over time. We have seen periods where oxygen levels were much higher than today (35% vs. 21% today), and other times when it was much lower (as low as 5%). This may have played a role in the movement of animals out of the water and onto the land, and the origin of tetrapods (see Chapter 5) because oxygen levels would be drastically reduced for active

12.5  What We Don’t Know

­ ater-dwelling organisms. Animals in the water that were active would w have been strongly driven to move onto the land where oxygen was less limiting. But we do not fully understand how and why oxygen levels fluctuate—why they stay relatively stable for long periods and then change. Questions to consider: 1. What role did oxygen level play in the evolution of dinosaurs? It has been posited that increased oxygen favored the evolution of larger dinosaurs while others argue that gigantism in dinosaurs (sauropods) is not explained by oxygen levels. 2. Could oxygen levels also have favored the origin of flight in avian dinosaurs? If oxygen were higher, it could have made it easier for their muscle cells to generate the power needed to fly. 3. Will further refining paleo-oxygen levels through time provide more insight into the evolution of animals into new habitats?

12.5.2 Why and How Did the Environments of the Jurassic and Cretaceous Favor Such Massive Sizes for Terrestrial Vertebrate Animals? The Earth has never seen terrestrial vertebrates as large as the massive sauropods that existed during the reign of the dinosaurs. Even the massive theropods like tyrannosaurus and Spinosaurus are unrivaled for terrestrial predators. The massive size attained by dinosaurs leads to a lot of unanswered questions about the ecological interactions of these giants and the organisms they shared the biosphere with. Questions to consider: 1. Why did predatory dinosaurs become so much larger than any predator that came before or after them? 2. How could such large herbivores sustain their dietary needs without completely wiping out and devastating the plants in their environment, especially if they lived communally? 3. Did such intense predation on plants drive the evolution of flowering plants? Flowering plants produce enclosed seeds that are more resistant to digestion. 4. Why did so many bipedal animals fill niches in the past that are only filled by quadrupeds today? All fast runners today (except the ostrich) are quadrupedal, but the fastest non-avian dinosaurs were bipeds.

CHAPTER ACKNOWLEDGMENTS We thank Dr. Chris Organ for his generous review and suggested improvements to this chapter. Dr. Organ is an Assistant Teaching and Research Professor at Montana State University. This chapter was also greatly improved by discussions with Dr. L. Witmer (Ohio University) and Dr. G. Retallack (University of Oregon).

INSTITUTIONAL RESOURCES Much of the work done at the Witmerlab at Ohio University led by Lawrence Witmer has paleo-ecological implications. Find out more here: https://people.ohio. edu/witmerl/lab.htm

299

300

CHAPTER 12    How Do We Interpret the Ecology of Dinosaurs?

LITERATURE DePalma, R. A., Burnham, D. A., Martin, L. D., Rothschild, B. M., and Larson, P. L. (2013). Physical evidence of predatory behavior in Tyrannosaurus rex. Proceedings of the National Academy of Sciences, 110(31), 12560–12564. Hyland, E. G., Sheldon, N. D., Van der Voo, R., Badgley, C., and Abrajevitch, A. (2015). A new paleoprecipitation proxy based on soil magnetic properties: Implications for expanding paleoclimate reconstructions. Bulletin, 127(7–8), 975–981. Mallon, J. C., and Anderson, J. S. (2014). The functional and palaeoecological implications of tooth morphology and wear for the megaherbivorous dinosaurs from the Dinosaur Park Formation (Upper Campanian) of Alberta, Canada. PLoS One, 9(6), e98605.

Tabor, N. J., and Myers, T. S. (2015). Paleosols as indicators of paleoenvironment and paleoclimate. Annual Review of Earth and Planetary Sciences, 43(1), 333–361. Wade, D. C., Abraham, N. L., Farnsworth, A., Valdes, P. J., Bragg, F., and Archibald, A. T. (2019). Simulating the climate response to atmospheric oxygen variability in the Phanerozoic: A focus on the Holocene, Cretaceous and Permian. Climate of the Past, 15(4), 1463–1483. Witmer, L. M., and Ridgely, R. C. (2009). New insights into the brain, braincase, and ear region of tyrannosaurs (Dinosauria, Theropoda), with implications for sensory organization and behavior. The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology: Advances in Integrative Anatomy and Evolutionary Biology, 292(9), 1266–1296.

13 HOW DO WE KNOW HOW DINOSAURS MOVED?

13

DINOSAUR FUNCTIONAL MORPHOLOGY

I

n Jurassic Park, there is a famous scene where a fierce, single-minded Tyrannosaurus rex is chasing down a jeep—and succeeding! In another scene, two hungry velociraptors are searching for children hiding in a kitchen, and they turn the door’s handle to get into the room. How realistic are these scenes? And more importantly, how can we possibly know what behaviors dinosaurs engaged in when no human has ever seen one? We can’t take out a stopwatch and clock how fast a T. rex ran. So how can we possibly determine the function, movement, and speed of extinct animals, including dinosaurs? To make any hypotheses about dinosaur function and lifestyle, you probably have guessed by now that we need living models to use as a baseline for what is possible—possible movement at joints, possible muscle attachment sites, etc.—and how these relate to the function of animals that possess them. However, herein lies a substantial limitation that affects the robustness of the conclusions we can draw: what living animals are appropriate models for non-avian dinosaurs? Birds are the only living representatives of Dinosauria, and aside from a few flightless basal species (e.g., ostriches and emus), the vast majority of avian taxa are highly adapted for flight in ways that make them poor models for extinct dinosaurs that lived their life on the ground. The diversity of form in today’s flightless terrestrial vertebrates lies in Mammalia, and, as you know, dinosaurs are not mammals. Mammals and dinosaurs are not only phylogenetically distant, but they are also physiologically distinct (Chapter 18), and these factors would directly affect how they function. For example, the ancestor of all dinosaurs was an obligate biped. The ancestor of all mammals, however, was an obligate quadruped. This most definitely affected their function and lifestyles. However, while this is certainly a limitation, all is not hopeless! Below we identify some relationships we observe between form and function in extant vertebrates, and discuss possible ways these might apply to extinct dinosaurs, always keeping the above caveats in mind.

IN THIS CHAPTER . . . 13.1 FORM AND FUNCTION 13.2 RUNNING: CURSORIAL LOCOMOTION ADAPTATIONS 13.3 CLIMBING: ADAPTATIONS FOR ARBOREAL LOCOMOTION 13.4 DIGGING: ADAPTATIONS FOR FOSSORIAL LOCOMOTION 13.5 JUMPING: ADAPTATIONS FOR SALTATORIAL LOCOMOTION 13.6 DINOSAUR BIOMECHANICS 13.7 WHAT WE DON’T KNOW

302

CHAPTER 13    How Do We Know How Dinosaurs Moved?

13.1 FORM AND FUNCTION After reading this section you should be able to… • Define biomechanics or functional morphology. • Describe the four different locomotor modes that terrestrial organisms use.

We have already seen that bones within a skeleton have different morphologies (shapes) (Chapter 6), and the same bone in different animals may be shaped differently. At first glance, your humerus doesn’t look much like that of a whale (Figure 13.1), though the fundamental features and patterns remain, reflecting their common ancestry; the humerus still articulates with the scapula, and the radius and ulna articulate at the distal end of the humerus. However, changes in limb function to adapt to either climbing (human) or swimming (whale) behaviors have radically altered the overall shapes of these bones. The variation in skeletal shape in animals that live very different lifestyles—and the skeletal similarities of those that occupy similar niches—is not a random coincidence. Rather, there is a close association between the shape of a bone and its function. Thus, by studying the subtle differences in bone shape, including the tiny raised scars that indicate where muscles are inserted on bone, we can discern certain features that are common to all animals that exhibit similar functions, regardless of their phylogenetic relationships. The study of how shape underlies function, and conversely, how function can be inferred from shape, is called functional morphology. A related discipline, biomechanics, is similar, but relies on Newtonian physics to calculate forces on bone and motions at joints. Both disciplines can be applied to dinosaurs as well as to living animals. Some of the biomechanical concepts we apply to interpret dinosaur behavior from skeletal elements are based upon principles that are likely quite familiar to you, but subconsciously applied. For example, something about Figure 13.2 is inherently wrong. You don’t look up in a forest full of trees and expect to see a horse. But why not? Why can’t horses climb trees? Humans can, even if we don’t practice this skill regularly,

Figure 13.1  Comparison of (A) human and (B) whale forelimbs. S = scapula,

H = humerus, R = radius, U = ulna. (A courtesy of P. Siedlecki; B courtesy of K. Tiffany, photographed at the North Carolina Museum of Natural Sciences.)

13.1  Form and Function

303

Figure 13.2  A horse in a tree?! What skeletal features of a horse make this a highly unlikely scenario? (Horse

image courtesy of K. Tiffany; tree adapted from B. Morin, https://commons.wikimedia. org/wiki/File:Sunn​y_gre​en_pa​ddy_f​i elds​ _with​_tree​s_and​_long​_shad​ows_a​t_gol​ den_h​our.j​pg.)

so what do we humans have that horses don’t? How are their bones, muscles, and other skeletal adaptations different than animals that can climb trees? And how can we apply this knowledge to dinosaurs? Osteology is the study of bones (osteo = bone; ology = study of). Looking at the bones and the joints between them gives an approximation of how they likely moved against one another. By comparing the same bone (e.g., the humerus) across species of living animals, we can determine similarities and differences, and the effects these have on function. We can then apply these concepts to related groups that are extinct. In other words, we use the comparative anatomy of creatures we can observe to determine certain things about animals we can’t. This is possible because all vertebrates, including dinosaurs, share certain features that reflect their common ancestry. For example, all vertebrates with limbs have one bone in their upper arm (the humerus), and two bones in their forearms (the radius and ulna), and they all possess the same muscle groups that move these bones at the joints—e.g, the deltoid, pectoralis, biceps, and triceps. Even lizards and turtles have these muscles. The size, shape, and relative thickness of these bones, and the mass of muscles may vary, but the pattern is consistent. Therefore, these principles can also be applied to extinct vertebrates as well. As you saw in Chapter 6, bone, regardless of who it belongs to, is a growing, vital, responsive tissue, and as such, it is capable of reacting to various stimuli. Muscles attach to bones to accomplish movement. If muscles did not have bone to provide resistance, vertebrate organisms, including humans, would simply be a shivering pool of goo—so thank your bones for your upright stance! To accomplish movement, though, bones must articulate with other bones, with few exceptions (e.g., the hyoid is a “floating” bone that

304

CHAPTER 13    How Do We Know How Dinosaurs Moved?

supports your tongue, but does not articulate with other bones). How bones articulate, as well as their overall shape, greatly affects function. Flat bones, like the scapula, have different functions and move in different ways than long bones like your femur. Knowing this lets us get at some basic functions dinosaurs likely could attain. How many ways are there for a terrestrial vertebrate to move? Observing those around us, we can see that animals can run, dig, hop, fly, or climb. These are not exclusive, because a fast runner, like a dog, can also dig—but that is not their primary locomotor mode. Non-avian dinosaurs were terrestrial animals that did not swim or fly as their main way to get around, so we will leave the discussion of the adaptations related to these specialized locomotor modes to the chapters that cover swimming and flying reptiles (Chapter 10) and birds (Chapter 19). Here, we will focus on four terrestrial locomotor modes. The four main terrestrial locomotor modes of vertebrates are: • Cursorial: Adapted to running • Arboreal: Adapted for climbing or living in trees • Fossorial: Adapted to digging • Saltatorial: Adapted to jumping/hopping For animals that display more than one locomotor mode, we see that their skeleton will have features of both. For example, dogs that run fast have long legs, but because they can dig, they also have enhanced features on their scapulae, pelves, and forelimbs that support that mode as well. And, in fact, different breeds of dogs that were bred for running (e.g., greyhounds, which were originally bred for chasing fox and deer) or digging (e.g., terriers, which were bred to dig rodents out of burrows) will show the features of these locomotor modes in their skeleton more strongly than others. To recognize the locomotor style of an animal from just its skeleton, then, we need to identify the skeletal features associated with each of these modes. Look at Figure 13.3. Which of these dogs is the fastest? What features do they possess that lead you to infer this? Now, let’s compare the forelimb skeletons of these same animals (Figure 13.4). There is not just a difference in overall size, but these limb

Figure 13.3  (A) Basset hound, (B) a German shepherd, (C) a Saluki, and (D) an English bulldog. Which of these

is the fastest? Why? What features do you associate with speed? (A and D courtesy of K. Tiffany; B courtesy of PROPOLI87, https:// commons.wikimedia.org/wiki/File:German_ shepard_female.jpg; C courtesy of Yohannvt, https://commons.wikimedia.org/ wiki/File:Saluki_in_India.jpg.)

13.2  Running: Cursorial Locomotion Adaptations

305

Figure 13.4  The skeletal forelimbs of (left to right) a Saluki (closely related to greyhounds), a German shepherd, English bulldog, and Basset hound.

(Courtesy of Frank van Tatenhove, EL Minja’s Lhasa Apsos, https://www.el-minjas. com/Movements.htm.)

elements vary in proportion as well. Notice the ratio of the upper limb (humerus) to the limb below the elbow in the skeleton of each of these dog breeds. The limbs of the cursorial dogs are very differently proportioned than for those dogs not adapted for speed!

13.2 RUNNING: CURSORIAL LOCOMOTION ADAPTATIONS After reading this section you should be able to… • Discuss adaptations for limb length, stride rate, and stability that are seen in cursorial locomotors. • Assess the relative speed of an animal based on its skeletal elements.

A cursorial animal is a runner—an animal adapted for speed. For a running animal, speed can be increased in two ways: (1) by increasing stride length (amount of ground covered between steps); or (2) by increasing stride rate (amount of time between footfalls). Essentially, speed is increased through skeletal adaptations that allow either longer steps, faster steps, or a combination of both.

13.2.1 Adaptations That Increase Stride Length A longer stride results in the ability to cover more ground with each footfall, for the same amount of effort. Functionally, an “easy” way to do this is to lengthen a limb, as longer legs can take bigger steps. However, when we look at skeletal adaptations that result in elongated limbs, they go far beyond simply increasing bone lengths.

306

CHAPTER 13    How Do We Know How Dinosaurs Moved?

Figure 13.5  (A) Human and (B) horse in lateral view show the placement of the scapula. On the human, it is

fully resting on the posterior ribs, but on the horse the scapula is more anterior and lateral, resting on the side of the ribs to stabilize the limb, helping to prevent rotation outward. (A adapted from BodyParts3D (DBCLS), https​://co​mmons​.wiki​ media​.org/​w/ind​ex.ph​p?cur​id=38​65671​9; B courtesy of K. Tiffany, photographed at the North Carolina State University School of Veterinary Medicine.)

Skeletal adaptations that result in functionally longer limbs, increasing stride length, include: • Scapula moves laterally: The movement of the shoulder from the back to the side lengthens the limb. • Distal limb elements elongate: The distal part of the limbs (i.e., the parts below the elbow and the knee) becomes longer relative to the proximal part of the limb (i.e., the upper arm and thigh). • Digitigrade or unguligrade foot posture: Much like standing on tiptoes makes one taller, a foot posture that raises the wrist or ankle off the ground lengthens the limb. Let’s compare a human with a horse to illustrate these concepts; while even the fastest human is relatively slow, a horse is an animal well adapted for a cursorial lifestyle. The human scapula rests completely on the back, while the horse scapula is oriented more toward the front and side of the rib cage, adding stability when limbs are in forward motion (Figure 13.5). As a result, it is much harder for a horse to dislocate its shoulder than for a human. The human scapula is also fixed, because it joins with the clavicle (collar bone) to hold the arm firmly in place. The horse, on the other hand, has lost its clavicles completely. This one single feature gives the shoulder more freedom to extend outward and forward in planar motion, which in turn allows increased stride length. Further, the human chest is flattened from front to back (Figure 13.6), which creates a greater surface (and thus greater wind resistance) in the direction of movement—the opposite of streamlining. The horse on the other hand is flattened from side to side, and has increased depth from back to front. When they run, there is less surface area to resist forward motion. Figure 13.7 illustrates other cursorial adaptations. The limbs of horses, deer, and other cursorial animals show that the further from the body, the relatively longer the skeletal elements become compared to non-cursorial animals. The femur, or thigh bone, is significantly shorter relative to the elements below the knee. In fact, in animals adapted for

13.2  Running: Cursorial Locomotion Adaptations

307

Figure 13.6  Cursorial animals like the horse (A) are narrow in anterior view, reducing the surface area that produces resistance and drag. Humans (B), on the other hand, are flattened front to back, and narrower in the lateral aspect. Reducing drag is not as important to non-cursors. (A

adapted from BodyParts3D (DBCLS), https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=38​65671​9; B courtesy of K. Tiffany, photographed at the North Carolina State University School of Veterinary Medicine.)

speed, the proximal joints are sometimes so close to the body that, when covered with skin, they might appear to the untrained eye as if they are inside the body wall (Figure 13.8). That is why at first glance, their knees and elbows appear to be “backward”—because it is actually the ankle and wrist you are seeing! Compare the relative lengths of a human’s foot, tibia, and femur with those of a horse (Figure 13.7). Let’s look at this in more depth, in animals whose speed we can measure. If you compare a leopard, a polar bear, an elephant, and a deer, you

Figure 13.7  The “knee” of the horse (A) and human (B) are marked with arrows. The “ankle” of both is marked

Figure 13.8  (A) Ostrich and (B) horse skeletons in lateral view, showing the body outline. Arrows indicate the femorotibial joint (knee) for each animal. In

animals adapted for speed, the proximal joints are often so close to the body that, when covered with skin, they appear as if they are inside the body wall. Thus, what many assume to be the knee (given its location when compared with ours) is actually the ankle. (B courtesy of T. Fletcher.)

with an asterisk. Measure the relative distance from the hip socket to the knee in each. The horse has proportionately elongated the leg from the knee down, in part by elevating the foot off the ground to an unguligrade posture. (A adapted from an image by BodyParts3D (DBCLS), https​:// co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=38​65671​9; B courtesy of K. Tiffany, photographed at the North Carolina State University School of Veterinary Medicine.)

308

CHAPTER 13    How Do We Know How Dinosaurs Moved?

probably already know which animals might come in first in a race—and it probably wouldn’t be the elephant! But why, exactly, is this true? If you look closely at Figure 13.9, a pattern emerges; it can be seen that the faster the animal, the shorter its femur relative to its tibia. Additionally, in the fastest animals, the ankles and toes also become relatively elongated, so that the leg above the knee is greatly reduced, relative to the leg below the knee. The general pattern is: • Femur > tibia: The animal is slow (measure the elephant limbs in Figure 13.9C). • Femur = tibia: The animal is moderately fast; (how does the bear compare to the leopard? • Femur < tibia: The animal is fast (e.g., the deer, Figure 13.9D). If this ratio is increased when considering the ankle and toe bones, the animal can run even faster. Look at the feet of the two fastest and the two slowest animals in Figure 13.9. What do you observe? Finally, as part of lengthening the lower limb, the foot posture changes to elevate the ankle off the ground, leaving only a small portion of the foot to touch the ground (Figure 13.10). The Amur leopard (Figure 13.11B) has a digitigrade foot posture—that is, it walks on the “balls of its feet”, as you might stand if you’re trying to reach something from a high self. The polar bear, on the other hand, walks with its feet flat and its ankle close to the ground (Figure 13.11A). This is called plantigrade foot posture, and it is the foot posture humans walk with as well. A horse (Figure 13.11C) goes even further than the leopard, and has an unguligrade foot posture—essentially standing on the tip of its toe, like a ballerina dancer “on-point”. Some of these same principles of proportion can be applied to dinosaurs—though it isn’t an exact comparison, because (with the exception of the ostrich) the fastest animals today (except the ostrich) are all quadrupedal mammals. Still, the length of the femur of the T. rex is almost equal to its tibia (Figure 13.12). When the distal limb elements are considered, its proportions are consistent with it being moderately fast—but even with its long legs, it probably was not fast enough to run down a speeding jeep! Conversely, the femur of the Lambeosaurus is longer than its tibia, and the foot below the ankle, while still digitigrade, is not greatly elongated. This dinosaur was relatively slow, making it a potentially delicious lunch for the T. rex. Thus, although a T. rex probably wasn’t an overly fast runner, we can say that it would have been fast enough to catch the meals it needed! Indeed, other evidence indicates that T. rex did occasionally munch on full-grown hadrosaurids (Chapter 15). Figure 13.9  Skeletons of (A) an Amur leopard, (B) a polar bear, (C) elephant, and (D) marsh deer. Pay

attention to the ratios of limb elements, the foot habit, the robustness of bones relative to size, and the placement of the scapulae in all of these. What do you see that is different? (A courtesy of L. Williams, SkeletonsUK.com; B adapted from Daderot, https​://co​mmons​.wiki​media​ .org/​w/ind​ex.ph​p?cur​id=23​13739​3; C courtesy of Skimsta, https​://co​mmons​.wiki​ media​.org/​w/ind​ex.ph​p?cur​id=99​51335​ ; D courtesy of the Museum of Veterinary Anatomy (FMVZ USP), https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=71​ 19910​0.)

So using the principles outlined above, what do you think about Figure 13.13? Do you think humans are adapted for speed? If we were the same size as a T. rex, could we outrun it?

13.2.2 Increasing Stride Rate Whereas increasing stride length increases speed by covering more ground per stride, increasing stride rate increases speed by making the limbs touch the ground faster and more often. Skeletal adaptations to increase stride rate include: • Reduction of the weight of limbs: Making them less energetically expensive to move rapidly. • Insertion of muscles close to the joint: Allowing shorter, faster muscle contractions to operate the limb movements.

13.2  Running: Cursorial Locomotion Adaptations

309

Figure 13.10  Various foot postures observed in living mammals: (A) human, (B) monkey, (C) dog, (D) sheep, and (E) horse. The human

and monkey (A, B) show plantigrade posture, where the entire foot (phalanges, metatarsals, and tarsals) including the heel are in contact with the ground. The dog (C) shows a digitigrade posture, where only the digits are in contact with the ground, while the metatarsals and tarsals are lifted. The sheep and the horse (D, E) show unguligrade posture, where only the last phalanx in the digit (the ungual) is in contact with the ground. (Adapted from J. LeConte, https://flic.kr/p/oupvCG.)

Figure 13.11  Hindlimbs of (A) plantigrade polar bear, (B) digitigrade Amur leopard, and (C) unguligrade horse. Which is the most adapted for

speed? Which is the slowest? (A adapted from Daderot, https​://co​mmons​.wiki​media​ .org/​w/ind​ex.ph​p?cur​id=23​13739​3; B courtesy of L. Williams, SkeletonsUK.com; C adapted from the Museum of Veterinary Anatomy (FMVZ USP), https​://co​mmons​.wiki​ media​.org/​w/ind​ex.ph​p?cur​id=70​07233​0.)

Figure 13.12  The hindlimb of (A) Tyrannosaurus rex compared with that of (B) Lambeosaurus. In each,

compare the length of the femur to the rest of the leg. By these measurements, which do you think is faster? What other factors might affect their overall speed? (A courtesy of K. Tiffany, photographed at the Field Museum; B adapted from Etemenanki3, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=64​85167​3.)

310

CHAPTER 13    How Do We Know How Dinosaurs Moved?

One way to increase stride rate is to reduce the weight of the limbs, thus reducing the amount of mass an animal must move with each stride and the energy they must expend to do so. One way to do this is to move the body of muscles that operate the limb closer toward the body core, reducing muscle mass in distal parts of the limb. Let’s return to our comparison between humans and horses. Humans have a lot of muscle in our lower legs, including those that form our “calves”. Conversely, the lower legs of horses, deer, cheetahs, and other fast mammals are basically just skin and tendon on bone. This is the result of two factors: the elongation of the ankle and foot, and the movement of the main muscle bodies more proximal, reducing the mass of the foot. The bodies of the major muscle of cursorial animals are concentrated in the legs above the wrist and/or ankle (as are ours), but from the ankle down, their lower limbs are mostly skin, bone, tendons, and ligaments. Skeletal evidence suggests that fast dinosaurs were similar to this. Take a look at the legs of the two very different animals depicted in Figure 13.14. Horses and elephants are doing different things with their legs! These physical constraints also operated in dinosaurs. We look at the muscle scars on bone indicating where they attached and how they moved (see below), and when we model dinosaurs, putting flesh and muscle over the bones we find, we apply this principle to get more accurate reconstructions. Dinosaurs with cursorial skeletal features are likewise reconstructed with a digitigrade posture that elevates the ankle, and very little muscle mass below the ankle joints (Figure 13.15A, C). As in modern birds, their knee joints were likely close to the body, so the majority of their muscle mass was contained proximal to the extended ankle joint, and the leg below the elongated ankle was mostly skin on bone. However, dinosaurs with robust heavy bones, ankles close to the ground, and other

Figure 13.13  Look closely at this human skeleton. How many specific

features can you identify that are not adapted for a cursorial lifestyle? (Adapted from Tiia Monto, https​://co​mmons​.wiki​ media​.org/​w/ind​ex.ph​p?cur​id=49​53860​5.)

Figure 13.14  Comparison of the hindlimbs of the (A) elephant and (B) horse. What specific features tell you

they are doing different things with their legs? The arrow marks the “knee” of each animal, and the (*) marks the ankle. What do you notice? Where is the muscle mass in both animals? (A courtesy of Skimsta, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=99​51335​; B courtesy of K. Tiffany, photographed at the North Carolina State University School of Veterinary Medicine.)

13.2  Running: Cursorial Locomotion Adaptations

features associated with mass are depicted with “bulked up” lower limbs containing a lot of muscle mass (Figure 13.15B, D). For example, the sauropod in Figure 13.15 has been reconstructed with a lot of muscle in the lower leg and ankle, because this animal did not need to be fast—in fact moving that amount of bulk would make speed almost impossible. However, sauropods would need power and endurance to migrate long distances to food sources, requiring muscles throughout the limb to help support its massive weight. On the other hand, the theropod is reconstructed with very thin legs below the ankle, basically just skin on bone—as we see in modern cursors, including the ostrich. Another way to reduce weight in distal portions of a limb is to move the muscle insertion points closer to the joint. Because of the scars on the bone left behind when muscles degrade, we have definite ways to determine where the muscles were. In Figure 13.16, the skeletal forelimb of a cheetah, a fast runner, is compared with a slower, more powerful badger (scaled as if they were the same size). Compare the bone proportions, robustness, and where the muscle inserts on the shaft of the bone relative to the joints. The muscle inserts close to halfway down the shaft of the badger humerus. In the cheetah, it is much closer to the joint. Also note that the bones are proportionately more slender in the cheetah, and more robust in the badger.

13.2.3 Stability and Efficiency Another critical factor for cursorial animals is stability. Imagine running for your life across a Pleistocene plain, being chased by a saber-tooth cat…and you twist your ankle. For want of a more stable ankle, you’d be a saber-tooth’s lunch. Skeletal adaptations that increase stability and efficiency include:

Figure 13.15  Comparing bone and muscle reconstructions of the hindlimb of (A, C) a cursorial theropod, and (B, D) a graviportal sauropod. Note the placement of the

knee relative to the body in each, and the elevation of the ankle relative to the ground. (Courtesy of M. Hallett.)

311

312

CHAPTER 13    How Do We Know How Dinosaurs Moved?

Figure 13.16  Comparison of skeletal adaptations in the forelimbs of a relatively slow badger (left), and a fast cheetah (right). Compare the

distance from the joint to where the muscle inserts on the bone shaft (double arrow). In faster animals, insertion is much closer to the joint. The center of gravity is also shifted from more posterior in the slow badger to more directly over the foot in the faster cheetah (labeled L). Finally note the shift in foot posture, from the plantigrade badger to the digitigrade cheetah. The size of the limbs is scaled for comparison. (Adapted from M. Hildebrand, 1960, How animals run. Scientific American, 202(5): 148–160. https://www.jstor.org/stable/24940484.)

• Joints restricted to one plane of motion: The inability to twist or rotate limbs prevent unintentional twisting during running. • Reduced number of digits: The weight of the foot is reduced and provides more stability when the foot hits the ground during running. • Elastic ligaments in feet and spine: Reduces the energy requirement for moving bones back to their original positions. Animals adapted for speed have many skeletal alterations to increase their stability and efficiency (i.e., maximize the energy output per unit energy put in) while running, that are not found, or not as well developed, in animals that fill other niches. For example, the joints of the hip (and shoulder in quadrupeds) are restricted so that they can only move in one plane; these animals cannot do side splits. Look at a dog. Its limbs can only move forward or backward, and unlike you, they cannot turn their palm toward their face. The knees (and elbows) are also reinforced with tight ligaments to prevent dislocation. Cursorial animals also modify their feet to increase stability and reduce weight. The ancestral state for tetrapod feet is five digits, but most runners reduce the number that touch the ground to three or fewer. Cursorial dinosaurs and birds have third digits that touch the ground during locomotion, and if they retain more, these digits are reduced and moved closer to the body, not touching the ground. Elk, deer, and other cursorial mammals reduce the digits in contact with the ground to either two or one (as in horses). In cursorial dinosaurs, often two of the three digits that remain are reduced in size, as we saw from footprint data as well (Chapter 16). Figure 13.17 compares the feet of two graviportal (heavy or massive) animals: an elephant (Figure 13.17A) and a sauropod (Figure 13.7B) scaled to approximately the same size. What similarities do you see that are adaptations for mass? On the other hand, Figure 13.18 compares the feet of three cursors—Deinonychus (left) Ornithomimus (center), and a

13.2  Running: Cursorial Locomotion Adaptations

313

Figure 13.17  The foot of an elephant (A) and sauropod (B). Both are

digitigrade. What advantages does this give? Because of what we know about elephants, we can propose that sauropods also walked with a massive pad under their feet. How do the number of digits and phalanges compare? What other adaptations do you see for mass? (Courtesy of K. Tiffany, A photographed at the North Carolina State University School of Veterinary Medicine; B photographed at the Field Museum.)

Figure 13.18  The feet of three cursorial animals. (A) Deinonychus shows the large retracted claw from which they derive their name (Deino = terrible, nychus = claw). (B) The foot of an ornithomimid. (C) A horse.

The star indicates the ankle of each. What adaptations do you see in each of these feet for speed? What differences do you note? (All courtesy of K. Tiffany, A photographed at the Field Museum, C photographed at the North Carolina State University School of Veterinary Medicine.)

horse (left). What similarities do you see? How are they different? In both figures, what can you say about the number of toes, and the number of phalanges in each toe? The feet of cursorial dinosaurs have three functional toes, with two of them much smaller than the third. This reduces the weight in the lower limbs. How does the horse compare? Finally, many cursorial animals have extra ligaments that run along the spine or in their feet. These are highly elastic, giving them a “springy” backbone, or feet that can return to the starting position without expending added energy. In horses, deer, and the like, these ligaments add great efficiency to their movements. What bony correlates to these ligaments would you predict? How (and why) might these be different in cursorial dinosaurs? These principles make sense and can be applied broadly, with one (very large) caveat. Most animals adapted for speed in today’s world are mammals, and mammals are very different than dinosaurs and birds in how their muscles operate, and in their evolutionary and metabolic histories. In addition, most cursorial mammals today walk and run on four legs,

314

CHAPTER 13    How Do We Know How Dinosaurs Moved?

but the earliest dinosaurs and all very fast dinosaurs were bipedal. This puts different stresses on the bone and different requirements on the muscles, so the application of some of the principles derived from living mammals must be applied to dinosaurs with caution. Interpreting dinosaur movements should always be done with a recognition of the limits of our models. Ostriches and emu are better models for dinosaur locomotion than mammals, so reconstructing dinosaur speed must take these limits into account.

13.3 CLIMBING: ADAPTATIONS FOR ARBOREAL LOCOMOTION After reading this section you should be able to… • Discuss the skeletal adaptations of arboreal locomotors.

Arboreal animals—animals that live primarily in trees—must be good climbers by necessity. Accordingly, animals that climb trees have very different skeletal requirements from those animals that run for a living. Instead of increased stride length, stride rate, and stability, tree climbers need flexibility, freedom of movement in their joints, and the ability to grasp branches. These are all qualities in direct opposition to the reduced digits and reinforced joints that favor running—which is part of the reason horses can’t climb trees! Instead, arboreal animals have completely different, distinctive skeletal features, adapted to increase the efficiency of movement in trees. Arboreal skeletal adaptations include: • Smooth, rounded hip and shoulder joints: Shoulder and hip joints of climbers allow close to a 360° range of motion. • Opposable digits: Arboreal animals retain the ancestral state in vertebrates of having five (or in birds, four) digits, but often one or two of these change in orientation relative to the rest (i.e., an orientation “opposed” to the rest) to allow grasping. This ability to grasp branches with hands—and sometimes feet or even tails— gives them a firmer, more versatile hold while climbing than animals that just dig their claws into bark. • Long, slender limb bones: The limb bones themselves are often long and slender because they don’t need to provide support against the greater stresses of running. • Scapula rotated toward the back: Figure 13.5 shows that runners have scapulae (shoulder blades) oriented on the sides of their rib cage, which streamlines the body to reduce resistance in the forward direction, and keep the fore- and hindlimbs moving in a single plane. Conversely, in arboreal mammals, the scapula is rotated toward the back, freeing the arm for movement in 360°. However, unlike mammals, cursorial dinosaurs were bipedal, so constraints were not present on the forelimbs as in mammals. Many of them had scapulae oriented for greater rotational freedom in the forelimbs • Chest narrows ventrodorsally: Where cursorial animals have their bodies “flattened” from side to side, so that there is less mass to create wind resistance in the forward direction, arboreal animals are “flattened” front to back, broadening the surface of the body that is in contact with the surface being climbed, thus changing the center of mass to make climbing more efficient.

13.3  Climbing: Adaptations for Arboreal Locomotion

315

As stated earlier, dinosaurs had bipedal ancestors, while mammalian ancestors were quadrupedal. The skeletal adaptations for running are quite different from those for climbing. Bipedalism is advantageous for both because liberating the forelimbs from locomotion frees them to take on other functions. Were any dinosaurs climbers? Do we see any of the features listed above in dinosaurs, consistent with climbing as their primary mode of locomotion? In the lineage of dinosaurs that led to birds—the maniraptorans—we see many traits that could be adaptations for flexibility in the upper body. For example, climbers need to be able to rotate their arms in almost 360°, moving forward to grasp and upward to hang. The shoulder girdle of small feathered dinosaurs that precede the first bird, Archaeopteryx (e.g., Epidexipteryx) show flexibility about this joint similar to that seen in modern birds (Figure 13.19). Many extant birds have one toe (or sometimes two) that is oriented backward relative to the rest—an opposable digit—that allows them to grasp and perch on branches (Figure 13.20). This condition in birds is called anisodactyly (an = not, iso = same, dactyl = digit). While good for climbing, it is not particularly favorable to running—and the ancestors of birds were cursors! Another adaptation that would facilitate climbing is the presence and position of elongated and highly recurved claws on the “hands” of some maniraptorans, such as Anchiornis. Surprisingly, we do see sim-

Figure 13.19  Some dinosaurs, such as Epidexipteryx hui (A), have adaptations that could be useful in climbing. In the skeletal reconstruction (B),

the humerus articulates with the scapula and corocoid in a way that allows rotation, and the claws on the hands and opposable digit could be used to grasp and climb surfaces. This dinosaur is older than the earliest recognized bird, Archaeopteryx. It does not have flight feathers, suggesting that its flying ability was very limited, if it could fly at all. A courtesy of Kumiko, https​ ://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=39​67845​9; B courtesy of Jaime A. Headden, https://commons.wikimedia.org/ wiki/File:Epidexipteryx_hui.jpg.)

Figure 13.20  Anisodactyly in (A) a living tui bird (Prosthemadera novaeseelandiae, and (B) Archaeopteryx. This adaptation is

excellent for grasping and perching, but not for running. (A courtesy of T. Willis, https​ ://co​mmons​.wiki​media​.org/​wiki/​Bird_​feet#​ /media/File:Tui_foot_02.jpg; B courtesy of E. Willoughby, https://commons.wikimedia. org/wiki/File:Berl​in_Ar​chaeo​ptery​x_-_d​etail​ _of_f​eet.j​pg.)

316

CHAPTER 13    How Do We Know How Dinosaurs Moved?

Figure 13.21  (A) Baby hoatzins have claws on the tip of their wings (arrow), which they employ to climb. It is possible that some dinosaurs may have used their clawed “hands” in a similar way. (B) An adult hoatzin. (A

courtesy of J.A. Thomson, https://commons. wikimedia.org/wiki/File:Hoatzin_chick.jpg; B courtesy of Kate, https​://co​mmons​.wiki​ media​.org/​w/ind​ex.ph​p?cur​id=14​03955​2.)

Figure 13.22  The semi lunate carpal (A, arrow) is a small half-moon shaped bone that changes the mechanics of the wrist. It allows lateral bending of the hand, critical to the flight stroke (B). This same bone is seen in maniraptorans like Deinonychus (C). (A courtesy of K.

Tiffany, photographed at the North Carolina State University School of Veterinary Medicine; B courtesy of I. Taylar, https​:// co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=84​47454​; C courtesy of K. Tiffany, photographed at the Field Museum.)

ilar-shaped claws on the “hands” of some living birds that can climb. Baby hoatzin, for example, retain claws on their wings and use them in climbing until they are mature (Figure 13.21). If an organism uses its forelimbs and hands to climb, it is important that they remain flexible, with a high degree of rotation in the wrist, as well as at the shoulder. By studying both the shape of the digits and the bones of the wrist, function and movement can be predicted. In particular, maniraptoran dinosaurs and their descendants possess a bone in their wrist only seen in this group. One of their wrist bones takes on the shape of a half-moon, which changes the degree and direction of motion at this joint. This little bone, called the semilunate carpal (Figure 13.22), covers other wrist bones, allows both a grasping motion in maniraptoran hands, and the lateral folding of the wings that makes the flight stroke in birds possible (Figure 13.22B).

13.4 DIGGING: ADAPTATIONS FOR FOSSORIAL LOCOMOTION After reading this section you should be able to… • Discuss the skeletal adaptations of fossorial locomotors.

Fossorial animals—animals that burrow for a living—have specific modifications to both their forelimbs and hindlimbs to make them more efficient, increase power, and increase stability in these body regions. Although few extant mammals are adapted to primarily dig, those that spend a significant amount of time digging or burrowing usually have at least some of these adaptations (except burrowing snakes, which don’t have forelimbs—or hindlimbs for that matter).

13.4  Digging: Adaptations for Fossorial Locomotion

317

Skeletal adaptations for animals that dig with their forelimbs include: • Increased power to the forelimbs: Animals adapted to a primarily fossorial lifestyle have enlarged areas for the attachment of larger muscles, and the muscles insert on the bone at points far from the joint, resulting in more power when they contract. • Robust shoulder and forelimb bones: Fossorial animals have shorter, more robust, and/or reinforced forelimb elements relative to non-fossorial animals. • Increased stability of shoulder girdle: Features such as the fusion of some vertebrae, and fused clavicles, make these skeletal regions less flexible and more stable. Animals that dig for a living, and even animals who dig secondarily (e.g., dogs, bears), require increased power to the forelimbs. This requires modifications to the shoulder girdle, arms, and hands that are almost the opposite of cursorial animals, and dissimilar to arboreal animals as well. Nothing in evolution happens without a trade-off; those adaptations that increase stability, power, and muscle efficiency result in a decrease in both flexibility and speed. One small mammal that is totally reliant on a digging lifestyle is the mole, and it is a good model in which to establish fossorial characters. Moles have bodies that are small and compact. Their necks are short and compressed, and their tails are also short. Because they spend a lot of time underground, their eyes are small and their vision is reduced, but their senses of smell and touch are increased. The shoulder anatomy of a mole can be seen in Figure 13.23. It is immediately apparent that the scapula is greatly elongated relative to less specialized organisms, to accommodate the huge muscles that work the arms. The clavicles (collarbones) are fused to hold the arms and shoulders stable, and these bones are also robust and reinforced compared with non-digging animals. In addition, the humerus of the mole is greatly expanded, with bumps and ridges for the insertion of powerful muscles (Figure 13.23C). In fact, it is so broad and flat it is hard to recognize as a long bone! The muscles of the arm and chest (e.g., deltoid and pectoralis) work the arm in a digging motion, and the expansion on the humerus for a large muscle insertion shows how powerful these muscles are. Furthermore, the bony

Figure 13.23  The skeleton of a mole, showing adaptations for digging, in (A) dorsal and (B) lateral views. The

scapula (*) is elongated above the vertebral column to provide more leverage for muscles that move the arm. The hands of the mole are greatly enlarged and oriented outward for more efficient digging. The olecranon process (elbow) is also enlarged (arrow), permitting the mass of the extensor muscles to increase. (C) The humerus has a greatly expanded surface area and attachment sites for muscles. (A and B courtesy of D. Descouens, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=12​ 77619​4; C courtesy of A.H. Harris.)

318

CHAPTER 13    How Do We Know How Dinosaurs Moved?

ridge where the muscle attaches extends more than halfway down the shaft of the bone. These features are the opposite of what is seen in cursors, where the muscle moves closer to the joint for speed. In fossorial animals, the insertion point for these muscles moves distal from the joint, conferring greater power. Although the most obvious adaptations for digging would be expected in the arms and shoulders (because these actually do the digging), the pelvic girdle must also adapt to keep the animal stable. Figure 13.24 shows a giant ground sloth, a large, herbivorous mammal from the Eocene (56–34 Mya) that originated in South America and ranged throughout the Americas. Its skeletal anatomy, including very robust limbs, muscle attachments far distal to the joints, and limited range of motion in the shoulders and hips, has led to the proposal that this animal was fossorial in its habits. Let’s apply these principles to dinosaurs. Once again, we must take into account that the ancestral state for dinosaurs is cursorial and bipedal. Bipedality is important because, as mentioned above, it allows the forelimbs to be adapted to multiple functions (e.g., flying or digging) while maintaining adaptations for speed in the hindlimbs. It is pretty obvious that the T. rex was not digging with its forearms—its nose would hit the ground before his arms could reach it! But many dinosaurs had very long arms that would facilitate both climbing/flying or digging. Recently, a small hypsilophodontid dinosaur was found whose skeleton showed many adaptations for digging (Figure 13.25). It had a large and broad snout, as seen in some animals today who use their snouts to loosen dirt or push it out of the way. The scapula of this dinosaur, Oryctodromeus, was robust when compared with other closely related dinosaurs. It was also fused to other bones of the shoulder girdle, and possessed a large Figure 13.24  Skeleton of a Megatherium (giant ground sloth).

Features consistent with a fossorial lifestyle in the forelimbs include massive hands and claws, robust arms with expanded olecranon processes (elbows), and a robust scapula with deep ridges for muscle attachment. Other features include a greatly expanded pelvic girdle for stability, greatly expanded femora, and plantigrade foot posture with massive digits. (Courtesy of Ballista, https​://co​mmons​.wiki​media​.org/​w/ ind​ex.ph​p?cur​id=13​34460​.)

13.5  Jumping: Adaptations for Saltatorial Locomotion

319

Figure 13.25  Oryctodromeus skeleton (A) and flesh reconstruction (B). This

dinosaur is hypothesized to have been fossorial. (Courtesy of T. Evanston, https:// flic.kr/p/HRvVYJ & https://flic.kr/p/HRvWVo.)

spine that would have provided a greater surface for muscles to attach. The scapula is also bent, and when this occurs in living animals like the digging armadillo, it acts like a lever to make the muscles more efficient, contracting the arm more powerfully. Further, it has a large crest or ridge on the humerus, for the insertion of deltoid muscles larger and more powerful than seen in humans, for example. It also shows modifications to the pelvis that would increase stability, such as the fusion of some of the vertebrae and expansion of the sacral region. What was most surprising though, was not only that the skeletal features hinted at a fossorial lifestyle, but also that its bones were found at the end of a structure that has been interpreted to be a burrow. The bones of two smaller Oryctodromeus skeletons were also found near the adult skeleton. It appears that this little dinosaur had dug a tunnel for itself, dug out an expanded “cave”, and died there with its babies. Thus, in this case, the skeletal adaptations and the other features of its environment allowed us to say that at least this one little dinosaur was most likely fossorial.

13.5 JUMPING: ADAPTATIONS FOR SALTATORIAL LOCOMOTION After reading this section you should be able to… • Discuss the skeletal adaptations of saltatorial locomotors.

Saltatorial animals—those whose main mode of locomotion is hopping or jumping—aren’t very common, but they have some very unique and distinctive skeletal adaptations. This is because this modality involves constant, jarring impacts with the ground, and consequently, applies constant stress to the back, pelvis, hips, feet, and neck—not to mention the brain! To account for these stresses, extant animals that jump for a living (e.g., frogs, kangaroos, and rabbits (lagomorphs)—show certain features in common. Saltatorial skeletal adaptations include: • Toe and foot bones are elongated: To increase the surface area of the foot with which to push off the ground. • Bones of the foot and ankles are fused: To increase stability for impact. • Plantigrade foot posture: Maximizes the surface area of the foot in contact with the ground. • Hindlimbs are elongated relative to forelimbs: They can sometimes be over twice the length of the forelimbs. • Enlarged, stabilized pelvis: Provides increased stability for the impact of feet against the ground.

320

CHAPTER 13    How Do We Know How Dinosaurs Moved?

First, like cursorial animals, saltatorial animals may show elongation of toe and foot bones. However, unlike cursors, which show a reduction in their number of toes, animals adapted for jumping sometimes show fused bones of the feet. Additionally, rather than digitigrade or unguligrade foot posture, jumping mammals are usually plantigrade, with heels that contact the ground. This gives them more surface area against which to push off the ground. Interestingly, this is not true in hopping birds. The hind limbs of saltatorial animals are also two to four times the length of their front limbs, with fused ankles to keep them stable. Jumping animals, like fossorial animals, also have very large and stable hip structures, but instead of being widened, the entire pelvis of saltatorial animals is elongated, and is sometimes fused. The vertebrae that are part of the pelvis may also be fused together for added stability. Two living animals that show saltatorial adaptations are rabbits and kangaroos (Figure 13.26). They are only distantly related, diverging from a common ancestor perhaps as long ago as the Jurassic (the kangaroo is a marsupial and the rabbit is a placental mammal), they nevertheless share some convergent features because of their similar lifestyles. Both have a highly curved spine, fused, elongate pelvis, elongated plantigrade feet, and shortened necks. Perhaps the most striking saltatorial adaptations are observed in the skull, and in the skulls of rabbits in particular. Removed from the rest of the body, the skull of the rabbit does not look much different from the skull of a rodent (Figure 13.27): they both have very large front teeth that are procumbent (i.e., stick out, like “buck teeth”). But the rabbit has two very distinctive features that are clearly adaptations for shock absorbance. First, the rabbit has very open, lacy sinuses in the skull. In life, these spaces are filled with fluid, so that the jarring forces experienced by the skull during locomotion are dissipated efficiently. Second, Figure 13.26  Skeletons of (A) a resting rabbit and (B) a leaping kangaroo, showing features common in saltatorial animals, including hindlimbs much longer than forelimbs, fusion of some bones in the foot, and a plantigrade foot posture. Saltatorial animals also often have

shortened necks with robust, reinforced vertebrae. (Courtesy of K. Tiffany, A photographed at the Field Museum; B photographed at the North Carolina State University Veterinary School.)

Figure 13.27  (A) Skull and (B) upper jaw of a rabbit. Saltatorial animals

sometimes have modifications to their skull that aid in their jumping lifestyle, such as fluid-filled sinuses that act to cushion their brains (A, arrow). In this little rabbit, another adaptation can be seen. Behind the protruding front “buck” teeth of the upper jaw is a second set of simple, peg-like flattened teeth (B, arrow). This second row of teeth prevents the bottom teeth from breaking—or piercing the mouth—during a forceful landing. (Courtesy of K. Tiffany.)

13.7  What We Don’t Know

although both rabbits and rodents have procumbent teeth, making them superficially similar and reflecting their recent common ancestrym, behind those two large front teeth in rabbits are two very small, peg-like teeth. These are shorter and simpler than the teeth in front of them, and their only function is to act as “brakes”, preventing the lower teeth from slamming into the upper front teeth and breaking them, and also serving to reduce shock experienced by the brain. As a result, even without any of the rest of the body, just by looking at a rabbit skull, we can recognize these saltatorial features. Have any of these saltatorial specializations been found in dinosaurs? So far, no non-avian dinosaur has been found to exhibit these traits. In fact, the anatomy and footprints of all archosaurs indicate that saltation did not evolve until modern birds. However, if we do not understand the features associated with saltation in living animals, we will not be able to recognize what we are looking at, should we ever find an extinct animal that was saltatorial.

13.6 DINOSAUR BIOMECHANICS After reading this section you should be able to… • Discuss the limitations in estimating dinosaur biomechanics.

To be able to say anything about dinosaur lifestyles requires a thorough knowledge of the biomechanics of living organisms and the careful study of skeletal correlations with certain behaviors. However, there are caveats to the general principles presented in this chapter. As discussed in various places above, most of what we can observe of cursorial animals today are quadrupedal mammals, whereas most dinosaur cursors would have been bipedal archosaurs. A bipedal stance greatly affects muscle insertions and the stresses and strain on bone. The best living analog to this is the only living fast, bipedal and cursorial dinosaur—the ostrich. But although bipedal, an adult ostrich weighs under 300 lbs., which is hardly comparable with (for example) an adult T. rex, estimated to weigh 7–8 tons. Even so, an ostrich is probably a better model for cursorial dinosaur movement than any mammal. Another factor to consider in estimating dinosaur biomechanics is the difference between ectothermic and endothermic muscle. Ectothermic muscles can generate greater power than endothermic muscles, but they cannot maintain this for long periods of time. When stress is applied to bones over short periods of time, it affects bones differently than when the stress is constant and long-lived. In short, many principles we use to interpret the abilities and behavior of dinosaurs are derived from mammals, because, in today’s world, mammals inhabit the niches that were once reserved for dinosaurs. Although mammals and dinosaurs are not directly comparable, traits used to interpret behavior may be convergent, so we can proceed—with caution.

13.7 WHAT WE DON’T KNOW 13.7.1 What Exactly Did T. rex Do with Its Tiny Arms? The arm of a T. rex was short for the overall size of a dinosaur. The length of the forelimb was approximately the same as that of a human arm and hand, but humans are not 40 feet long and 7 tons! The T. rex arm was relatively robust, and it had scars on the bone indicating that the biceps inserted more distal to the shoulder joint than do those of humans. This supports the powerful muscle action on the bone. Biomechanical princi-

321

322

CHAPTER 13    How Do We Know How Dinosaurs Moved?

ples applied to the arm estimate that it was quite strong, able to deadlift several hundred pounds. Suggestions for uses have included grasping a mate during copulation, helping the animal rise from a resting position, holding struggling prey, or as weapons to slash prey. Questions to consider: • The abelisaurid theropods like Carnotaurus had the shortest forelimbs of all the large carnivorous dinosaurs, and it has been proposed that their arms were vestigial (structures that are retained but have lost their function). Were T. rex arms also vestigial? • What fossil evidence could we find to provide conclusive evidence for how T. rex may have used its arms? Can the fossil record even be used to test all the hypotheses put forward? Why or why not?

13.7.2 Speaking of Theropod Arms, What Did the Herbivorous Therizinosaurs Do with the Giant Claws (Up to Three Feet Long and the Longest Known from Any Animal!) on the Ends of Their Hands? The Therizinosaurs were a group of bipedal, herbivorous theropods that had large claws on the ends of their hands (see Chapter 19). The idea of a large plant-eating animal having the largest claws known from any animal raises the obvious question of what were they using these giant claws for if not to kill or injure prey? Many ideas have been put forth and tested, including to dig for colonial insects or roots, stripping bark off trees, raking in vegetation to eat, defense, or sexual selection. Questions to consider: • Therizinosaurus, the largest therizinosaur, is only known from fragmentary limb bones, what could finding a more complete specimen tell us about the biology of this bizarre creature? • Were Therizinosaurs with smaller claws using them the same way as those with larger claws? It’s been suggested that the larger claws would not withstand the stresses of a fossorial function, but maybe those like Alxasaurus with smaller claws did use them for digging.

CHAPTER ACKNOWLEDGMENTS We thank Dr. John Hutchinson for his generous review and suggested improvements to this chapter. Dr. Hutchinson is a Professor of Evolutionary Biomechanics at the Royal Veterinary College of the University of London.

LITERATURE Alexander, R. M. (2006). Dinosaur biomechanics. Proceedings of the Royal Society. Series B: Biological Sciences, 273(1596), 1849–1855. Bishop, P. J., Clemente, C. J., Weems, R. E., Graham, D. F., Lamas, L. P., Hutchinson, J. R., Rubenson, J., Wilson, R. S., Hocknull, S. A., Barrett, R. S., and Lloyd, D. G. (2017). Using step width to compare locomotor biomechanics between extinct, non-avian theropod dinosaurs and modern obligate bipeds. Journal of the Royal Society Interface, 14(132), 20170276.

Bishop, P. J., Graham, D. F., Lamas, L. P., Hutchinson, J. R., Rubenson, J., Hancock, J. A., Wilson, R. S., Hocknull, S. A., Barrett, R. S., Lloyd, D. G., and Clemente, C. J. (2018). The influence of speed and size on avian terrestrial locomotor biomechanics: Predicting locomotion in extinct theropod dinosaurs. PLoS One, 13(2), e0192172. Hutchinson, J. R., Bates, K. T., Molnar, J., Allen, V., and Makovicky, P. J. (2011). A computational analysis of limb and body dimensions in Tyrannosaurus rex with implications for locomotion, ontogeny, and growth. PLoS One, 6(10), e26037.

13.7  What We Don’t Know Lautenschlager, S. (2014). Morphological and functional diversity in therizinosaur claws and the implications for theropod claw evolution. Proceedings of the Royal Society. Series B,: Biological Sciences, 281(1785), 20140497.

323

Varricchio, D. J., Martin, A. J., and Katsura, Y. (2007). First trace and body fossil evidence of a burrowing, denning dinosaur. Proceedings of the Royal Society. Series B: Biological Sciences, 274(1616), 1361–1368.

14 14

HOW DO WE KNOW WHAT DINOSAURS LOOKED LIKE? DINOSAUR APPEARANCE

P

icture a Tyrannosaurus rex in your mind. Now picture a Triceratops. Now picture a Stegosaurus.

Chances are, you immediately pictured an animal like this (Figure 14.1), with flesh on their bodies, perhaps even moving around, rather than the skeletons mounted on metal rods like the ones you’ve seen at a museum. But non-avian dinosaurs are extinct, and the pictures we see in our minds are certainly not based upon human experiences with them, as humans did not arrive on the scene for 65 million years after the last non-avian dinosaur walked the Earth! So, when you see an image like Figure 14.1, or a movie like Jurassic Park, those are based upon artistic reconstructions of what we think dinosaurs looked like. But how do we know?

14.1 RECONSTRUCTING DINOSAUR APPEARANCE After reading this section you should be able to… • Explain how bone is used to reconstruct dinosaur appearance. • Discuss some of the constraints in reconstructing dinosaur appearance accurately.

Except in rare circumstances, bones and teeth are all that remain of most extinct dinosaurs. However, this is never how living animals appear! The bones of living animals are never exposed to air; they are covered with muscles, tendons, and ligaments. Bones support and protect organs such as brains, hearts, and guts, but bone is ultimately covered by the integument (skin) and structures derived from it, such as beaks, hooves, horns, and claws. How, then, can we use just bones, preserved as fossils, to determine what the overall size, shape, and function of the living animal might have been? Furthermore, very often, the bones used for these reconstructions are either not complete enough to make

IN THIS CHAPTER . . . 14.1 RECONSTRUCTING DINOSAUR APPEARANCE 14.2 SKIN 14.3 SAILS, PLATES, AND ARMOR: DINOSAUR ORNAMENTATION 14.4 COLORS AND COLOR PATTERNS 14.5 WHAT WE DON’T KNOW

326

CHAPTER 14    How Do We Know What Dinosaurs Looked Like?

Figure 14.1  When most people think about dinosaurs, they probably think of them as fleshed in, threedimensional animals like this reconstruction of Daspletosaurus—not as a pile of bones. Yet, a pile of bones is

usually what we find in the fossil record. So how can we know what dinosaurs looked like in real life? (Courtesy of Steveoc 86, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=48​83573​2.)

a whole skeleton, or they are composites from many individuals. Are we just making it all up from our wildest imaginations? Just how accurate are the depictions, and how accurate can we make them? To reconstruct what a dinosaur looked like, we work from the inside out, starting with the principles outlined in the previous chapter. As we discussed, bone is a responsive tissue, and if a muscle is attached to bone during life, it leaves a mark in the living tissue. Moreover, the shape of the bone is both phylogenetically (derived from an ancestor) and functionally constrained by the forces of those muscles acting on it (for an in-depth review, see Chapter 13). Thus, just as to reconstruct their movements, to reconstruct dinosaur appearance, we need the scars and markings remaining on the bone. For example, living crocodiles possess a large muscle in their hind end called the caudofemoralis longus (caudo = “tail”, femoralis = femur; the name tells you where it is). It originates on the tail (the transverse processes of caudal vertebrae) and inserts on the fourth trochanter that you should recognize as being a synapomorphy of Archosauria. In living crocodiles, the caudofemoralis is critical to pulling the leg back as they walk (Figure 14.2). Dinosaurs had both a fourth trochanter and transverse processes on their tail vertebrae, so from these data, we concluded that it is likely they possessed this muscle. If so, then they might have had bigger rear ends than we usually depict them with! However, in maniraptorans and more derived dinosaurs, indicators for this muscle

Figure 14.2  The arrow points to the caudofemoralis muscle in a caiman.

This muscle inserts on the fourth trochanter (the presence of which is a synapomorphy of Archosauria), and acts to move the tail and retract the leg when walking. (Courtesy of S. Persons.)

14.1  Reconstructing Dinosaur Appearance

327

begin to diminish until they are mere traces on the bones. In fact, it has been proposed that until this extreme reduction happened, flight could not have originated. Perhaps most dinosaurs had big behinds, but small dromaeosaurs possessed slender hips and gracile tails! The above example sounds pretty straightforward, but there is a lot of uncertainty inherent in these types of investigations. For example, it is possible that dinosaurs may have had new or modified muscle groups. But is this a testable hypothesis? And what would you need to test it? Additionally, the size of their muscles may have been constrained by their physiology; were dinosaurs warm-blooded, or cold (Chapter 18)? Understanding these basic characteristics impacts the accuracy of our reconstructions, as do other factors discussed below. So, when reconstructing a dinosaur, what model do we use? Lizards? Crocodiles? Birds? Mammals? Placing our dinosaurs within the extant phylogenetic bracket (EPB, Chapter 4), we can use features shared by crocodiles and birds and infer what they might have looked like, but then again, crocodiles are all quadrupedal, and employ a splayed posture, whereas dinosaurs were all upright, and comprised members that were both quadrupedal and bipedal. Birds are all bipedal, but the constraints of flight operate on the shape and placement of muscles in their upper bodies, and might not apply directly as models for the vast majority of dinosaurs that didn’t fly. Furthermore, most dinosaurs were far more massive than any model we might choose among living animals. It is clear, then, that we must employ an approach that incorporates skeletal features, the EPB, and physics for the best estimates—relying solely on any one introduces many biases. For example, early dinosaur workers, certain that these dinosaurs were “reptiles”, reconstructed them with features such as a quadrupedal stance, splayed posture, and/or dragging tails (Figure 14.3), because that best fit their image of what a large reptile should look like. We know now that such poses were virtually impossible for dinosaurs to hold. Nevertheless, even with all data now available, all of our reconstructions, at best, are estimates, regardless of how realistic they may seem. The methods we use to reconstruct dinosaurs are not that much different from those used by forensic artists who try to reconstruct the faces of

Figure 14.3  This early reconstruction of two Edmontosaurus specimens stopping for a drink shows them dragging their tails and walking more like a human than a dinosaur.

Reconstructing them like this did not take into account modern biomechanical studies, but reveals the early biases of the scientific community when dinosaurs were first being studied. (Artwork by Charles R. Knight.)

328

CHAPTER 14    How Do We Know What Dinosaurs Looked Like?

murder victims or long-dead remains. Often, they begin with only bones as well (although they do have living humans to use as models), and depending on the mode of death, these skulls may be missing pieces. Features on the bones can be associated with biological parameters such as age-at-death, sex, and ancestry. By knowing general anatomy, they can fill in the gaps with an understanding of how bones of whole crania (a skull without the lower jaw) fit together. The artists use this biological information, estimated by forensic anthropologists or bioarcheologists, to develop a rendering in either ink or a three-dimensional clay model of what this individual may have looked like in life. In the past, forensics artists would place tissue markers on the landmarks, then use clay to lay the muscles of the right depth to the skull, followed by an overlay with a covering resembling skin. Now, however, scientists can do this digitally (Figure 14.4). It isn’t possible to know the exact shade of eye or skin or hair color, but nose shape, the width of the mouth, and eye placement in the socket can be estimated using averages drawn from cadaver studies or scans of living humans. As seen in Figure 14.4, it gives a good estimate of overall features from a starting point of only bones. We use the same principles to reconstruct what dinosaurs may have looked like. For example, the very first complete arm of a Tyrannosaurus rex was found in 1991 by paleontologists at the Museum of the Rockies, allowing an accurate reconstruction to be made. The first step was to make a scientifically precise model of the arm and shoulder bones from the original specimen (Figure 14.5A). Using the muscle scars preserved Figure 14.4  This series of images shows the progression of digitally reconstructing a human face, beginning with the skull. The skull has

certain bony features that allow placement of muscles and estimates of tissue depth, along with indications of some ethnic features. Once the reconstructed muscles are in place, skin and other external features can be added to provide a realistic reconstruction. (Courtesy of C. Moraes, https://en.wikipedia.org/wiki/File:Fore​nsic_​ facia​l_rec​onstr​uctio​n_of_​Alber​to_di​_Tren​ to.jp​g.)

14.1  Reconstructing Dinosaur Appearance

329

Figure 14.5  (A) Cast of the first complete T. rex arm ever recovered. (B) Using the muscle scars on the bone, paleoartist Matt Smith was able to reconstruct the deep muscles of the arm. (C, D) More superficial muscles of the arm and shoulder were added next, allowing calculation of the power these muscles could generate to move the arm and elbow. (E) When the arms were put in context with the rest of the skeleton, we learned that the only part of the arm that protruded from the body was from the elbow distally, making the already ridiculously short arm proportionately even shorter functionally. The two fingers of the hands

on the bones and a thorough knowledge of anatomy, paleoartist Matt Smith proceeded in the same manner as the human forensic reconstructions above. First, he used muscle scars to place the deep muscles (Figure 14.5B) then overlaid the more superficial muscles (Figure 14.5 C, D). This reconstruction allowed a more accurate calculation of the biomechanics of the arm. Although certain features had been previously hypothesized for a T. rex arm based upon the anatomy of close relatives, this was the first complete arm that could provide accurate anatomy. The arm reconstructed from these bones didn’t look that much different from what we had modeled previously, but there were some key differences. In particular, we learned that the little bitty arm was pretty powerful! Additionally, the reconstruction showed that the elbow joint had only about a 30o arc of movement. Finally, it showed that the humerus was mostly contained within the body, further restricting movement (Figure 14.5E). Thus, although the arm was estimated to be quite powerful, T. rex couldn’t touch its arms together, couldn’t pick its nose, and certainly couldn’t use the arms to wrestle prey.

would not be able to touch, making it even more confusing when trying to determine exactly what function the small, but powerful arms provided in the living animal. (Courtesy of Matt Smith.)

What role does the soft tissue normally covering bones play in reconstructing the appearance of dinosaurs? Soft tissues can utterly change the interpretation of an animal. For example, look at the dog’s skull in Figure 14.6 compared with the fleshed-in version. Would you have given this dog a soft bulbous nose, or the floppy ears that give it character based upon only features in the bony skull?

Figure 14.6  (A) The skull of a golden retriever compared with (B) a living golden retriever. This illustrates how we

need more than bone to determine the exact physical appearance of any animal. (A adapted from Wagner Souza e Silva, https​://co​mmons​.wiki​media​.org/​w/ind​ ex.ph​p?cur​id=72​18387​6; B adapted from Newyorker10021, https​://co​mmons​.wiki​ media​.org/​w/ind​ex.ph​p?cur​id=35​26655​7.)

330

CHAPTER 14    How Do We Know What Dinosaurs Looked Like?

Figure 14.7  Alligator (A) skull and (B) fleshed head. Unlike the golden retriever

above, there is very little difference in shape between the skull alone and the head when it is covered in flesh. Archosaurs in general have relatively few facial muscles and are incapable of “expression”. It is almost certain that dinosaurs shared this trait, emphasizing the need for understanding phylogenetic relationships in dinosaur reconstructions. (Courtesy of K. Tiffany; skull from the specimen collection of A. Heartstone-Rose.)

Figure 14.8  (A) Skull and (B) flesh reconstruction of the saurischian Allosaurus. (C) Skull and (D) flesh reconstruction of the ornithischian Parasaurolophus. In both cases, the

overall shape of the flesh reconstruction is not as different from the skull, unlike the golden retriever (or most other mammals). Note that Parasaurolophus is reconstructed with cheeks, but Allosaurus is not (see Chapter 15). When reconstructing a dinosaur in flesh and skin from only bony evidence, these phylogenetic factors are important to consider for accuracy. (A adapted from Jebulon, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=11​ 82808​4; B courtesy of Jakub Hałun, https​:// co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=37​01234​; C and D courtesy of K. Tiffany, taken at the Field Museum.)

Phylogenetics, as well as bony features, are vital to “fleshing out” extinct animals. Mammals have extra fat and muscles in their faces, and these make their faces capable of a greater range of expression than either reptiles or birds. A dog can convey confusion, surprise, and other personality traits, but reptiles have little more than skin laying almost directly over the bones of their face. Thus, they are rather expressionless, and their skulls look almost the same without skin as with it. Comparing the skull of a crocodile with the fleshed-in version (Figure 14.7) does not show nearly as much difference as the dog skull and face in Figure 14.6. Even birds that have soft tissue structures like combs and waddles do not have much in the way of soft tissues in their face. Using the EPB, then, tells us that dinosaurs, like their closest living relatives, almost certainly had relatively few facial muscles. That gives a little more confidence to our reconstructions (Figure 14.8)—and a little bit less in the cartoons that depict dinosaurs with human expressions!

14.2 SKIN After reading this section you should be able to… • Describe how findings in the fossil record have informed reconstructions of dinosaur skin and outward appearance.

14.2  Skin

331

• Discuss the limitations of reconstructing a dinosaur appearance based on the fossil record.

The first thing you see when you look at another animal is their skin, and the structures that are derived from it, like hair, feathers, and scales. Similarly, the first thing we would see when looking out our Mesozoic windows into the backyard would be creatures with skin on! But skin is a soft tissue, and therefore would not be expected to persist into the fossil record, right? Intriguingly, skin has been found in association with many dinosaurs. Skin can be preserved as impressions (which, like a footprint, leaves a mark but no actual tissue), or as body skin—actual tissue preserved in three dimensions, directly associated with the body fossils. Skin and/or skin impressions are known from various groups of ornithischians, including psittacosaurs and centrosaurs within the marginocephalians, the armored thyreophorans, and ornithopods. Indeed, ornithischian dinosaur mummies with preserved skin all over the body are not unheard of. Figure 14.9 shows a spectacular example of body skin in an articulated and beautifully preserved Psittacosaurus from China. It is preserved with scales, but also tubercles, rounded bumps on the surface of an animal. Dark spots within the general skin background persist. Does this mean that this dinosaur was polka-dotted? We don’t know if this reflects compositional or structural differences in the skin during life, or some taphonomic process yet to be described. In addition to scale and skin patterns, the entire skeleton of this small, basal ceratopsian is surrounded by a body outline, telling us about the three-dimensional shape of the animal before the skin and muscle degraded! Surprisingly, this little dinosaur also possessed thin filaments arising from the tail, perhaps related to feathers. As you can imagine, there is much we can learn from specimens preserved in this manner, and it is rare—but not as rare as you might think—to find such spectacular specimens. A single specimen preserved like this gives us more information about the appearance and functions of the once-living animal than we can possibly know from even a thousand disarticulated bones.

Figure 14.9  A spectacularly wellpreserved Psittacosaurus specimen (A) is preserved with skin, filamentous structures, and evidence of the overall size and shape of the complete organism for the first time. It has been proposed that the filaments on the tail are closely related to feathers, but remember, this dinosaur is an ornithischian, and not closely related to birds! These data were used to reconstruct what the dinosaur may have looked like in life (B). We

know the skin was highly textured and punctuated with rounded tubercles. Even some of the original color patterns can be discerned. (A courtesy of Ghedoghedo, https://commons.wikimedia.org/wiki/ File:Psittacosaurus_mongoliensis.jpg; B courtesy of R. Nicholls, https://commons. wikimedia.org/wiki/File:Psittacosaurus_ model.jpg.)

332

CHAPTER 14    How Do We Know What Dinosaurs Looked Like?

Within Saurischia, body skin has been identified with sauropods (diplodocids and the macronarians Titanosaurus and Haestasaurus). Intriguingly, the scale patterns on skin recovered from these dinosaurs are highly varied. For example, many eggs and nests were recovered from a nesting ground in Argentina, and some of the eggs contained embryonic remains with skin! In these, scales vary greatly in size and pattern, depending on where on the body they are found. In some regions, scales form delicate rosette patterns (Figure 14.10), and in other areas, they are simple bumps or tubercles. Similar variation can be observed on the feet of birds today, with large scales on the anterior of the foot, some overlapping, whereas on the bottom of the feet, in contact with the ground, scales are small and simple. Among theropods, preserved skin is not as common, although scaly skin has been observed in patches on some specimens, again with scales that vary in size and shape. The ceratosaur Carnotaurus has been found with small regions of skin impressions, and some coelurosaurs have as well. Skin has been observed in patches on a specimen of Tyrannosaurus rex and other large theropods, and is usually located on the abdomen and/or legs. Some ornithomimids show evidence of preserved skin, but what is found most often with derived, small-bodied theropods is feathers. These feathers range in morphology from thin, filamentous structures arising from and outlining the dinosaur, to structures with all the recognizable features of avian flight feathers—such as a central rachis with branching barbs and barbules. Sometimes, these feathers preserve original visual patterns (or what we think might be original patterns). Sinosauropteryx, a tiny little dinosaur that shows amazing preservation (Figure 14.11), was found in China and first reported in 1995. This little individual was the first dinosaur to be found with identifiable structures derived from its skin, and it was proposed that these were related to feathers in birds. The importance of this one small fossil cannot be overstated. It had been predicted for decades, based on phylogenetic relationships, that some dinosaurs should have had feathers. With the discovery of Sinosauropteryx, we had a dinosaur that preserved what may have been the equivalent of feathers. If one looks closely at the tail of this baby dinosaur, it is clear that these feather-like structures are not preserved randomly, but as evenly spaced “clumps” or tufts spaced along the tail. From those data, it was proposed that these dinosaurs might have had striped tails! Immediately, an entire ecosystem and even behavioral patterns were Figure 14.10  Skin recovered from a sauropod embryo, imaged using transmitted light microscopy. This

image allows us to see the scale pattern of these embryonic sauropods in great detail. (Courtesy of L. Chiappe.)

14.3  Sails, Plates, and Armor: Dinosaur Ornamentation

proposed. This provided some wonderful dinosaur art (Figure 14.11B). It is not yet clear how accurate this portrayal would have been, but sites in China continue to produce an abundance of feathered theropods and birds, as well as many specimens of dinosaurs and other vertebrates with skin. This exceptional preservation has changed the way we think about and portray the appearance of many dinosaurian groups. Where skin is preserved in all these lineages, it is where feathers (at least in theropods) are not. This may be because in large animals, feathers (a more efficient means of heat retention than skin) are not needed for insulation, and were perhaps present only in very young dinosaurs (Chapter 18). This may also be dictated by taphonomy (Chapter 11), because feathered skin is usually thin and delicate relative to the scaly skin covering feet and toes. In any case, the preservation of skin or feathers in the theropod lineage can be used to suggest some interesting evolutionary patterns.

14.3 SAILS, PLATES, AND ARMOR: DINOSAUR ORNAMENTATION After reading this section you should be able to… • Identify examples of ornamentation in different groups of dinosaurs. • Explain how ornamentation differed within certain groups of dinosaurs.

In addition to skin and the patterns and structures associated with it, many groups of dinosaurs exhibit ornamentation, usually bony ornamentation, on the skull or elsewhere on the body. Many reasons have been proposed for why such ornamentation might have been selectively favored, and these were probably as varied as the ornamentation itself. In living animals, ornamentation can serve several functions: • Sexual dimorphism: That is, marked changes between males and females in a group. For example, male peacocks have extravagant tails, but females are rather plain in appearance. • Indicators of sexual maturity: These features do not appear until adulthood is attained, and typically signal the animal has reached the age at which it can start reproducing. • Species recognition: Closely related organisms that overlap in habitat/range often possess exaggerated ornamentation to identify “us vs. them”. If ornamentation arose for species recognition, when do you think they would appear in an animal’s ontogeny (developmental stage)? If used for indicators of sexual maturity, or sexual dimorphism, then what would you predict?

333

Figure 14.11  (A) Fossilized specimen of Sinosauropteryx prima, a hatchling compsognathid found in China. This tiny dinosaur was the first to be found with a filamentous, epidermally derived covering, proposed to consist of “protofeathers”. This hypothesis was debated, but the preservation of many different dinosaurs with feathers has confirmed this idea. (B) The dinosaur has been reconstructed with a striped tail because of apparent banding observed in the fossil. Intriguingly, other, larger specimens

of Sinosauropteryx do not show this banding. Is the pattern reflective of the original organism, or is it taphonomic? What are the implications of this observation? (A courtesy of Sam/Olai Ose/ Skjaervoy, https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=42​09411​; B courtesy of Dinoguy2, https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=58​57705​5.)

334

CHAPTER 14    How Do We Know What Dinosaurs Looked Like?

14.3.1 Ornithopods From the neck down, hadrosaurids (the duck-billed dinosaurs) look very similar. But there is wide variation in the crests and ridges in their skulls. These variants are important for determining relationships and can be the basis for assigning the dinosaurs possessing them to different taxa (Figure 14.12). This ornamentation has been proposed to serve many functions, from sound production mechanisms, to species identification, to sexual display. Just like the huge and colorful feathers of a peacock’s tail do not, at first glance, seem to confer an evolutionary advantage, so too the ornamentation on the heads of some dinosaurs may seem counterproductive. We know, however, that evolution doesn’t work that way, and that to be maintained in a population, these traits must have provided dinosaurs with advantages that outweigh not having them. Although sexual dimorphism has been proposed as an explanation for the varied head ornaments in hadrosaurids, dimorphism has not been conclusively demonstrated for ornithopods (see Chapter 17). In particular, there is a wide variety of ornamentation in hadrosaurs, and the type of ornament, as well as the bones that make them up, vary with phylogeny (Chapter 8). Lambeosaurines like Parasaurolophus, Hypacrosaurus, or Corythosaurus have elaborate crests, whereas saurolophines usually have only small projections or crests, or none at all, like Edmontosaurus, Maiasaurus, or Gryphosaurus.

14.3.2 Ceratopsians Ceratopsians have a variety of horn shapes and sizes on their heads, in addition to the massive frills formed from bones at the back of their skull. These vary in number, shape, and size in different groups, as does the presence, absence, and/or number of horn-like projections on the outer rims of the shield (Figure 14.13). These bony projections (or epioccipitals) can be rather small, as in Triceratops, or very large in other ceratopsians.

Figure 14.12  (A) Gryposaurus and (B) Parasaurolophus are both hadrosaurs, but Gryposaurus is a “crestless” saurolophine, and Parasaurolophus is a crested lambeosaurine. Their post-

cranial skeletons are extremely similar, but the skulls possess significant differences that aid in classification. (A adapted from R. Taylor, https://commons.wikimedia. org/wiki/File:Gryposaurus_incurvimanus. jpg; B adapted from A. Zienowicz, https:// commons.wikimedia.org/wiki/File:Muze​ um_Ew​olucj​i_PAN​_-_Pa​rasau​rolop​hus_w​ alker​i_(od​lew_s​zkiel​etu).​JPG.)​

14.3  Sails, Plates, and Armor: Dinosaur Ornamentation

335

Figure 14.13  Centrosaur Wendiceratops (A) compared with the chasmosaur Chasmosaurus belli (B). These animals differ in the size and

prominence of the nose horn (bigger in centrosaurs) and eye horns (bigger in chasmosaurs). Chasmosaurs also have a much larger frill, or bony shield. Both are found with openings in the frill, which lightens the skull, making them more maneuverable than if the mass of the skull had not been reduced in this way. It has been proposed that these frills are covered with a skin-like covering that may have been brightly colored. (Courtesy of D. Evans

Figure 14.14  These images represent a growth series for Triceratops, the most famous ceratopsian. The smallest

Furthermore, growth series studies confirm that the size, shape, and fusion of these bony protrusions change as the animal grows (Figure 14.14), as does the relative size and orientation of the horns. Intriguingly, the shields themselves are riddled with deep grooves, marking the location of blood vessels. Blood vessels on the surface of bones usually indicate that the bones had a covering in life, most likely keratin. We see this in the antlers of moose and deer, for example, which are covered in keratinous “velvet” as they first emerge. Although they eventually lose this covering, the vessel markings remain. In modern birds, keratinous structures like beaks and feathers are often brightly colored. Maybe, if the ceratopsian shields were covered in keratin, they could have been equally colored! In addition to the size and shape, these colors could have contributed to species recognition or dimorphism. We are not used to thinking of Triceratops with a bright red and yellow head, but it is not unreasonable to propose. However, because color expression is usually the result of many different pigments (see below), we have no way of knowing for sure what these colors may be. So far, there is no hard data to support or refute this hypothesis—it may indeed be an untestable one!

14.3.3 Sauropods Some sauropods exhibited scutes, or osteoderms (osteo = bone, derm = skin) in their skin. These bony plates were even found in embryonic

of these has a frill roughly the size of a dinner plate. As we move from the smallest to the largest, we observe the following changes: the small bones surrounding the frill are not fused to the frill until the dinosaur is about half grown. The nose horn changes in both size and orientation. In the smallest, the horn is not solidly fused to the rest of the skull, but rests as a small triangle on the nasals. As it grows, it points from anterior and horizontal to curving posterior. The eye horns also change, first curving up and back, then horizontal, and then pointing anterior and down. It is easy to understand how some of these might be assigned to separate species, if some were not shown to still be actively growing in histological studies. (Photographed by M. Schweitzer from specimens on display at the Museum of the Rockies (MOR), with permission. All specimens are MOR specimens except the smallest (top left) which is a UCMP specimen.)

and the Royal Ontario Museum © ROM.)

336

CHAPTER 14    How Do We Know What Dinosaurs Looked Like?

Figure 14.15  Life reconstruction of Shunosaurus, a sauropod that has been found with what appears to be spikes on its tail, or perhaps a small tail club. This sauropod also has

an unusually short neck (for a sauropod, that is). What might the presence of a tail club in this dinosaur mean? (Courtesy of Smokeybjb and Paleocolour, https​://co​ mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=74​18357​3.)

specimens preserved in eggs from Argentina When the animal dies and the skin degrades, these osteoderms remain and can be identified. Much like crocodile scutes, they can be highly vascular, or pitted, and may have functioned in thermoregulation, calcium storage, or maintaining homeostasis. In life they were covered in skin, and may have contributed to patterning in these dinosaurs. In addition, some sauropods may have had spines of varying sizes and shapes along their tail and/or over their backs. Recent finds suggest that some, such as Shunosaurus (Figure 14.15), may have possessed tail clubs or tail spikes, convergent with some thyreophorans!

14.3.4 Thyreophorans We have already mentioned (Chapter 8) that all members of this group had bony plates, spikes, or armor. In stegosaurs, these vertical plates or spikes are also marked with vascular grooves, similar to ceratopsians, it has been speculated that these grooves mean that the plates were covered with keratin. If so, they could also have been brightly colored. Imagine stegosaurs with hot pink plates along their spines! However, the other group of living archosaurs, the crocodiles, are not brightly colored. Rather, they are drab to blend into their environments. Currently, there is no data to support either of these hypotheses regarding coloration within thyreophorans, so both are within the realm of possibility. Recently, two exceptionally preserved, complete ankylosaurs were recovered that shed light on another aspect of the appearance of these dinosaurs (Figure 14.16). These discoveries confirm that the bony osteoderms for which this lineage is famous were covered with skin. However, they also show that the keratin sheaths covering some of their dermal spikes could have extended as much as 25% beyond the bone, expanding

Figure 14.16  This specimen of Borealopelta, a nodosaurid recovered intact from oil sands in Alberta, Canada. It is preserved in three dimensions,

and skin has been described for this specimen, preserved as polygonal scales on the forelimb and elsewhere. (Courtesy of C.M. Brown, https​://co​mmons​.wiki​media​ .org/​w/ind​ex.ph​p?cur​id=64​45944​0.)

14.3  Sails, Plates, and Armor: Dinosaur Ornamentation

337

their functional size greatly. Think of a horn on a rhinoceros. No matter how big the bony nose protrusion on their skull is, the keratinous horn that rises from it makes the entire structure bigger. The same is true of the bone bearing your cat or parrot’s claws—the bone is small, but the claw itself is longer and sharper. Such keratinous sheaths on the bony spikes of ankylosaurs would certainly change the appearance of these dinosaurs, and again shows the value of exceptionally preserved fossils to our understanding of dinosaur appearance.

14.3.5 Theropods We know that many theropods exhibited bony ornamentation. Remember Spinosaurus, with the sail-like bony expansions on their back (Chapter 9)? Those neural spines were most certainly covered with skin. Could they have been colored in a way to make them larger and more threatening? That is purely speculation, of course, and no evidence for this exists. But as discussed above, their avian descendants are often brightly colored, as opposed to the drab colors of crocodiles, so it isn’t unreasonable to propose. However, spinosaurs were not the only theropods that possibly had showy, perhaps colorful features. Some theropods displayed cranial ornamentation. This was not as extensive as in the previously discussed ornithischians, but the presence of these features would certainly change the appearance of these dinosaurs. Dilophosaurus, a basal Jurassic theropod, is known for its paired, parallel head crests. The function of these is still unknown, but they were too thin and fragile to serve as defensive structures, and most probably were used for display. Allosaurs had small, triangular horns over their eyes that look somewhat like “devil horns”, and ceratosaurs showed similar bony skull features consistent with horns or decorative ridges (Figure 14.17). The oviraptors, already known for their parenting skills (Chapter 17), are easily recognized by their large head crests. We don’t know exactly why so many theropods had these bony skull ornaments, but in 2016, researchers showed that these may be linked to body size in theropods, and that there was a size limit below which they could not form. Because all birds today fall well below that limit, this may partly explain the lack of bony head ornamentation in birds. Of course, bony skull ornaments might also be a nuisance when flying. Other, smaller theropods may well have possessed outlandish and (from our perspective) odd-looking ornamentation. But if these ornaments Figure 14.17  (A) Fossilized skull elements from Ceratosaurus show odd growths and horns unusual for a theropod. These features have

led some to propose that at least some theropods also possessed ornamentation, although not as elaborate as some seen on ornithischians. Post-cranially (B), these dinosaurs are similar to other large theropods, but the cranial features have led to some creative ideas about how they fit in their own ecological niches (C). (A and B courtesy of J. Lallensack, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=61​ 33969​1, https​://co​mmons​.wiki​media​.org/​w/ ind​ex.ph​p?cur​id=63​78711​6; C courtesy of DiBgd, https​://co​mmons​.wiki​media​.org/​w/ ind​ex.ph​p?cur​id=24​43219​.)

338

CHAPTER 14    How Do We Know What Dinosaurs Looked Like?

Figure 14.18  A turkey skull superimposed next to a mounted, feathered turkey. How many features

on the turkey head are likely to be retained in the fossil record? How might our interpretation of the biology and ecology of dinosaurs be affected by this taphonomic bias? (Courtesy of K. Tiffany.)

were not preserved in their bony skeletons, would we know? Remember that science must be conservative. We can speculate, but without hard data, that is what it must remain—great for movies, but not for science. We know, for example, that some dinosaurs had feathers (see Chapter 19), but what about soft and fleshy ornaments? Look at Figure 14.18. If you only ever had the skull of a turkey, would you ever reconstruct it with colorful skin and a long, squishy wattle? Does this support or eliminate the possibility of similar features on, for example, a Velociraptor? This would certainly change how we enjoy Jurassic Park, right? Are these dinosaurs less scary when made to look less like a cold, heartless, lizard-like creature and more like a not-so-smart turkey (Figure 14.19)? Although such soft tissue appendages have never been observed in theropod fossils, phylogenetics makes such proposals within the realm of possibility. And they do occasionally show up in artwork! In Chapters 8, 9, and 10, we described filamentous coverings and feathers as features we observe in various groups within Avemetatarsalia. However, whether these structures are homologous or convergent between pterosaurs, ornithischians like Psittacosaurus, and theropods is not currently resolved. We can say—based upon direct evidence and phylogeny—that many theropods were covered with feathers. Additionally, feathers have been proposed for Velociraptor based upon quill knobs, bony projections on the ulna similar to those seen on the ulna of many flying birds. These knobs represent insertion points for muscles controlling feathers in birds (see Figure 19.11), and may have served a similar function in non-flying dinosaurs, giving them the ability to spread feathers for display or to make them look larger. Most birds exhibit colored feathers, although some are completely black (like crows) or all white (like some terns). It may be that theropods with feathers, from the early Anchiornis to later oviraptors, had brightly colored feathers as well. These meat-eating beasts would be less threatening, perhaps, covered in soft fluffy down, as observed in Yutyrannus (Figure 14.20)! We ­discuss “true”

14.4  Colors and Color Patterns

339

Figure 14.19  Artists reconstruction of a maniraptoran dinosaur covered in feathers and with other fleshy ornamentation. (Courtesy of Luis Rey.)

Figure 14.20  An artistic reconstruction of Yutyrannus. Based upon the

preservation of imprints of feather-like structures, it was proposed that the entire dinosaur was covered in a thick, fuzzy coat. (Courtesy of Tomopteryx, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=50​ 60839​4.)

feathers further in Chapter 19, as well as the implications the presence of these structures has for both physiology and the onset of flight.

14.4 COLORS AND COLOR PATTERNS After reading this section you should be able to… • List the different uses of coloration in animals. • State the arguments for and against the preservation of melanosomes and their contribution to color. • Use examples of extant animals to discuss how dinosaurs may have made use of coloration.

A question that comes to mind every time someone is faced with the blank pages and empty outlines in a dinosaur coloring book is: What colors were they? Were they all shades of earth-tone greens and browns, or can I use my fuchsia and fluorescent green crayons? While you might think the bright orange and purple polka dots a child chooses to color their dinosaur drawing is fanciful imagination, living, avian dinosaurs come in a riot of colors and patterns (Figure 14.21). So are pink and aqua dinosaurs really that far of a reach? Or would a better model be the dull, boring browns and greens of living crocodiles?

340

CHAPTER 14    How Do We Know What Dinosaurs Looked Like?

Figure 14.21  Living birds that express a range of colors. If we could remove

the feathers, do you think the skin beneath would be similarly colored? Why or why not? (Courtesy of K. Tiffany.)

First, let’s discuss what functions colors serve in living animals, and what is possible vs. what is probable. Modern animals use coloration and color patterns for a wide variety of purposes and behaviors. Colors and color patterns are used for: • Camouflage: Enables organisms to blend into their environments to avoid detection by predators or, for ambush hunters, to hide from intended prey. • Warning: Signals to predators that a species is poisonous or otherwise inedible (without the predator needing to eat it to find out). • Sexual display: Used to attract mates. • Species recognition: Distinguishes between individuals of different species that are otherwise morphologically similar, much like complicated head ornamentation. Distinguishing potential mates through features linked to a particular species helps animals avoid wasting time and resources directing courtship rituals at individuals that are incompatible.

14.4.1 Camouflage Camouflage can be used in different ways among animal groups today— including among living dinosaurs, the birds—and this was probably true for dinosaurs as well. There are four basic types of camouflage employed by animals for different purposes, although there is some overlap. When camouflage coloring is employed to help an animal blend into its surroundings and environment, it’s called cryptic coloration. Many animals, particularly young ones, use crypsis to hide from predators, but is advantageous for predators as well. Birds like the snowy owl employ this strategy (Figure 14.22A). When animals are lighter on the bottom and darker on the top (to hide it from those looking up into the light or down

14.4  Colors and Color Patterns

341

Figure 14.22  Different types of camouflage employed by the closest living relatives of dinosaurs—the birds. (A) Cryptic coloration in a

at the earth or ocean depths) it’s called countershading (Figure 14.16B). When striking patterns are employed to break up the body outline of an animal, it’s called disruptive coloration. Zebras and giraffes are good mammalian examples, but birds do this as well, using dark and light feathers to blend the stark outlines of their body with surrounding foliage (Figure 14.22C). When color is used to make an animal look like a different (usually more threatening) species than it actually is, that’s called mimicry (Figure 14.22D, E). These types of uses of color and color patterns are broadly employed throughout the animal kingdom, from insects to octopi, frogs to lizards, and mammals to birds. Thus, it is likely that dinosaurs also used coloration in a similar manner for similar purposes—in fact, it would be truly bizarre if they didn’t! Many marine animals use countershading, including the penguin in Figure 14.16B. Baby sea turtles are another living example (Figure 14.23A). Sea turtles lay their eggs on land, bury them in the sand, and then abandon them. Once hatched, the babies have to make their way to the ocean by themselves. This journey is perilous, as they are easy prey for numerous predators. However, if they do make it to the ocean, they are not home free either, as many hungry fish and other predators await. Living sea turtles employ countershading, so that they blend in with the sunlit water when hungry marine predators look up, but for sea birds looking for a turtle dinner, they are hard to see when looking down against the dark ocean. A tiny fossil sea turtle recovered from Eocene (34–56 Mya) sediments in Germany appeared to exhibit countershading (Figure 14.23B). Because of its exceptional preservation, including soft tissues, this little turtle was examined for both chemical and morphological evidence of countershading by a team of scientists led by Johan Lindgren of Lund University in Sweden. Chemical evidence for melanin supported the idea that as far back as the Eocene, the animals employed this strategy. Furthermore, the melanin signal was detected only in certain regions of the fossil, consistent with countershading.

snowy owl. The feathers of this predator change to white in the winter, making it virtually invisible in the snow. (B) Countershading employed by many creatures inhabiting a marine ecosystem. The dark color on the back helps the penguin blend in with the dark waters, protecting them from attack from above. Their white bellies protect from predators below, which would find it hard to see against the lighter background of the sky. (C) A long-eared owl blends into its background using disruptive coloration. (D) The cuckoo bird is a brood parasite, laying its eggs in the nests of other birds, like this predatory sparrowhawk. The color patterns are very similar between these birds, allowing the cuckoo to go unrecognized when laying her eggs. (A adapted from K. Servant, https://commons.wikimedia.org/wiki/ File:Harf​ang_d​es_ne​iges_​-_Sno​wy_ow​l_(25​ 47828​9536)​.jpg;​B courtesy of L. Quinn, https​://co​mmons​.wiki​media​.org/​w/ind​ ex.ph​p?cur​id=15​68398​4; C courtesy of R. Silberman, https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=80​38912​7; D and E courtesy of C. Chap, https​://co​mmons​.wiki​ media​.org/​w/ind​ex.ph​p?cur​id=18​86126​9.)

342

CHAPTER 14    How Do We Know What Dinosaurs Looked Like?

Figure 14.23  Newly hatched sea turtle (top) shows countershading, with a dark dorsal surface and a white underbelly. This is dangerous for the baby

when making its way to the sea because it doesn’t blend in with the lighter sand. However, once in the water, the dark top is a protection from flying predators looking down at it in the ocean, and the white belly is camouflage for predators looking up at it (and the light) from below. This tiny fossil of a baby sea turtle, called Tasbacka danica, shows similar patterns that extend to the molecular level. (A courtesy of Wildlifeppl, https​://co​mmons​.wiki​media​.org/​w/ind​ ex.ph​p?cur​id=16​72778​7; B courtesy of R. Sylvestersen, https​://co​mmons​.wiki​media​ .org/​w/ind​ex.ph​p?cur​id=25​03295​8.)

So, what would countershading in a terrestrial dinosaur look like? And in what habitats might we be most likely to observe it? Countershading has been suggested for the exceptionally preserved thyreophoran Borealopelta (Figure 14.16). Could there be information related to the original color preserved as well? Patterns suggestive of color variation can also sometimes be seen in feather-like or filamentous integumentary structures, but we have to be very careful to consider taphonomy before drawing hard conclusions. Sometimes, individual feathers are preserved with patterns—stripes or patches of light and dark—and we can use these to suggest how patterns may have functioned or fit in larger ecosystems. But it is important to remember that such information will always be incomplete, and is based, to a certain degree, on untested assumptions. The little Sinosauropteryx specimen referred to above was depicted with a striped tail. This isn’t unreasonable because alternating tufts of dark filaments were preserved with this fossil (Figure 14.11). However, other, larger Sinosauropteryx specimens do not show this pattern so clearly. Is this the result of taphonomy? Or was this pattern present only in hatchlings, with the tail becoming more uniform in older animals? T. rex probably did not possess countershading, but if T. rex participated in ambush predation, it may have exhibited cryptic or disruptive coloration to allow it to remain hidden before lunging out to grab its unlucky prey (Figure 14.24A). If T. rex was primarily an active predator, concealment was probably not all that important, but perhaps they employed bright colors for display (Figure 14.24B). How do you think these patterns would change if T. rex were covered in downy feathers (Figure 14.24C)? Although there is some hard evidence for color patterns in some extinct species, whether these patterns, in life, were blue or gray or red or yellow is something we cannot say for certain. Colors in living birds are usually derived from more than one pigment, and these have different

14.4  Colors and Color Patterns

343

Figure 14.24  Representations of possible camouflage or color patterns in T. rex, based upon examples in birds. T. rex could have employed cryptic or disruptive coloration (A) to blend in with the environment and lie in wait for unsuspecting prey. If camouflage were not the goal, could they have employed bright color patterns (B), or were they more like crocodiles (C), which are uniformly drab? Would these patterns be different in

areas with feathers? Why or why not? (A courtesy of Ryanz720; B courtesy of Gunk 78; C courtesy of Durbed, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=37​ 15728​3.)

likelihoods for preservation. There is evidence that some pigments, such as melanin, may preserve in the rock record. In fact, it has been proposed that the durability of melanin pigments play a role in preserving the structures that contain it, providing resistance to degradation and supporting a possible mechanism for the preservation of normally labile tissues such as feathers and skin. But the extent to which preserved melanin can inform on the original color of dinosaurs is a subject of intense research and much controversy. Color in living animals is determined by biopigments. Compounds like carotenoids, melanin, heme, and other porphyrins confer most of the colors displayed in living animals. These chemicals have many other functions as well, and are so important that they arose very early in the history of life. For example, heme is the iron-based pigment that makes your blood red, but it has many other very important functions as well. Because the biopigment heme is found in virtually all living organisms, from bacteria to humans, we infer that it arose in the common ancestor of all these varied organisms—at the very dawn of life. Furthermore, melanin and heme pigments, at least, are very resistant to degradation, and chemical analyses show that these pigments can persist in rocks far older than those that contain dinosaur remains! But carotenoids, which include yellow, orange, and red pigments and are common in bird feathers, may not be as stable. Indeed, no unambiguous chemical evidence for carotenoid persistence in fossils has been demonstrated. Determining original color in dinosaur and other fossils has proceeded from speculation to data in only the last decade or so, and began with what may have been a misidentification (or not?). In 1995, researchers identified some fossil feathers in Tertiary deposits, and decided to study them using a scanning electron microscope. When they did, they saw

344

CHAPTER 14    How Do We Know What Dinosaurs Looked Like?

Figure 14.25  (A) Small bodies were originally identified as bacteria when first observed under scanning electron microscope (SEM) in 1995 (David and Briggs 1995). They covered the surface of this Eocene feather, and were proposed to provide a mechanism for feather preservation. Many fossil feathers showed this pattern. Compare the size, shape, and pattern of these bodies to a modern feather on which bacteria were purposely grown (B). The double-headed

arrow shows the thickness and continuity of the biofilm. The triple arrow indicates individual bacterial bodies, and “K” labels the keratin surface of feathers. (A courtesy of P. G. Davis and D. E. G. Briggs; B courtesy of A. Moyer et al.)

that overlying these feathers and covering the surface was a smooth mat of small oval microbodies (Figure 14.25A). Based upon the morphology of these small bodies, they proposed that they were the result of microbial overgrowth on these ancient feathers, and that their presence may have been why the feathers persisted long enough to fossilize. Bacteria secrete a slime called biofilm—you probably have felt it on your teeth when you wake up in the morning! It helps them adhere to the surfaces of organic material like decaying skin, feathers, or other materials. If you have ever picked up a feather that has floated in a pond for a while, you can see this slimy film. Biofilm is also rich in enzymes that help to break down the material they colonize, and is easily mineralized. When modern feathers that had been colonized by bacteria were observed under electron microscopy, a similar “flowing mat” of bacteria was also seen (Figure 14.25B). It was hypothesized that the slime these microbes produced in the process of degrading the feathers could become mineralized, and this mineralized “slime” would contribute to feather preservation by stabilizing the structures, increasing their resistance to further degradation. In other words, through mineralization, the microbes had “self-fossilized”, preserving the feather structure along with bacterial bodies in the process. This is a reasonable hypothesis because the biofilm of living microorganisms is negatively charged, so positively charged mineral ions from the environment deposit on the surfaces of the biofilm. That is why plaque on your teeth has to be scraped off; it is mineralized biofilm. Similar microbodies, which included both elongate and round morphologies, have been noted on the surfaces of many feathers and other structures in the fossil record. The hypothesis that bacteria could fossilize, and in the process preserve the materials they had colonized was testable, and it was subsequently shown in experiments that microbial bodies can indeed mineralize quite rapidly when they colonize some organic materials in the right environments. However, in 2008, over ten years after this original discovery, these small bodies were re-interpreted as melanosomes. Melanosomes are small intracellular organelles, about 1 µm in size (some can be smaller) and they can be round or oval, thus overlapping with microbes in both size and shape (Figure 14.26A, B). Melanosomes contain the pigment melanin, which contributes to the color of modern bird feathers as well as skin and other keratinous structures. Using the criteria of size and shape of either these small bodies, or depressions on the surface of fossils that are proposed to be remnants of them, it has been suggested that we can now distinguish colors in feathers preserved with dinosaurs and fossil birds, because in modern feathers, elongate melanosomes correlate to black or gray colors, whereas round melanosomes seem to impart dull orange, red, or rust colors. If these bodies were melanosomes, and not microbes, it appeared that at last we had a way to directly examine dinosaur color—at least the feathered ones! But, is shape enough to determine this? We had two

14.4  Colors and Color Patterns Figure 14.26  SEM images of round (A) and elongate (B) melanosomes associated with a keratin matrix in modern bird feathers. Fossil bird preserved with feathers (C) shows only impressions under SEM (D). No

bodies are seen. (Courtesy of Li et al.)

competing hypotheses based upon the same body of data: small, round, or oval microbodies in an amorphous matrix associated with degraded, originally organic matter. Were they pigment-containing melanosomes, or bacteria participating in degrading the fossil before burial? Which of these hypotheses best fits the data? So far, the hypotheses seem equally weighted. But here it gets complicated. Upon closer examination, in many cases where melanosomes were proposed to be present and associated with fossil materials, it was not microbodies preserved with ancient feathers, but often a homogenous layer containing “voids”, or melanosome/bacterial-shaped holes in this layer (Figure 14.26D). This was very comparable to biofilm, but didn’t rule out melanosomes (remember, taphonomy!). It became evident that microscopy alone was not sufficient to distinguish between melanosomes and microbes. These bodies may represent melanosomes, or microbes, or a mix of both in degrading organic remains. The only way to tell the difference is through the chemical identification of the melanin pigment, mapped to these bodies. That has only been done in a handful of fossils, and most of these are not feathers. Until chemistry sheds light on the identity of these bodies, there still remains a lot of uncertainty in determining color. Even if we are able to definitively identify melanosomes in fossils using chemical methods, this information does not tell us the expressed color of ancient organisms—that is, the color we’d actually see with our eyes, which is the sum total of all pigments in those tissues. Living animals, especially birds, use many different pigments in addition to melanin to produce expressed color. In addition to these pigments, they use structural color as well—the arrangement of tissues and air pockets that cause refraction. Additional pigments besides melanin, as well as structural colors, probably worked together to determine the final color of the organisms, just like they do today! Although they were probably present with melanin in living tissues, these other pigments may not survive

345

346

CHAPTER 14    How Do We Know What Dinosaurs Looked Like?

into the fossil record, because they are not as chemically robust. Thus, objective determination of the expressed color of dinosaurs is beyond our grasp, at least with current knowledge and technology. How would you test the melanosome-microbe hypotheses? If microbes, what should you see? If melanosomes, what would you predict? What is needed to support one conclusion over the other? Could both be right?

14.5 WHAT WE DON’T KNOW 14.5.1  So, What Did Dinosaurs Look Like? After reading this chapter, you should have an idea that determining the outward appearance of dinosaurs is not an easy task. But even many soft tissue structures that they may have possessed often don’t leave behind clues on the bones, making it difficult to predict their presence if these features don’t preserve in the fossil record. And even if we recover a frill, horn, or scute, we don’t know anything about the keratin that covered it in terms of color, size, and shape. Questions to consider: • What types of soft tissue structures may be missing from common reconstructions of currently known dinosaurs? • While there is currently no evidence for it, were non-avian dinosaurs sexually dimorphic based on color or soft tissue structures? • Did non-avian dinosaurs possess the diversity of photoreceptor cells that birds do today, allowing for an even greater diversity of colors that we can visually appreciate ourselves? • Will there ever be a conclusive way to determine the coloration of extinct dinosaurs?

14.5.2 What Role Did Feathers or Feather-Like Structures Play in Dinosaur Appearance? While we know that many avian dinosaurs had feathers, some non-avian dinosaurs like Psittacosaurus have been found with filamentous integuments. Pterosaurs have been found with integumentary structures called pycnofibers. If these pterosaur integuments are homologous to dinosaur filaments or protofeathers, it would make this feature ancestral in Avemetatarsalia and to all dinosaurs. Questions to consider: • What type of integument did the common ancestor of all dinosaurs possess? • How many dinosaur species possessed feathers? • Did featherless species (at least ones with no fossil evidence of feathers) possess feathers at a young age and then lose them?

CHAPTER ACKNOWLEDGMENTS We thank Jack Wilson, Jake Gardner, and Matt Smith for their generous reviews and suggested improvements to this chapter.

INSTITUTIONAL RESOURCES Witton, M. P. (2018). Palaeoartist's Handbook: Recreating Prehistoric Animals in Art. The Crowood Press, Ramsbury, UK.

14.5  What We Don’t Know

347

LITERATURE Brown, C. M. (2017). An exceptionally preserved armored dinosaur reveals the morphology and allometry of osteoderms and their horny epidermal coverings. PeerJ, 5, e4066. Davis, P. G., and Briggs, D. E. (1995). Fossilization of feathers. Geology, 23(9), 783–786. Gates, T. A., Organ, C., and Zanno, L. E. (2016). Bony cranial ornamentation linked to rapid evolution of gigantic theropod dinosaurs. Nature Communications, 7(1), 1–10. Horner, J. R., and Goodwin, M. B. (2006). Major cranial changes during Triceratops ontogeny. Proceedings of the Royal Society Series B: Biological Sciences, 273(1602), 2757–2761. Li, Q., Clarke, J. A., Gao, K. Q., Zhou, C. F., Meng, Q., Li, D., D’Alba, L., and Shawkey, M. D. (2014). Melanosome evolution indicates a key physiological shift within feathered dinosaurs. Nature, 507(7492), 350–353.

Moyer, A. E., Zheng, W., Johnson, E. A., Lamanna, M. C., Li, D. Q., Lacovara, K. J., and Schweitzer, M. H. (2014). Melanosomes or microbes: Testing an alternative hypothesis for the origin of microbodies in fossil feathers. Scientific Reports, 4(1), 1–9. Scannella, J. B., and Horner, J. R. (2010). Torosaurus Marsh, 1891, is Triceratops Marsh, 1889 (Ceratopsidae: Chasmosaurinae): Synonymy through ontogeny. Journal of Vertebrate Paleontology, 30(4), 1157–1168. Schweitzer, M. H., Chiappe, L., Garrido, A. C., Lowenstein, J. M., and Pincus, S. H. (2005). Molecular preservation in Late Cretaceous sauropod dinosaur eggshells. Proceedings of the Royal Society Series B: Biological Sciences, 272(1565), 775–784. Vinther, J., Nicholls, R., Lautenschlager, S., Pittman, M., Kaye, T. G., Rayfield, E., Mayr, G., and Cuthill, I. C. (2016). 3D camouflage in an ornithischian dinosaur. Current Biology: CB, 26(18), 2456–2462.

15 HOW DO WE KNOW WHAT DINOSAURS ATE?

15

DIRECT AND INDIRECT EVIDENCE FOR DINOSAUR DIETS

T

he world today is very different from the world of the dinosaurs, but one thing certainly hasn’t changed: animals have to eat! There are many different ways by which animals obtain nutrients to survive, and the same was true of dinosaurs. Thus, if our goal is to understand dinosaurs—how they lived and the world in which they lived—part of that is knowing what they ate, and how they obtained and processed their food. Eating must provide two things: energy to function, and nutrients. Not all foods eaten by an animal provide both. For example, deer sometimes gnaw on bones to supplement their calcium intake. Although chewing bones fulfills one of their nutritional requirements, as herbivores, their gut cannot process bone tissue to produce energy. Conversely, cats sometimes eat grass to aid in eliminating hairballs, or consume catnip as a treat, but these plants do not provide cats with either energy or nutritional value. You may already know that carnivores are animals that obtain their energy and nutrients primarily from meat (i.e., the tissues of other animals) and herbivores are those that obtain energy and nutrients mainly from plants. However, vertebrates today have a wide variety of diets beyond just “meat-eaters” and “plant-eaters”, with all kinds of specialized feeding strategies within these groups. Some examples of specialized carnivores include: • Piscivores: Carnivores that eat fish • Insectivores: Carnivores that eat insects • Vermivores: Carnivores specialized to eat worms • Hypercarnivores: Carnivores with diets that are almost exclusively meat-based Some examples of specialized herbivores include: • Frugivores: Herbivores that eat fruit • Folivores: Herbivores that eat leaves (foliage)

IN THIS CHAPTER . . . 15.1 CARNIVORY VS. HERBIVORY: ADVANTAGES AND DISADVANTAGES 15.2 INDIRECT EVIDENCE: TOOTH MORPHOLOGY 15.3 INDIRECT EVIDENCE: JAW SHAPE, MUSCULATURE, AND ARTICULATION 15.4 INDIRECT EVIDENCE: BONY CORRELATES OF CHEEKS 15.5 INDIRECT EVIDENCE FOR DIET: SKELETAL ANATOMY 15.6 INDIRECT EVIDENCE FOR DIET: FECES (COPROLITES) 15.7 CAUGHT IN THE ACT: DIRECT EVIDENCE FOR DIET 15.8 WHAT WE DON’T KNOW

350

CHAPTER 15    How Do We Know What Dinosaurs Ate?

• Granivores: Herbivores that eat seeds • Nectarivore: Herbivores that eat nectar • Browsers: Herbivores that feed on high-growing vegetation, like shrubs • Grazers: Herbivores that feed on low vegetation, like grasses Beyond these groups, animals can also be omnivores, meaning they have the ability to derive energy and nutrition from both plant and animal tissues. As stated above, many animals considered herbivores may occasionally consume animal tissue, and many carnivores may consume plants from time to time. It is the ability to process both sources for energy and nutrition, not just one or the other, that defines omnivores. If there is such wide variation among today’s living vertebrates, how can we possibly know what dinosaurs ate? Establishing the diet of animals that went extinct more than 65 million years ago is hardly straightforward, but using the principles we have already discussed, like extant phylogenetic bracketing (EPB, Chapter 4) and comparative anatomy, we can come to some robust conclusions about dinosaur diets. However, as we move forward, there’s a major caveat to keep in mind when making our inferences: most of our models are derived from observing mammals, which are, of course, very different from dinosaurs. When using these extant lineages for comparison, we should always keep in mind that it makes our inferences from indirect evidence a bit less certain.

15.1 CARNIVORY VS. HERBIVORY: ADVANTAGES AND DISADVANTAGES After reading this section you should be able to… • Compare the advantages and disadvantages of carnivory and herbivory.

First, let’s talk about the costs and benefits of carnivory and herbivory as feeding strategies. Much like metabolic strategies (Chapter 18) or parenting strategies (Chapter 17), there are distinct advantages and disadvantages associated with each. Carnivory: Advantages • Nutritive value: Meat has far more nutritional value per unit eaten than plants, so in terms of weight of food ingested, carnivory is a more efficient way to meet metabolic needs than herbivory. Additionally, in many cases, one kill can feed several individuals— many allosaurs could eat from a single titanosaur. These factors mean that a carnivore needs far less food to survive, proportionately, than animals consuming plants. • Less digestive processing: Compared with plants, digesting meat is relatively easy, and requires less energy to break down for absorption by the body. Thus, proportionally more calories can go toward building and maintaining body tissues, rather than processing food taken in. These are great advantages! So why aren’t all animals carnivores? There are obviously some big disadvantages to carnivory as well.

15.1  Carnivory vs. Herbivory: Advantages and Disadvantages

Carnivory: Disadvantages • Meat can be energetically expensive to catch: Carnivores face a high likelihood of their dinner running away. The amount of energy that a carnivore expends catching and killing its food can be steep, especially if the chase ends with the prey getting away! Not only has the predator expended a lot of energy, it has nothing to replace it with. The life of a carnivore is one that must balance the calories burned in the pursuit of its food with the calories that food ends up providing. The more active an animal is, the more important these considerations become. • Predation is dangerous for the predator, too: Racing after prey on uneven ground, in addition to the risk that prey will fight back, increases the likelihood of injury to carnivores. Even a relatively small injury, like one broken toe, can impact a predator’s ability to hunt, and potentially cause a lethal infection. • Meat is an unstable food supply: Finally, the food supply for a carnivore is not stable—because it depends on the food available to herbivores! For example, mammalian herbivores today often form large herds and migrate from place to place, and predators follow. If there is a drought or other environmental compromise, mobile animals can be hard to find, so predators relying on them also begin to die. Herbivory: Advantages • Plants don’t run away: If you’ve ever seen a herd of cows grazing in a field, you know that herbivores don’t have to expend that much physical energy to obtain their food. If animals don’t need to spend energy chasing food, they can use the calories they take in to grow and maintain tissues, compensating somewhat for the cost of processing their dinner. • Plants are plentiful: There are more plants than animals (usually) per unit area. When a herd consumes the plants in an area, they can move to a new area. Additionally, because plants usually recover relatively quickly from grazing, they can return to the same spot a few years later. Herbivory: Disadvantages • Plants are nutrient-poor: Plants provide far fewer calories and less nitrogen (which is required to build protein) per unit of intake than meat. Plant tissues also generally lack high levels of saturated fats, protein, and other essential nutrients required for biological functions in vertebrates. Because plants are less nutritious, much more plant material must be consumed to support an animal’s life processes than if they ate meat. Thus, although the animal might not have to waste energy catching its food, it spends an enormous portion of its time just taking in food. An elephant, for example, can spend ~80% of its day just eating. • Plants are hard to digest: In addition to not providing essential nutrients, some of the nutrients that are present are impossible for vertebrates to access. The cellulose that comprises the cell walls of plant tissues is extremely tough and takes a long time to break down into a useable form. Thus, many obligate herbivores have special adaptations to their gut to aid them in this process. • Plant availability may vary: Because plants are susceptible to climate variations, conditions like drought will affect both herbivores and the carnivores that prey on them.

351

352

CHAPTER 15    How Do We Know What Dinosaurs Ate?

Regardless of the advantages and challenges of herbivory, the multiple origins of this trait in dinosaurs suggest that the advantages of adopting this feeding strategy outweighed the disadvantages for several groups. But where in Dinosauria did it arrive? Here’s a question you may not have considered before: were the earliest dinosaurs carnivorous or herbivorous? It’s a common misconception that herbivores “come first” because they occupy a lower trophic level than carnivores. However, in terms of the evolutionary history of feeding strategies, in vertebrate lineages (including dinosaurs), carnivory is the ancestral state, and herbivory evolves later. Although the earliest members of Dinosauria that we have discovered are carnivorous, the fact that herbivory is present throughout the dinosaur family tree indicates that plant-eating evolved multiple times, independently (Figure 15.1). As far as we know, all members of Ornithischia are herbivorous. It has been suggested that some ornithischians may have been omnivorous, but this is still a matter of debate. Thus, although herbivory is derived for animals, it is an ancestral trait within the ornithischian lineage. This means that, at the latest, it originated within the common ancestor of all ornithischians. Separately, in Saurischia, herbivory arises independently at least twice: once within Sauropodomorpha, including all sauropods and the basal sauropodomorphs, and at least once (and likely multiple times) within Theropoda, in various members of Maniraptoriformes (e.g., ornithomimids, therizinosaurs, and living birds). But how can we diagnose these states in long-dead animals when we can’t observe what (or even how) they eat? We rely on both indirect evidence, which is fossil data that allows inferences about an animal’s diet through a comparison with living animals, and direct evidence, which is fossil evidence of the actual act of eating and/or digesting. Let’s start with the indirect evidence for diet. Like all other aspects of dinosaur biology, we must begin with what we can observe and measure—living animals, their diets, and the biological features that are correlated with them. We can then look for evidence of those features in the fossilized remains of dinosaurs, keeping in mind the caveats mentioned above about comparisons with distantly related taxa. Sources of indirect evidence for dinosaur diets include: • Tooth morphology • Jaw shape, articulation, musculature, and cheeks Figure 15.1  Although the earliest members of Dinosauria were carnivorous, herbivory evolved at least three times in dinosaurs: once in the ancestor of all ornithischians, once in Sauropodomorpha, and at least once (likely multiple times) in Maniraptoriformes. The combination

of the leaf and bone above this group signifies that there are both carnivores and herbivores (and omnivores!) within that group.

15.2  Indirect Evidence: Tooth Morphology

• Skeletal anatomy • Feces

15.2 INDIRECT EVIDENCE: TOOTH MORPHOLOGY After reading this section you should be able to… • Explain the limitations in using the teeth of extant animal groups as models for inferring dinosaur diet. • Compare the teeth of modern analogs to those of hadrosaurs and theropods and make inferences about the respective diets of each.

When food enters the body, it first encounters the mouth. Thus, one of the primary features of living animals that is associated with their diet is, unsurprisingly, their teeth. Because teeth can be highly specialized to the preferred food type of the animal bearing them, they can give us some information about what that animal was eating. However, as mentioned above, living animals are limited as models for dinosaurs in the case of tooth morphology. The extant phylogenetic bracket that surrounds dinosaurs consists of crocodiles, which are all carnivorous, and birds, which include both herbivorous and carnivorous groups, but which are all toothless. Mammals have teeth, of course, and have both herbivorous and carnivorous groups, but dinosaurs and mammals are not closely related, and this is reflected in their teeth. With a few exceptions, mammals do not continually shed their teeth as do dinosaurs and other “reptiles”. Rather, mammals lose their “baby teeth” or “milk teeth”, which are replaced with a “permanent” set of teeth. For most mammals, these last until they die. Dinosaurs, on the other hand, like most lizards, snakes, and crocodiles, replaced each tooth continually throughout their lifetimes. Losing any one tooth during feeding or self-defense was no great loss, as it was replaced fairly quickly. Additionally, mammal teeth are complex, varying in shape depending on where they are in the mouth. This condition is called heterodonty (Figure 15.2A), and it is present in most mammals, except for some very derived groups like dolphins and whales. You, for example, exhibit heterodont dentition, and you have probably noticed your molars, incisors, and canines all look quite different, and each type has a

Figure 15.2  Examples of (A) heterodont dentition in an American black bear (Ursus americanus) and (B) homodont dentition in an alligator. Most

mammals, except for dolphins and a few other derived groups, have teeth that are shaped very differently depending on their functions: incisors for shearing, canines for tearing, and molars for grinding all vary greatly from each other. Most other vertebrates, including reptiles and most dinosaurs, have teeth that look the same, regardless of function or where they are placed in the mouth, like this alligator. (Courtesy of K. Tiffany, specimens courtesy of A. Heartstone-Rose.)

353

354

CHAPTER 15    How Do We Know What Dinosaurs Ate?

Figure 15.3  These drawings depict the upper jaws of three heterodontosaurid dinosaurs (left to right), Heterodontosaurus, Abrictosaurus, and Tianyulong. Notice

that unlike most dinosaurs, which are largely homodonts, within their mouths these heterodontids have differentiated teeth. (Courtesy of J.A. Headden, https://commons.wikimedia.org/wiki/ File:Heterodontosaur_snouts.jpg.)

different function as well; you don’t chew with your incisors, and you don’t take a bite from your fork with your molars. This makes feeding very efficient. Conversely, almost all dinosaurs—indeed, almost all “reptiles”—are homodont (Figure 15.2B), meaning that all their teeth are the same shape regardless of where they are in the mouth. Among dinosaurs, the one notable exception to this is the aptly named heterodontosaurids (Figure 15.3). Among extant “reptiles”, turtles have no teeth, and so cannot be used to model dinosaur dentition. Lizards and snakes have homodont teeth like dinosaurs, and there are groups of both herbivorous and carnivorous lizards, so they might seem a more appropriate comparison for dinosaurs than mammals. However, although lizards share the homodont condition with dinosaurs, their teeth are rooted very differently. In lizards, the teeth are either acrodont, meaning the base of the tooth rests on top of the jaw, (Figure 15.4A) or pleurodont, meaning they have a longer root that is only weakly attached to one side of the jaw (Figure 15.4B). In both of these cases, the teeth are held in place by ligaments. Conversely, in archosaurs (including crocodiles and dinosaurs), the teeth are set in deep bony sockets, a condition called thecodont (Figure 15.4C). This means in archosaurs, the teeth are held in the jaw much more securely than they are in lizards. Mammal teeth are also thecodont, but mammals evolved this trait completely independently from archosaurs. Thus, no matter what modern analogs we use, we must use caution when applying models and inferring traits to extinct non-avian dinosaurs. Even though mammals are somewhat limited as a model for dinosaur diets, they do share some convergent tooth traits related to diet that prove useful. For example, many herbivorous mammals have adaptations for

Figure 15.4  Teeth can be classified by the way they are rooted in the mouth. Most amphibians and fish (including sharks) have acrodont teeth (A), which

sit on top of the curve of the jawbone, and are connected to the bone by dense ligaments. Many reptiles have pleurodont teeth (B), where the jaw has a curve that holds the tooth on one side, and the rest of the tooth is secured by ligaments. Pleurodont teeth seem to be intermediate between the ancestral acrodont state, and thecodont teeth (C), which are set deep in bony sockets. Mammals and archosaurs, including crocodiles and dinosaurs, have thecodont teeth. (Adapted from H.E. Walter and L.P. Sayles, A, https​://ar​chive​.org/​detai​ls/b2​98212​77/pa​ge/27​2/mod​e/2up​; B and C (1949), https://flic.kr/p/w7dyhE.)

15.2  Indirect Evidence: Tooth Morphology

355

Figure 15.5  A comparison of a human tooth (left) to a horse tooth (right) (comparison not to scale). In human

teeth, the entire grinding surface is covered in enamel that protects the softer dentine, and cementum is present at the roots of the tooth. In horse teeth, hard enamel, softer dentine, and cementum are folded together across the grinding surface. Because they wear at different rates, this creates hard ridges of enamel or lophs, that aid in grinding. Additionally, horse teeth are hypsodont (high crowned), while human teeth are brachydont (low crowned). The high crowns of hypsodont teeth take a long time to wear down, giving these animals an advantage when eating tough abrasive foods. Because dinosaurs continually replaced their teeth, crown height was not as important. (Courtesy of Higgins D., Austin J.J., DOI: https​://do​i.org​/10.1​ 007/9​78-1-​4939-​3185-​9_13, used with permission.)

processing hard-to-chew, nutrient-poor plant tissues. For example, the hard enamel that is usually found on the outer surface of teeth becomes folded into the internal areas of the tooth, and interlayered with softer dentine (Figure 15.5). As the dentine wears down with use, the harder enamel wears more slowly, resulting in hard, sharp ridges (or lophs) on the grinding surface (Figure 15.6A) that aid in grinding tough material. When we see complex grinding surfaces on dinosaurs, then, we can speculate about the texture of their diet, even if we cannot identify particular plants. For example, sauropods and hadrosaurs both ate plants. But their teeth differ widely in complexity, and we can hypothesize that hadrosaurs ate much rougher-textured, harder to chew plants (Figure 15.6B). So what good are these ridges? Likely you know that horses eat types of grass. When horses pull grasses from the ground, abrasive soils often cling to the roots. Additionally, grasses themselves are tough, fibrous plants that may incorporate silica into their structure—perhaps as a “defensive strategy” to being preyed upon! This silica has the same effect as tiny bits of glass or sand (the chemical formula of both glass and sand is SiO2). Between the soil and the silica, as horses chew, their teeth become scratched and worn. Imagine what eating sandpaper would do to your teeth over time! Although grasses are hard to chew and difficult to digest, they are nevertheless the preferred food for horses and cows. Accordingly, the teeth of cows and horses have adapted to this food source by evolving high crowns that take a long time to wear down (a condition called hypsodonty) (Figure 15.5), as well as the sharp enamel-dentine ridges mentioned above to help break down the plant fibers. Although no dinosaurs exhibited true hypsodont teeth (because when they wore down from abrasive food they could just replace with a new tooth), the teeth of some dinosaurs, especially hadrosaurs, have some similar features to horse teeth. They both have vertical ridges, or carina, down the cheek side of the tooth (Figure 15.7), as well as similar folded grinding surfaces described above (Figure 15.5). The sharp carina and the folded and ridged enamel function to efficiently grind plants into smaller fragments, allowing more efficient nutrient extraction in the gut.

356

CHAPTER 15    How Do We Know What Dinosaurs Ate?

Figure 15.6  (A) The chewing surface of horse teeth shows ridges of highly folded enamel (arrows) that are well adapted for grinding tough plant material. Although there

is no similarity folded enamel in hadrosaur teeth (B), they had strong ridges that probably served the same function. And remember, dinosaurs shed their teeth continually, whereas mammals (usually) have only babe teeth and adult teeth, so the enamel would not have time to wear into the pattern in dinosaurs. (A courtesy of PM ParésCasanova, http://dx.doi.org/10.13070/ rs.en.1.951; B adapted from T. Evanston, https://commons.wikimedia.org/wiki/ File:Edmontosaurus_jaw.jpg.)

Figure 15.7  It has been suggested that hadrosaurid teeth (A), with their strong, sometimes denticulated carina, may have been eating plants similar in texture to the grasses that form the diet of horses (B) today.

Horse teeth have vertical ridges down the side of their teeth, as well as ridged enamel on the grinding surface. Similarly, hadrosaur teeth also have vertical ridges that aid in grinding. (A courtesy of K. Tiffany, B adapted from R. Atherton, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=55​ 79283​6.)

However, whereas horse teeth evolved in response to the challenges of eating grass, we have very little evidence for grasses in the Mesozoic. The origin of grasses has been suggested to have occurred in the Miocene, in response to the global drying of the climate. What could hadrosaurs have been eating then, that had similar tough and fibrous textures? What about those very early dinosaurs, close to the base of the dinosaur tree? What do their teeth reveal about the texture of foods they were eating? We see some similarities, and some major differences, between

15.2  Indirect Evidence: Tooth Morphology

357

Figure 15.8  (A) Skull of Lesothosaurus, a very basal, planteating dinosaur. Inset shows that its teeth are rather leaf-shaped, and small denticles can be seen on the sides of each tooth. These denticles (arrows) make shredding plant material more efficient, and aid in extracting nutrients from the plants. (B) Skull of a green iguana, with magnified inset of teeth. Green

iguanas are primarily herbivorous, and their teeth are also leaf-shaped with denticles at the margins. (A adapted from Ghedo, https://commons.wikimedia.org/wiki/ File:Lesothosaurus_sp_skull_3894.jpg; B adapted from B. Gratwicke and B. Kimmel, https://commons.wikimedia.org/wiki/ File:Gree​n_Igu​ana_s​kull_​(Igua​na_ig​uana)​ _and_​teeth​.png.​)

early plant-eating dinosaurs like Lesothosaurus (Figure 15.8) and more derived food processors like hadrosaurs. Early herbivorous ornithischians share similar tooth morphology. Their teeth have a single root anchored in a socket (thecodont), and the crowns of the teeth are simple and leaf-like, with tiny denticles on the edges (Figure 15.8A). We see this same pattern in herbivorous lizards (Figure 15.8B). This leaf-shaped pattern is tightly correlated to herbivory in living, non-mammalian herbivores. With the exception of some very early taxa, all ornithischians, including Lesothosaurus, were herbivores (Chapter 8). However, herbivory also evolved early in the saurischian lineage in sauropods. Although sauropods are not closely related to the ornithischians, they share some overall similarities in tooth morphology. The earliest sauropodomorphs also possess leaf-shaped teeth with denticles (Figure 15.9), similar to those of early ornithischians. However, sauropods did not evolve the very robust jaws with strong muscle attachments that are seen in many

Figure 15.9  Teeth from the early sauropodomorph Archaeodontosaurus show a pattern very similar to basal ornithischians, with a single root and leaf-like shape, with small denticles (arrow) to aid in processing plant material. (Adapted from D. Descouens,

https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=10​68659​6.)

358

CHAPTER 15    How Do We Know What Dinosaurs Ate?

Figure 15.10  Comparison of (A) derived hadrosaurid lower jaw and (B) Camarasaurus lower jaw. Hadrosaur

teeth are contained in a dental battery, allowing them to be continually replaced if they become worn down or broken. Sauropods also replace their teeth, but they are not arranged in these complex batteries. In addition, sauropod teeth are not as robustly rooted, and the bony projections for attachment of chewing muscles are much smaller than that of hadrosaurs. This suggests that hadrosaurs were capable of chewing and processing much tougher plant material more efficiently than most sauropods. (A courtesy of K. Tiffany. B adapted from K. Wiersma and P. M. Sander, Figure 4c in https​://do​i.org​/10.1​007/s​12542​ -016-​0332-​6.)

derived ornithischians, and the way their teeth are set in the jaws tells us they probably didn’t rely on their teeth to finely grind their food in the same way. Whereas early ornithischian and saurischian herbivores show similarities in their dentition, more derived herbivores of these groups differ greatly in their dental features. Sauropod teeth and jaws remain rather gracile, and are both less complex and less robust than the advanced ornithischians. Their teeth are simple, peg-like structures that are weakly rooted (although some later macronarians develop more complex teeth), and sauropods are not found to develop the deep and complex dental batteries of derived hadrosaurs and ceratopsians (Figure 15.10). The teeth within the dental batteries of derived ornithischians are also offset with keeled ridges. Both these groups continually replaced their teeth, with new teeth pushing up and out toward the surface to replace those teeth lost to wear. If only mammals had adopted this trait—your days at the dentist would be over! What about theropod tooth morphology? Although herbivory developed in both saurischians and ornithischians soon after they diverged, carnivory is the ancestral state for all dinosaurs. Meat is easier to break down and is more nutritious, and so doesn’t require the many modifications that herbivory does. However, carnivores still need to both catch and dismember struggling prey with their teeth. As a result, carnivores usually have much simpler teeth than those of herbivores. Their teeth are ideal for ripping, cutting, and/or crushing, but not chewing. In fact, most carnivores alive today don’t really chew their food, but participate in what is called “gorge feeding”. This is a style of feeding in which the carnivore rips large chunks of meat off their prey and swallow it nearly whole. This rapid feeding of a large amount of food is advantageous for carnivores who don’t know when or where they will eat again. Most theropod teeth are sharp, pointed, and recurved, with serrations that vary in size and number. In fact, these serrations can be diagnostic (autapomorphic) for a species. They may also differ in overall shape; some are almost round in cross-section with blunted tips, while others are laterally flattened and sharply pointed. Theropod teeth can also vary in thickness and degree of curvature. For example, Tyrannosaurus rex teeth are broad and thick, shaped almost like a banana. This robust form makes them well-suited for crushing dense bones of prey animals. However, the teeth of Carcharodontosaurus, despite being similar in size to T. rex, are more knife-like, flatter, and possess larger serrations (Figure 15.11). This suggests that Carcharodontosaurus teeth were more efficient at slicing and shredding muscle than crushing bone. So, how do we know what dinosaurs did with all these variations in tooth shape? As in everything else, living animals are our guide. For example, living gavial (gharial) crocodiles have diets consisting almost exclusively of fish. They also express a unique combination of facial and dental morphology that includes a narrow, elongate snout filled with many long, sharp, conical teeth that lack serrations. Spinosaurs (basal tetanuran theropods, Chapter 9), although bipedal and much larger than living crocodiles, ex-

15.2  Indirect Evidence: Tooth Morphology Figure 15.11  Although similar in size, the teeth of Tyrannosaurus rex and Carcharodontosaurus are very different. Whereas T. rex teeth are robust

with tiny serrations—good for crushing— Carcharodontosaurus teeth are flat and blade-like with large serrations—good for slicing. (Courtesy of K. Tiffany.)

Figure 15.12  Comparison of the skull of (A) a living gharial (a fish-eating semi-aquatic crocodile), with (B) the skull of the tetanuran Spinosaurus.

Although these two animals are not closely related in terms of time or evolutionary lineage, it has been posited that they share the same diet (and niche) because of convergent features in their skull, teeth, and jaw morphology. (A adapted from Gerrusson, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​id=19​41777​1; B adapted from Kabacchi, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​id=83​85023​.)

hibit convergent features with gavials (Figure 15.12). Their sharp teeth are also long, straight, and conical when compared with other theropods, and they lack serrations. The narrow snout and elongate conical gavial teeth are perfect for catching and holding slippery fish, and it has been hypothesized that this was also the case for spinosaurs. This is a striking example of convergence between the two very distantly related animals.

359

360

CHAPTER 15    How Do We Know What Dinosaurs Ate?

15.3 INDIRECT EVIDENCE: JAW SHAPE, MUSCULATURE, AND ARTICULATION After reading this section you should be able to… • Contrast the jaw shape and musculature of herbivorous and carnivorous dinosaurs. • State the function of cheeks. • Contrast herbivore and carnivore jaws in relation to cheeks and bony correlates of cheeks.

Not only can tooth shape be correlated (roughly) to food type, jaw morphology can also tell us much about how dinosaurs ate. In living vertebrates, the overall shape of the jaw, the relative placement of the teeth within it, and the orientation of muscles attached to it (as revealed by the muscle scars on bones) are indicative of diet. Remember the concept of bones and joints as levers, which we discussed in Chapter 13? The closer the muscle inserts to the joint, the more speed and flexibility the joint has, while the further away, the more power it has. This applies to jaw joints as well, and by looking at these bones and joints, we can get an idea of how animals were using their jaws. However, it should be noted that while in mammals, the dentary (mandible in mammals) articulates with the skull, in dinosaurs, it is a different bone entirely, the surangular, that articulates with the skull. This changes the mechanics of the jaw, so we need to be cautious about our comparisons of the two.

Figure 15.13  Comparison of the dentaries (mandibles) of four mammals, (A) horse, (B) deer, (C) coyote, and (D) lynx. The two

herbivores (A and B), show very different biomechanical features from the jaws of the two carnivores (C and D). The arrow indicates the condyle of the jaw joint, where it articulates with the skull. In the herbivores, this bone beneath the condyle is very deep (line), greatly expanded to accommodate jaw muscles for the repetitive motion of chewing—which herbivores do for much of the day. In the carnivores, the depth of the jaw is reduced at the condyle. Additionally, the muscle insertion for the jaw muscles (dotted line) does not extend very far forward in the jaw, remaining behind the tooth row, where in herbivores, it runs beneath the entire tooth row. These features result in a much smaller gape for herbivores, and a much wider gape and rapid bite closure in carnivores. (A–C courtesy of K. Tiffany; D adapted from Coluberssymbol, https://commons. wikimedia.org/wiki/File:Feli​s_cat​us_ga​ping_​ skull​_and_​mandi​ble.j​pg.)

In mammals, the depth of the jaw at the point where it articulates with the skull, as well as the length of the jaw along which the muscles attach, is different for herbivores and carnivores (Figure 15.13). In herbivores (Figures 15.13A, B), the jaw at the articulation point is very deep, and the insertion point for the muscle is very long, extending far toward the front of the mouth. These are features that suit an animal that spends a great portion of its day chewing; they increase efficiency for the continuous, repetitive motion of grinding food. However, they do come at the cost of a smaller gape (i.e., how widely an animal can open its jaws). Notice in Figures 15.13A and 15.13B that the muscle insertion runs almost entirely below the tooth row in these herbivores. That prevents these animals from opening their mouths too widely, or closing them very quickly.

15.3  Indirect Evidence: Jaw Shape, Musculature, and Articulation

361

However, for herbivores, this doesn’t really matter, as grasses and foliage aren’t usually in a great hurry to struggle and escape. In carnivores (Figures 15.13C, D), this pattern is different. The articulation point is comparatively shallow, and the insertion point for jaw muscles is shorter and remains mostly posterior of the tooth row. This configuration allows for a very large gape and a very rapid closure at the front of the mouth—perfect for capturing wriggling prey. Although the attachment site for their jaw muscles is smaller, they attach a lot of powerful muscle onto that insertion, allowing them to generate incredible bite forces. However, carnivores cannot sustain the repeated motions that herbivore jaws can, and indeed, most carnivores don’t chew their food at all once it’s caught, but simply tear out pieces and swallow them whole. How similar is the musculature of dinosaur carnivores and herbivores to the mammals discussed above? As in mammals, there is more variation among herbivores than among carnivores. Carnivore jaws and teeth possess certain common features, regardless of who they belong to. But herbivores vary across taxa…or even within taxa. For example, in Figure 15.14, two herbivorous sauropods are compared with two ornithischian herbivores. Sauropod teeth are simple, and are not arranged in the complex “batteries” of hadrosaurs like Edmontosaurus. But even the jaw of the more basal Pachycephalosaurus shows attachment points for more robust musculature than do the sauropods. All of the dinosaurs in Figure 15.14 were processing food very differently from each other, indicating that these filled different ecological niches! The dinosaurs in Figure 15.14 are all herbivores, based upon tooth and jaw morphology as well as other factors. How does their inferred musculature (e.g., position and length of attachment site) compare with that of meat-eating theropods (Figure 15.15B–D)? Theropod jaws are instead more comparable to living crocodiles, with a relatively flat area for both articulation and muscle attachment (Figure 15.15A). In Figure 15.15, we can see that the jaw muscles of crocodiles attach to a relatively smaller site compared with the attachment sites of herbivores, allowing their large gape and quick snap. However, even though the attachment site is small, they pack enough muscle into this area to generate an enormous bite force (ranging from about 900–3,700 pounds, depending on species

Figure 15.14  The skulls of four herbivorous dinosaurs, (A) Camarasaurus, (B) Diplodocus, (C) Edmontosaurus, and (D) Pachycephalosaurus. Although all

these dinosaurs are herbivores, their teeth and jaw musculature tell us they were processing food very differently. The arrows indicate the articulation of the jaw with the rest of the skull. In addition, there is strong bony evidence of cheek musculature on both the Pachycephalosaurus and Edmontosaurus (indicated by raised ridges highlighted by the dotted line) that are lacking in the sauropods. (A and D courtesy of K. Tiffany; B courtesy of L. Witmer; C photographed by M. Schweitzer at the Museum of the Rockies.)

362

CHAPTER 15    How Do We Know What Dinosaurs Ate?

Figure 15.15  The skulls of four carnivorous archosaurs, (A) an extant crocodylian, (B) Majungasaurus, an abelisaurid, (C) Tyrannosaurus rex, and (D) Deinonychus. The lower jaws

of all these meat-eaters are rather flat, without the large bony processes for muscle attachment that are seen in the herbivores. The theropod jaws show less variation than is seen among various herbivores, but the crocodile differs from the dinosaurs in tooth shape. The crocodile teeth are straight and conical, whereas the theropod teeth are more flattened and recurved. (All courtesy of K. Tiffany, photographed at the Field Museum.)

and body mass), as measured directly from hungry crocodiles by Dr. Gregory Erickson. Using this information as well as phylogenetic bracketing, biomechanics, and inferences about T. rex jaw musculature from fossil skull elements, computer models were generated to estimate the bite force of T. rex. They estimated a maximum bite force over twice that of an average crocodile, or almost 8,000 pounds! This number is much lower, however, than the bite force estimated for ancient crocodiles, like the massive crocodile Deinosuchus, which had a bite force of about 23,000 pounds! So, in an imaginary battle between Deinosuchus and T. rex (imaginary because these two taxa did not overlap in time; Deinosuchus went extinct before T. rex evolved), Deinosuchus would probably have made a tasty lunch of the top terrestrial carnivore. However, studies on crocodiles suggest that bite force increases with body size in this group. So, does the bite of a T. rex generate greater force because it has stronger muscles, or because it is simply bigger all around—bigger skull, bigger teeth, bigger neck? To put all this in perspective, we humans apply a bite force of a mere 150 pounds when they are eating a steak. We can’t do a lot of damage with our teeth, relatively speaking.

15.4 INDIRECT EVIDENCE: BONY CORRELATES OF CHEEKS After reading this section you should be able to… • State the function of cheeks. • Contrast herbivore and carnivore jaws in relation to cheeks and bony correlates of cheeks.

Here’s a question you may not have thought about: did dinosaurs have cheeks? First, let’s talk about what cheeks are. In mammals, cheeks are a subset of muscles used to move the jaw for food processing. Cheeks are formed by several muscle groups, including buccinator and masseter muscles, that originate in the upper jaw (maxilla) or skull and insert on the lower jaw. In addition to moving the jaw for food intake and processing, they play another, equally important role—they hold food

15.4  Indirect Evidence: Bony Correlates of Cheeks

in the mouth while chewing. The next time you eat something, think about how hard it would be to keep your dinner in your mouth and not all over the table if your cheeks suddenly disappeared! Dinosaurs, of course, were not mammals, and it has been suggested that perhaps they did not have muscular, mammalian-like cheeks. Rather, it has been proposed that the pocket of dinosaurian cheeks was formed by a thin layer of elastic connective tissue and skin covering the tooth row. In this case, dinosaur cheeks would only function to hold food in, and not to move the jaws. To extract the most nutrients possible, many herbivores must retain the food they eat in their body far longer than carnivores do. Cheeks contribute to this retention, in that they are essentially a pocket that allows animals to hold food in their mouth for a time, grinding it into small particles before it moves on in the digestion process. As a result of the fleshy cheeks that form a space around the tooth (Figure 15.16A), herbivores generally have a smaller gape. Carnivores, on the other hand, have a much smaller insertion on the bone, and it is further back, allowing a wider gape for subduing and holding large active prey. Cheeks are only necessary if you do, in fact, chew your food—and most carnivores do not. This is reflected not only in their sharp teeth, but in the fact that in carnivores like cats, the masseter muscles are narrower. In Figure 15.16, a T. rex skull is compared with that of a horse and a cat. Skeletal evidence shows that instead of fleshy cheeks, cats and most other living carnivores have a wide, open gape, and no true cheeks to hold in food—this is why your cat is a really messy eater! T. rex shows a similar pattern. In contrast, the horse has massive muscles that cover the side of its face, inserting almost to the anterior end of the tooth row. All ornithischians, with the exception of the very earliest and most basal, have a tooth row that is inset from the margin of the jaw (Figure 15.17), in addition to attachment points for cheek tissues that would cover much more of the face than we see in carnivores. Thus, tooth morphology, inset tooth rows, and tissue scars for cheeks together provide strong evidence for herbivory in certain dinosaur groups. Interestingly, although these features we’ve identified in extant herbivores are prevalent in ornithischian dinosaurs, they are not observed in sauropods. When compared with ornithischians, sauropods had relatively delicate jaws (Figure 15.18), and weakly rooted teeth, very different from the robust skulls, ridged teeth, and efficient dental batteries of many ornithischians. These bony and dental features provide evidence that sauropods did not chew their food, and raises the question of how these massive, fast-growing animals managed to take in and process enough plant material to sustain their enormous bodies. It has been proposed that sauropods likely employed a strategy of very high food intake—tons of food per day—coupled with long residence times in the gut to extract more nutrients, whereas the more derived ornithischians used a more mammal-like strategy of chewing to break down plant material. Even given this, there is still a lot we don’t know about sauropods or their diets—they pushed the limit of vertebrate function as we know it on just about every level! Both diplodocids and macronarians were massive obligate herbivores that overlapped in both temporal and geographic ranges. With the amount of plant material these massive beasts had to process each day to grow and maintain their body mass, how could groups of these animals occupy the same region? Only by eating different foods—and eating those foods differently. A recent study used the bony correlates for chewing muscles in the skulls of Camarasaurus and Diplodocus to create three-dimensional models (Figure 15.19). The authors concluded that

363

364

CHAPTER 15    How Do We Know What Dinosaurs Ate?

Figure 15.16  Chewing muscles in (A) a horse, an extant herbivore, (B) a cat, an extant carnivore, and (C) Tyrannosaurus rex, theropod.

The arrows show the origin and insertion points of various chewing muscles. In the horse, the chewing muscles are extensive and cover most of the side of the face. The teeth are also inset, creating a pocket between the muscles and the teeth—a cheek! The cheek muscles extend forward almost to the anterior end of the tooth row, leaving a small gape. On the cat, the muscles insert on a narrower point, behind the tooth row. The teeth are flush with the sides of the jaw, with no room for a cheek pocket. The T. rex shows a similar pattern to the cat, with muscles inserting over a narrow portion of the lower jaw, behind the tooth row. This suggests the possibility of a wide gape, which in a T. rex would amount to over 5 feet! Additionally, note that the teeth of the dinosaur are not differentiated by function like the heterodont teeth of either mammal. Rather, T. rex had homodont teeth that were the same no matter where they were in the jaw. (A adapted from Vassil, B adapted from Coluberssymbol, https​://co​mmons​.wiki​ media​.org/​w/ind​ex.ph​p?cur​id=15​76049​1; C courtesy of K. Tiffany, photographed at the Field Museum.)

Camarasaurus, with its more robust skull, generated much greater bite forces than Diplodocus. Thus, it was proposed that perhaps Diplodocus stripped branches by biting, then pulling their heads backward, while Camarasaurus had a more generalized diet that was tougher in texture. These different feeding styles allowed for effective niche partitioning, allowing these two megaherbivores to overlap.

15.5 INDIRECT EVIDENCE FOR DIET: SKELETAL ANATOMY After reading this section you should be able to… • Discuss skeletal features that are indicative of either herbivory or carnivory. • Define gastrolith and state what it does and what type of diet it is evidence of.

15.5  Indirect Evidence for Diet: Skeletal Anatomy

365

Figure 15.17  The skull of a small ceratopsian Wendiceratops, showing two skeletal features consistent with cheeks: robust bony processes for the attachment of cheek muscles (or perhaps elastic, non-muscular cheek tissue) (arrows), and tooth rows that are inset from these margins to form a pocket of space. The bony attachments

for cheek tissues extend far forward, toward the tip of the beak, resulting in the small gape usually seen in plant-eaters. (Courtesy of the Royal Ontario Museum © ROM.)

Figure 15.18  Lower jaws of (A) Camarasaurus and (B) Diplodocus.

Teeth and jaws are not the only characters we can use to infer diet in extinct organisms. Herbivores compensate for the nutrient-poor quality of plants by housing large populations of various bacteria in their large guts. These gut bacteria can break plant material down to release nutrients in a form that vertebrates can then access. In some cases, like cows, their “stomach” is separated into four chambers, each with distinct properties that allow them to process grass, hay, and other plants much more efficiently than our stomachs would. As a result, if a human and a cow ate the same plant, the cow could draw many more nutrients out of the same amount of plant material than the human could. On the other hand, have you ever seen a skinny cow? Extant herbivorous mammals have a greatly expanded gut space. For the same reason that they need cheeks—to hold food in for longer oral processing—they also need to hold food for a longer time within their gut. Plant material, primarily

Although these animals are both sauropods and therefore share an ancestor in common more recently than with other dinosaur groups, they are biomechanically quite different. The lower jaw of the macronarian, Camarasaurus, is more robust. Its teeth are relatively large and spoon-shaped, and the jaw has greater depth than the diplodocid, Diplodocus. Diplodocus has very small, narrow, stubby teeth relative to the macronarian, and the teeth are only found in the front. This supports the idea that these dinosaur mouths functioned like rakes, stripping leaves from branches, but not chewing them at all. Images are not to scale. (A courtesy of K. Tiffany; B courtesy of L. Witmer, https​://pe​ople.​ohio.​edu/w​ itmer​l/col​lecti​ons/i​mages​/Dipl​odocu​s_Lon​ gus_D​SC_02​90.JP​G.)

366

CHAPTER 15    How Do We Know What Dinosaurs Ate?

Figure 15.19  This three-dimensional reconstruction of the skulls of (A) Camarasaurus and (B) Diplodocus is based upon bony correlates of the chewing muscles preserved in these dinosaurs. Muscles are superimposed

on the models, allowing calculations of power behind the bites. It turns out that Camarasaurus, with its robust skull and jaws, as well as bigger teeth, was adapted to eating tough-textured foods. Conversely, Diplodocus was more restricted in its diet. (Courtesy of D. Button.)

the tough, resistant cellulose that makes up plant cell walls, is insoluble, and cannot be broken down solely by the enzymes produced by vertebrate herbivores. Thus, most vertebrates that subsist on a plant diet require a heavy load of bacteria in their guts. Bacteria produce an enzyme called cellulase that is specific for this carbohydrate. The bacteria are well protected and thrive in the gut of a cow, or in the intestines of a horse, where they break down the cellulose fibers, releasing nutrients. However, the plants must be exposed to cellulase for significant periods of time, so this time-consuming process requires a complex digestive tract. The result is that most vertebrate herbivores have a greatly expanded gut space. Many of the dinosaurs that have other features consistent with an herbivorous diet also have skeletal adaptations that imply an expanded gut space (Figure 15.20). In particular, within the herbivorous clade Ornithischia, the defining character of this entire group (a retroverted pubis) can be considered an adaptation for herbivory, because it allows the gut to occupy a much larger area. Members of Maniraptora, the theropod lineage most closely related to living birds, developed a retroverted pubis convergently, and it has been suggested that this shift in pubic orientation coincided with the adaptation in some members of this group to a diet that included plants. Another skeletal change is more outwardly

Figure 15.20  Skeletal drawings of a juvenile ornithischian, Parasaurolophus, compared with a saurischian theropod (Stenonychosaurus). The retroverted

pubis characteristic of ornithischians greatly expands the gut space (dotted red line). This allows hard-to-digest plant material to be retained longer, giving enzymes more time to break plants down. The theropod, with its tripod pelvis, has a far smaller gut. The space is reduced even further by the presence of gastralia. These features support the interpretation that these animals were eating meat, which is far easier to digest. (A and B adapted from artwork by Scott Hartman, https:// doi.org/10.7717/peerj.182/fig-4 and doi:10.1371/journal.pone.0024487.)

15.5  Indirect Evidence for Diet: Skeletal Anatomy

splayed ribs. Rather than being narrow when viewed from the front, some dinosaurs show wide rib cages that make room for a bigger gut. Extant herbivorous birds still need to process and retain tough plant material in their bodies. However, this group has two major problems: (1) they don’t have teeth, ridged or otherwise, and (2) they need to keep their body as lightweight as possible to meet the constraints of flight (Chapter 19). Instead of teeth, living birds possess a complex digestive system that includes a very muscular organ called a gizzard, which is part of the bird’s stomach. Herbivorous birds often swallow gravel, which is held in the gizzard, where the strong muscles grind ingested plants and the gravel together, functioning almost like teeth to break the plants down (Figure 15.21). Even though living crocodiles are all carnivores and have teeth, they also possess a chambered stomach, with one very muscular chamber that some compare to a functional gizzard. How likely is it, then, that dinosaurs possessed this trait? In some lineages of dinosaurs, small accumulations of pebbles have been found within the body cavity, close to where the stomach would have been. This gravel is very different from the very fine-grained sediments surrounding the rest of the skeleton. It has been proposed that these small accumulations of rock represent gizzards in dinosaurs (Figure 15.22) and are called gastroliths (gastro = stomach; lith = stone). These have now been found in association with dinosaurs from many different groups and are thought to be adaptations to an herbivorous diet. Intriguingly, it has been proposed that some sauropods may have possessed a gizzard with such gastroliths to aid in plant breakdown, compensating for their relatively delicate skulls and teeth. However, to date, possible gastroliths have not been found in association with sauropod remains in sufficient volume for them to have played a functional role in digestion. Although we have not yet found conclusive evidence for gastroliths in sauropods, their absence doesn’t mean that sauropods did not possess a muscular “gizzard” as well. As with many aspects of dinosaur anatomy, we must look to future discoveries to shed light on this question!

Figure 15.21  This gizzard, which was removed from an extant mallard, shows the ingested grit that, together with strong muscles, helps to grind and process tough food for this toothless bird. (Courtesy of M.

Bowyer and the Missouri Department of Conservation, https​://ww​w.mis​souri​conse​ rvati​on.or​g/fil​es/ma​llard​-gizz​ardjp​g.)

367

368

CHAPTER 15    How Do We Know What Dinosaurs Ate?

Figure 15.22  This articulated specimen of Caudipteryx was found in very fine-grained sediments that preserved many aspects of its anatomy, including feathers and stomach stones (arrow). This dinosaur had only a

few teeth in the front of its mouth, which were clearly not adapted for grinding. Thus, these gastroliths may have aided in digestion, functioning like the gizzard of modern plant-eating birds. (Adapted from Daderot, https​://co​mmons​.wiki​media​.org/​w/ ind​ex.ph​p?cur​id=24​55672​5.)

15.6 INDIRECT EVIDENCE FOR DIET: FECES (COPROLITES) After reading this section you should be able to… • Define coprolite. • Discuss what evidence coprolites provide about dinosaur diet. • State the limitation of using coprolites to infer dinosaur diet.

When people go to a dinosaur exhibit in a museum, they don’t often see dinosaur poop on display. However, poop production was certainly a vital aspect of how they functioned biologically, because even for dinosaurs, what goes in must come out! Think of a herd of hundreds of nesting sauropods or thousands of hadrosaurs, staying in one area to lay and hatch their eggs. Imagine the effect of all the feces they produced on the environment (not to mention the smell)! For living animals, waste products (i.e., poop) can tell us much about their diet and overall health. Coprolites, or fossilized feces, can likewise tell us a lot about the diet of the animal that produced it and the ecosystem in which they lived. But how likely is it that fecal matter would survive long enough to fossilize? Feces have already been through the entire digestive system of the animal that produced it, and have been acted upon by the teeth and tongue to physically alter foot matter, as well as salivary enzymes, gut enzymes, and intestinal microbes, all designed to break down the food for nutrients (proteins, carbohydrates) the animal needs to function. Despite this, under just the right conditions, we know that coprolites survive. For example, the coprolites in Figure 15.23 were recovered from the Kaiparowits Formation and are Campanian in age (~75 million years old).

15.6  Indirect Evidence for Diet: Feces (Coprolites)

369

Figure 15.23  (A) Dinosaur coprolite, as discovered in the field. The yellow

arrow shows a back-filled dung beetle burrow, indicating that dung beetles were important in recycling Mesozoic dung, just as they are today. (B) Microscopic image of a section from a different coprolite, showing that the dinosaur that made it ate rotted conifer wood. (Courtesy of K. Chin. Micrograph from coprolite in collections at the Denver Museum of Nature and Science.)

The presence of a back-filled dung beetle burrow on the surface of coprolite in Figure 15.23A (arrow) provides evidence of part of a Cretaceous food web; the dinosaur ate food, processed it, and the burrowing dung beetle and its babies ate what the dinosaur left behind. But what kind of dinosaur is the key to this food web, and how can we tell? To extract the most information from coprolites, we must look at them under the microscope. Many Mesozoic coprolites show different kinds of plant material. Figure 15.23B shows woody conifer material, including tracheids, which are part of the plant vascular system. Such microscopic textures confirm that first, this is a coprolite (and not just a poop-shaped rock). Second, it shows that whoever produced it was a plant-eater. So, we have an herbivorous dinosaur eating rotten conifer wood, and then dung beetles colonizing and eating the inevitable poop! Using only evidence of fossil “leavings”, we know the “poopetrator” (as paleontologist Karen Chin likes to say) was an herbivore. Coprolites from smaller animals have even been found with insect remains, indicating that some may have been insectivores, or at least enjoyed the occasional insect snack. Also, remember those phytoliths (silicified plant tissues) from Chapter 12? Phytoliths have been found in some dinosaur coprolites, providing evidence that the types of plants that comprised the diet of those poop-producers were tough and abrasive, like some modern grasses. In fact, the presence of phytoliths preserved in fossilized poop suggests that perhaps grasses evolved well before the Miocene, and if further evidence supports this, maybe dinosaurs ate grasses after all! Although evidence from coprolites suggests that grasses may have been part of Late Cretaceous ecosystems, this is still controversial, as most other evidence points to a later origin, and fossil grasses have yet to be described from these ancient rocks. Just as with living organisms, major components of a dinosaur’s diet are revealed by what it expelled as waste material. Bone fragments or insects remains have been found in dinosaur coprolites, and these give valuable clues as to what dinosaurs may have been eating. The downside to coprolite evidence of diet is similar to that of footprints (Chapter 16); we can never be sure of which specific animal produced the feces. Indeed, unless a coprolite is very large, we may not even know whether it was produced by a dinosaur, turtle, crocodilian, or fish that lived in the same geographic region as dinosaurs. The sure identifier of a carnivore’s coprolite is the presence of bone and/ or muscle tissue, and in fact, carnivore coprolites are easier to identify in fossils than those of herbivores, because they tend to keep their original and distinctive, poop-shaped (fusiform) morphology better! But for very large coprolites this is more difficult, because it is more likely the fecal matter will have broken apart by the time it hit the ground, or

370

CHAPTER 15    How Do We Know What Dinosaurs Ate?

Figure 15.24  Massive mineralized coprolite in a field jacket. It was

attributed to Tyrannosaurus rex based upon its size (T. rex was the largest carnivore in this region at the end-Cretaceous) and the presence of purported muscle fibers preserved inside of it. (Courtesy of the United States Geological Survey.)

Figure 15.25  Microscopic examination of this massive coprolite showed morphological evidence of striated skeletal muscle. The muscle fiber recovered from the coprolite (A) has an identical microstructure to striated skeletal muscle from living vertebrates, at the same magnification (B). Other regions of

the coprolite contained bone fragments uniquely identifiable as belonging to a Pachycephalosaurus. (Courtesy of K. Chin doi: https://doi.org/10.1669/08831351(2003)0182.0 .CO;2.)

be trampled afterward. But of course, “more difficult” does not mean impossible. When paleontologists were looking for dinosaur bones in end-Cretaceous sediments in the early 2000s, they recovered an unusual mineralized mass from the Dinosaur Park Formation in Alberta, Canada (Figure 15.24). Looking at sections of this mass under a microscope revealed that it was indeed produced by a carnivore, and the very large size of it suggested a tyrannosaur was the culprit. Inside the matrix of this coprolite was not plant material, but what appeared to be muscle tissue! Figure 15.25 shows the microscopic components comprising this massive coprolite, compared with muscle tissues from a modern animal. Think of what must have happened to produce a fossil like this! The dinosaur would have had to kill an animal or find a carcass and eat parts of it, which would then have to pass through its digestive system without being fully broken down, suggesting a gorge feeding strategy. Then it would have to exit the dinosaur and hit the ground, where it would have to be stabilized long enough to fossilize and become part of the fossil record. Quite the journey for us to be able to learn from it today! As informative as feces are with respect to an animal’s diet, the niche it filled, and its ecosystem, identifying what species produced the coprolite always rests on inference. The only way to determine the originator of the coprolite conclusively is to find fecal material still within the body cavity of an articulated dinosaur—and although it has happened, it is a very rare occurrence! Although their usefulness in understanding the paleobiology of particular dinosaurs may be limited, coprolites can and do provide a lot of information about paleoecological relationships. In the example given above (Figure 15.23; also see Chapter 20), coprolites were used to show that Mesozoic dung beetles and snails exploited dinosaur dung. Feeding on fecal matter is called coprophagy. This was one of the first Mesozoic food webs to be described, and showed how dinosaurs fit into one particular ecosystem.

15.7  Caught in the Act: Direct Evidence for Diet

15.7 CAUGHT IN THE ACT: DIRECT EVIDENCE FOR DIET After reading this section you should be able to… • Discuss the types of fossil evidence that provide direct evidence for dinosaur diets.

The surest way of knowing what a dinosaur was eating is to find direct evidence of it “caught in the act” of feeding or digesting. This includes finding teeth or tooth marks that can conclusively be linked to one species on the bones or tissues of another, or the very rare instance in which the stomach contents of a dinosaur have been preserved.

15.7.1 Teeth and Tooth Marks If we find teeth, or toothmarks, in or on the bones of an animal, this is powerful evidence of predation or scavenging by the animal that left them. However, we must be able to conclusively link the teeth to a particular culprit dinosaur—that is one reason why understanding and characterizing tooth morphology is so important. Figure 15.26 shows an example of such evidence. An Edmontosaurus vertebra was discovered with a theropod tooth lodged inside it—conclusive evidence that some theropod was trying to make a meal of it! Based on the size and robustness of the tooth, as well as the size, number, and spacings of its serrations, researchers identified this tooth as belonging to Tyrannosaurus rex. This is direct evidence of not only what type of food T. rex was eating, but who it was eating as well.

15.7.2 Stomach Contents By far the most direct evidence we have of dinosaur diets—or anyone’s diet—is the remnants of its last meal—its stomach contents. For example, we know that alligators and crocodiles sometimes eat people, because we find human body parts in their stomachs! Crocodiles are not picky eaters, and their stomach contents show us that; parts of zebras, ostriches, snakes, and virtually any other animal—even humans—have been found inside their guts.

Figure 15.26  An Edmontosaurus vertebra that was discovered with a Tyrannosaurus rex tooth embedded in it. The discovery of a T. rex tooth in

an Edmontosaurus tail bone is strong, direct evidence that T. rex was eating Edmontosaurus. (Courtesy of D. Burnham and R. DePalma.)

371

372

CHAPTER 15    How Do We Know What Dinosaurs Ate?

Similarly, we can learn about the diet of dinosaurs by the fossilized contents within their stomachs, if these preserve with the rest of the body. Exquisitely preserved skeletons of very primitive dinosaurs like Sinosauropteryx and Compsognathus have been found with the bones and jaws of tiny lizards in their stomach region. Stomach contents confirm the bite-mark evidence above, and also show that these dinosaurs ate other dinosaurs. In at least one case, an early compsognathid dinosaur called Sinocalliopteryx gigas (Figure 15.27) was found with the foot and leg of a small dromaeosaur (possibly Sinornithosaurus) inside the gut region, complete with tufts of undigested feathers (Figure 15.28)! Within the gut of Baryonyx, researchers found fish scales, supporting evidence from tooth and skull shape that this spinosaurid survived at least partly on fish. A Campanian Daspletosaurus (a close relative of the later Tyrannosaurus rex) contained remains of a juvenile hadrosaur in its gut region. A spectacular Microraptor from China showed evidence of feathers, and the bones of an early bird, within its abdomen. In several cases, we see the body parts of tiny mammals inside dinosaurs of different kinds, indicating that they were not averse to a mammal diet. However, every now and then, the mammals got their revenge. A (relatively) large Mesozoic mammal called Repenomamus was found with parts of a baby dinosaur inside (Figure 15.29). Based upon this direct evidence, we can say with confidence that the menu for carnivorous dinosaurs was quite varied.

Figure 15.27  Full skeleton of Sinocalliopteryx gigas, showing gut contents. (Courtesy of L. Xing, et.al.,

doi:10.1371/journal.pone.0044012.g001.)

Figure 15.28  (A) Enlarged view of the stomach contents of Sinocalliopteryx, showing undigested featherlike structures. (B) Diagram of skeleton and stomach contents. (Adapted

from L. Xing, et.al., doi:10.1371/journal. pone.0044012.g001.)

15.8  What We Don’t Know

373

Figure 15.29  Even though mammals were preyed upon by dinosaurs, occasionally, mammals got their revenge. The stomach contents of

Repenomamus robustus show evidence of the bones of a baby dinosaur, which was a true giant of its day. (Adapted from J. Chen, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=80​42794​8.)

15.8 WHAT WE DON’T KNOW 15.8.1 How Did Large, Herbivorous Dinosaurs (e.g., Sauropods, Ceratopsians) Consume Enough Plant Material to Maintain Their Body Mass, Especially If Their Energy Requirements Were Higher Than Regular Ectotherms (See Chapter 18)? Unit for unit, today’s plants are not very nutritious, and they don’t provide nearly as much of the “raw material” for growth and tissue maintenance as meat. The flowering plants we are familiar with today (e.g., grasses, fruit trees) are generally more nutritious than gymnosperms (e.g., pine trees and cycads) but they did not evolve until the Late Cretaceous, so most sauropods, ankylosaurs, and other plant-eaters did not have the option of eating these relatively more nutritious plants. Given what we know from living herbivores, it would seem that these large herbivores, many times the size of a cow or elephant, would be required to eat more often and longer, all things being equal, than large living herbivores—possibly up to 24 hours a day, seven days week! Probably, that still wouldn’t be enough to support their great masses. So how did they do it? Questions to consider: • Could plants have been more nutritious in the Mesozoic? How might we try to investigate the nutritive value of plants that are also extinct?

374

CHAPTER 15    How Do We Know What Dinosaurs Ate?

• Did herbivorous dinosaurs have enzymes or gut bacteria that allowed them to recover more nutrition from plants? How could we test this idea, when digestive tracts and other organs of dinosaurs are not typically preserved? • Both of the above suggest that aspects of either plant or dinosaur biology could have been different from what we are familiar with today. How would you test these hypotheses?

15.8.2 What Did Toothless (Or Nearly Toothless) Dinosaurs Like Oviraptor Eat? Dinosaur teeth were generally adapted to the things they ate, so by studying their teeth we can get a pretty good idea of what they were eating. But for dinosaurs without teeth, like oviraptor who only had two bony projections in its jaw, determining what it ate becomes an even more speculative task, unless we find direct evidence like preserved stomach contents. It has been suggested that toothless Maniraptoriformes were omnivorous, eating seeds, fruits, and insects much like modern birds. It is also thought that oviraptor may have used its strong jaws and beak to crush and eat mollusks, like clams. • What may have driven the loss of teeth in oviraptorosaurs? • What functional purpose did the two bony projections inside the jaw of oviraptors serve?

CHAPTER ACKNOWLEDGMENTS We thank Dr. Greg Erickson, Dr. Karen Chin, and Dr. David Button for their generous reviews and suggested improvements to this chapter. Dr. Erickson is a Professor of Anatomy and Vertebrate Paleontology in the Department of Biological Sciences at Florida State University. Dr. Chin is an Associate Professor and Curator of Paleontology in the Department of Geological Sciences and Museum of Natural History at the University of Colorado at Boulder. Dr. Button is a researcher in the Department of Earth Sciences at the Natural History Museum of London.

LITERATURE Button, D. J., Rayfield, E. J., and Barrett, P. M. (2014). Cranial biomechanics underpins high sauropod diversity in resource-poor environments. Proceedings of the Royal Society Series B: Biological Sciences, 281(1795), 2014–2114.

O'Connor, J., Zhou, Z., and Xu, X. (2011). Additional specimen of Microraptor provides unique evidence of dinosaurs preying on birds. Proceedings of the National Academy of Sciences of the United States of America, 108(49), 19662–19665.

Chin, K., Eberth, D. A., Schweitzer, M. H., Rando, T. A., Sloboda, W. J., and Horner, J. R. (2003). Remarkable preservation of undigested muscle tissue within a Late Cretaceous tyrannosaurid coprolite from Alberta, Canada. Palaios, 18(3), 286–294.

Varricchio, D. J. (2001). Gut contents from a Cretaceous tyrannosaurid: Implications for theropod dinosaur digestive tracts. Journal of Paleontology, 75(2), 401–406.

Erickson, G. M., Gignac, P. M., Steppan, S. J., Lappin, A. K., Vliet, K. A., Brueggen, J. D., Inouye, B. D., Kledzik, D., and Webb, G. J. (2012). Insights into the ecology and evolutionary success of crocodilians revealed through bite-force and tooth-pressure experimentation. PLoS One, 7(3), e31781. Gignac, P. M., and Erickson, G. M. (2017). The biomechanics behind extreme osteophagy in Tyrannosaurus rex. Scientific Reports, 7(1), 1–10. Hone, D. W., and Rauhut, O. W. (2010). Feeding behaviour and bone utilization by theropod dinosaurs. Lethaia, 43(2), 232–244.

Wiersma, K., and Sander, P. M. (2017). The dentition of a well-preserved specimen of Camarasaurus sp.: Implications for function, tooth replacement, soft part reconstruction, and food intake. PalZ, 91(1), 145–161. Xing, L., Bell, P. R., Persons, I. V., Ji, S., Miyashita, T., Burns, M. E., and Currie, P. J. (2012). Abdominal contents from two large Early Cretaceous compsognathids (Dinosauria: Theropoda) demonstrate feeding on confuciusornithids and dromaeosaurids. PLoS One, 7(8), e44012.

16 HOW DO WE INTERPRET DINOSAUR BEHAVIOR?

16

DINOSAUR TRACKWAYS, HERDING, AND PATHOLOGIES

T

he vast majority of studies that investigate dinosaur paleobiology are carried out on bones, and are supplemented by studies of other, rarely preserved body tissues, such as skin or feathers. However, an animal is more than the sum of its parts. Its behavior, while certainly influenced by its biology, encompasses activities beyond those that can be inferred from its bones and tissues alone. For example, bones might provide clues as to whether a dinosaur could have possibly climbed a tree or ran quickly, but what about whether they were social or solitary individuals? Did they migrate? Did young dinosaurs stay with adults like those of some mammals and birds? Or were they left to find their own way in the world like turtles and most other reptiles? We can’t directly observe non-avian dinosaurs, but they obviously had behaviors. Body fossils rarely (but sometimes) preserve these. A good example of non-avian dinosaur behavior captured in the fossil record is the little oviraptor, Citipati, still brooding its eggs and protecting its nest as discussed in Chapter 17, Reproduction. In Chapter 15, we discussed dinosaur diets and feeding behaviors. In Chapter 17, we will discuss dinosaur reproduction and mating behaviors. Here, we discuss some more generalized behaviors, as observed through trackways, death assemblages, and pathologies. Of course, to understand dinosaur behaviors, we need to first study different behaviors in animals alive today that are closely related, and identify indicators of these behaviors that might be discernable in the fossil and rock records. This sets the range of possibilities for behaviors that dinosaurs could have conducted. For example, some tracks and trackways in living animals can be correlated to their behaviors, and this helps us to understand the relationships between skeletal features and footprints in dinosaurs.

IN THIS CHAPTER . . . 16.1 ON THE MOVE: FOOTPRINTS AND TRACKWAYS 16.2 DINOSAUR GRAVEYARDS: MASS DEATH ASSEMBLAGES 16.3 INJURIES AND SICKNESSES: PALEOPATHOLOGIES 16.4 WHAT WE DON’T KNOW

376

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

16.1 ON THE MOVE: FOOTPRINTS AND TRACKWAYS After reading this section you should be able to… • Discuss the limitations and advantages of studying trackways and what they can tell us about dinosaurs. • Describe factors that affect whether a dinosaur will leave footprints behind. • Compare and contrast the information we can get from a single footprint versus trackways. • Identify the dinosaur group that left a track based on the features of the print.

What can you say about the scene in Figure 16.1A? From this image, can you determine how many organisms were present? Can you determine the types of organisms that were present? The direction and speed at which they were moving? Just based upon the data shown, can you determine if these organisms were present at the same time? Were they all from one species? Alternatively, what can you tell about the patterns shown in Figure 16.1B? What information is conveyed here? How rigorous are your conclusions? How is the information different than what is gained from bones? How do you think trackway data compare with skeletal data? Which do you think is more limited, and what are these limitations? These questions should get you thinking about the utility of incorporating footprint/trackway data into paleontological studies. Trace fossils such as footprints and trackways record dinosaurs in the act of behaving, and thus there are several advantages to studying tracks and trackways that are not applicable to bone and skeletal information. Advantages to studying tracks include: • Most tracks are found where behaviors occurred: Footprints faithfully record where dinosaurs were living, moving, or otherwise behaving. Unlike dinosaur bones that can be carried to new regions by water or removed by scavenging, trace fossils like foot-

Figure 16.1  Trackways allow us to interpret behavior. (A) How many

organisms were present in this environment? What direction is the organism going? Was it running or walking? Bipedal or quadrupedal? What can you say about the feet of the organism? Notice that even if all you had of the organism were these footprints, there is much you can say. Now, ask the same questions of image (B). Are your answers different? Just like you can detect aspects of human and other vertebrates from only trackways, as we shall see, the same is true with dinosaur footprints. (A courtesy of P. Halling, https​://co​mmons​.wiki​ media​.org/​w/ind​ex.ph​p?cur​id=12​94103​1; B courtesy of A. Beecroft, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=13​ 88870​8.)

16.1  On the Move: Footprints and Trackways

prints almost always occur in situ (in place), in the very sediments that they walked in. • Tracks are direct evidence of behavior at a moment in time: Trackways capture direct evidence of behaviors difficult to discern from bones alone, including walking, running, resting (Figure 16.2), and sometimes noticing and chasing other animals. • Animals make more tracks than bones: The potential number of footprints left behind by an animal is much, much greater than the number of bones it can leave behind. Your fitness tracker will nag you to deposit 10,000 “footprints” per day. But you can only deposit 206 bones, and you can only do that once! Does that translate into a better chance of finding tracks than bones? As we shall see, tracks are susceptible to different taphonomic processes (Chapter 11) than bone, and that is enough to offset the sheer number of footprint data. In general, tracks are best preserved in calm, low energy conditions, but bones usually preserve best when buried rapidly. Calm environments also result in better chances of recovering articulated skeletons, but rapid deep burial usually is deleterious to footprints, which is why tracks and bones are seldom found together. • Tracks can yield soft tissue morphology: An animal doesn’t walk on its bones, it walks on fleshy (or hooved) feet; thus, its bony foot skeleton is not an accurate reflection of the part of the animal that interacted with the ground, nor vice-versa. The soft tissues that overlay the bone are a much more accurate picture of how the animal functioned in life than are the bones alone. In addition, under just the right conditions, footprints can be sources for skin and scale patterns, the shape and size of fleshy pads that underlie each digit, and the structure of flesh or keratinous sheaths or hooves that cover the hind- and/or forefeet. For example, Figure 16.2 shows an imprint left when a bipedal theropod dinosaur, probably Dilophosaurus, stopped and rested, leaving an impression of part of the pelvis, hands, and tail amidst footprints in the sand. In addition to testifying that, like other animals, they needed to rest periodically, this type of trace fossil tells us that theropods actually inhabited areas where sediments were sandy and moist enough to retain an impression. A trace fossil such as this might add to the information from bones regarding the biomechanics of their pelvis and legs, and how these elements contributed to posture.

377

Figure 16.2  (A) Footprints in Lower Jurassic (~200 Ma) sediments, left behind by what is thought to be Dilophosaurus. (B) Schematic of the track is shown in A. The red tracks on

this drawing represent where the animal first sat. The two hind feet are LP and RP, the two handprints are LM and RM, and the protruding ischium (i.e., where it rested its butt) is labeled IC. Then, the dinosaur did a little wiggle, shifting its feet somewhat, as shown in yellow. After it rested enough, the green tracks show where it shoved off from the ground, dragging its tail in the process of rising (TD, blue). (C) An artistic interpretation of this scene based upon these footprint data. (The colors and feathering are speculation; no data have been found to support this directly.) (All courtesy of Milner et al., artwork by H. K. Luterman.)

378

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

16.1.1 Footprint Formation and Preservation Dinosaur footprints result from the physics of displacement, just as your footprints on the beach do. When dinosaurs walked on sediments sufficiently moist and firm enough to form footprints (see below), the pressure exerted by the dinosaur’s foot caused the underlying sediments to deform, compressing in the direction of the pressure. Close to the surface of the print (i.e., nearest to the contact of skin and sediment), the deformation of the sediment is greatest, and the fidelity of the print is maximized. In other words, the print left at the very surface of the sediment is the least distorted—most accurately reflecting the size and shape of the foot (Figure 16.3). We call this the true track (also, an imprint or natural mold). However, the layers of sediment under the surface print also compress and deform under the weight of the dinosaur, creating an undertrack—an impression left by the pressure of the foot on deeper layers of sediment. Thus, if the surface layer of the print—the one with the most information—is eroded away, we may still get some information from the undertrack. However, the deeper we go, the more resolution is lost, and the original shape and size of the foot become less distinct in deeper undertracks. To understand undertracks, think of it in terms of writing on a pad of paper. If you press hard on the pen while writing a sentence, then remove the first layer of paper, you can feel the indentation of the words in the next layer of paper. This is called a palimpsest. This palimpsest might also be felt on the third sheet of paper, but it will not be as deep, and the words will not be as easy to make out. If you peel back successive layers of paper, eventually, there will be no palimpsest at all. If we do not account for the possibility that we are observing deeper layers of a track, and assume that no distortion has occurred, it can lead to misinterpretations regarding the size and shape of the foot, thus misidentifying the dinosaur that made it. Figure 16.3  Top panel shows the process of making footprints, how they preserve, and the possible results. (From left to right) A dinosaur

walks on sediments that are the right grain size and have sufficient water content and density to preserve a footprint. This skin-sediment contact forms a true track, or mold. The depression is then filled with sediments that remain stuck in the print. If this infilling (or infilled track) becomes separated from the surrounding sediments, it will form a natural cast. Infilled tracks may show little topographical relief, and thus could be easily overlooked. Additionally, there are undertracks that result from sediments deformed by the weight of the dinosaur. Overtracks (not shown) result when thin layers of sediment above a trackbed record indistinct depressions of the tracks below them. Neither accurately reflect the size and shape of the original foot. After erosion, however, these are all that may remain. The bottom panel shows the possibilities that could form from the taphonomic alteration of a single theropod footprint, depending on the depth of penetration and the type of substrate. (Top panel courtesy of D. Bonadonna. Bottom panel courtesy of Glen Kuban.)

In contrast, infilled tracks can result from sediments depositing within an original track. These sediments are usually of a different texture and/ or color than those in which the original track was made, but have little

16.1  On the Move: Footprints and Trackways

379

Figure 16.4  Qualities of the substrate a footprint is made in can affect the print. (A) A dog print in supersaturated muds. (B) A dog print in almost-dry sand. (C) A dog print on firm, wet sand. Which is best preserved

with the least deformation? Which is most likely to persist in the fossil record? Which conveys the most accurate information about foot shape, size, and biomechanics?

or no topographical relief when seen from the surface (so it isn’t obvious a track is present). If these infilling sediments are dislodged from the track (i.e., if after they lithify to become solid rock, they are eroded out of the depression) they form a natural cast, which can produce a high fidelity, three-dimensional copy of the foot (Figure 16.3, top right). This is not to be confused with an overtrack, which is a thin layer of sediment that may settle into a track, obscuring some of the detail of the tracks beneath them.

16.1.2 Effects of Substrate As seen in Figure 16.3 (bottom panel), the texture, consistency, and moisture content of the sediment plays a role in what is preserved of a track, and to what degree. Substrate factors that affect preservation of footprints include: • Vegetation: Are you more likely to leave tracks on a grassy lawn, or a sandy beach? Walking on a highly vegetated surface is not likely to leave distinct footprints—plants absorb much of the pressure applied by an animal, preventing compression of the sediments that are needed to retain a footprint. Thus, to preserve a footprint into deep time requires a surface largely free of vegetation. • Sediment consistency: If sediments are too soft or wet, the footprints collapse or fill back in (mud collapse), and information on shape and size can be distorted. If they are too dry, the footprints won’t appear in the first place (Figure 16.3 bottom panel, Figure 16.4). • Sediment grain size: Small grain size—muds or fine-grained sands, as shown above—have the ability to create more detailed impressions of a foot, the same way a screen with more pixels allows an image to be shown in higher resolution. Conversely, a dinosaur walking on gravel is not likely to leave readable footprints, no matter how heavy it is. The same factors that contribute to footprint preservation also provide information about environmental differences—we can tell much about where dinosaurs were actually living and functioning by examining grain size, moisture content, nearby plant materials, and indicators of humidity or aridity in sediment substrates containing dinosaur footprints.

16.1.3 Footprint Taphonomy The factors that influence the formation and preservation of footprints are all important to remember when interpreting the data they hold. Just like taphonomic processes acting on bone can lead to false conclusions

380

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

if not accounted for, footprints also undergo taphonomic change that can lead to misinterpretation if not properly addressed. This happened most notably after some theropod trackways were found along the Paluxy River in Texas in the early 1900s. Later excursions identified many additional tracks, including some assigned to the feet of a blunt-toed sauropod, as well as many more tracks of a large, three-toed theropod (Figure 16.5). The sauropod and theropod dinosaurs that had left these tracks had clearly walked through some fine-grained muds of just the right consistency to preserve many tracks with exquisite detail. Although sauropods are massive quadrupeds, their ancestors were facultative bipeds, and this history is reflected in the fact that the front feet of these massive animals are sized and shaped differently than the hind feet; their manus (hand) prints are almost round, and their pes (foot) prints are more triangular and often show claw marks. In addition, some sauropods carried more weight on their back legs, while others (including, perhaps, these track makers) put more weight on the front. These factors can cause the fore- and hindfeet to penetrate the sediment to different depths, contributing to different preservation potential, depending on the substrate. These Texas trackways are interesting from another standpoint as well. In some, sauropods appear to be walking in parallel, which supports herding behavior (see also Figure 16.14). It has been proposed that the theropod tracks intermingling with the sauropod tracks may have been a hungry predator eyeing a potential sauropod dinner! Sections of the trackways were removed and sent to different institutions for study after their discovery. R. T. Bird, who discovered the tracks, suggested that they might indicate a chase or an attack because the theropod and sauropod tracks seemed to converge at the same place. However, others think that is unlikely, because there is no change in gait or irregular steps recorded in either the sauropod or theropod trackways. It may be that the theropod was following at a distance, or that it just happened to travel the same path as the sauropod at a later (but not much later) time. All agree, however, that there are areas where the

Figure 16.5  (A) Original image of the Lower Cretaceous theropod and sauropod trackways discovered by R. T. Bird in 1938 in the Paluxy Riverbed near Glen Rose, Texas. (B) The same image with trackways labeled for clarity. Left hand (yellow) arrows mark

a bipedal theropod trail, and right hand (blue) arrows indicate alternating footprints of a sauropod. It has been proposed that this trackway shows a dinosaur “chase scene”, with the theropod chasing and finally catching its enormous prey. However, it is hard to ascertain if the theropod was trailing it or just happened to pass through the same area at a different time. (Image courtesy of the American Museum of Natural History.)

16.1  On the Move: Footprints and Trackways

381

theropod tracks deform the underlying sauropod tracks, so it must have come after the big plant-eaters—just how long after is still unclear. The theropod tracks in this same region in Texas may also shed light on different biomechanics of walking. When theropods are walking digitigrade, as their foot skeleton suggests they typically do, the footprints reflect this by showing only digits with clawed toes and the fleshy “ball” of the foot. However, some trackways also preserve metatarsal tracks (Figure 16.6B), which indicate a change in the way they walked (Figure 16.6C). The theropod that left these elongate metatarsal (“heel impressed”) tracks was walking with more of its foot in contact with the ground, possibly crouched over. These elongate, narrow metatarsal tracks can also undergo taphonomic alteration, as suggested in Figure 16.6A, including loss of clawed digit information. In the past, these tracks have been misinterpreted by some groups as evidence of giant humans walking with dinosaurs.

16.1.4 Tracks vs. Trackways Depending upon what survives taphonomic processes, we may find an entire series of prints (e.g., a trackway), or a single, isolated track where other tracks were either eroded or not preserved. Each provides different types of information about a dinosaur’s life.

16.1.4.1 Individual Tracks From an individual track, we can gain much more information than you might expect. For example, a single, well-preserved footprint can provide information on what direction the animal was facing when it left the track. Additionally, a footprint can tell about the biomechanics of walking by looking at pressure marks or pressure-release patterns (Figure 16.7), which shed light on the biomechanics of their foot, and how the muscles worked against the bones to help the foot traverse Figure 16.6  (A) A distinct “metatarsal track” and how it may be taphonomically altered from the original shape. The actual metatarsal track (A) can undergo “mud collapse” (B), where soft sediment slumps back into the digit impressions, obscuring them. Alternatively, these same tracks can undergo erosion or infilling (C), making them appear shallow and indistinct, and causing the loss of digit information. Although theropods usually walk digitigrade (where only the toes and ball of the foot contact the ground) these bipedal dinosaurs could sometimes adopt a plantigrade habit, impressing the entire “sole” and “heel” of the foot into sediments as they walked (D). When these elongate prints are

taphonomically altered, they sometimes can resemble very large human footprints, for which they have been mistaken. Many metatarsal tracks in Texas appear to have been made by rather small, gracile theropods, perhaps ornithomimids, walking in a crouched position that made foraging for small food items easier. The animal’s right hindlimb in D shows the foot posture that would have left a metatarsal track. (Images courtesy of Glen Kuban.)

382

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

varying sediments. To illustrate this, compare the changes in your foot if you are walking on soft sand versus a hard surface. On sand, your toes might curl slightly to get a better grip, and your foot sometimes slides back a little bit. Often, your heel will go deeper in the sand, indicating where you put the most pressure on your foot during locomotion. If the substrate is muddy or slippery, your toes curl tighter. Now, imagine running across that same sandy surface. Would that change where and how your foot interacts with the sand? Maybe your heel and toe would be similar in depth of penetration, as the push-off forces would be greater in running. Maybe the curl of your toes would be lessened. Those are very different biomechanical patterns than if you are walking on the tile floor in your kitchen. Although dinosaur feet are very different from your feet, dinosaur foot biomechanics would also have had to change with different substrates. Sometimes the toes angle downward in softer sediments, and in deep tracks (in softer sediments), there may be evidence of claw marks or splaying of digits that reflect these adjustments. A footprint can also tell us about the soft tissue anatomy and functional shape of the foot, and how it interacted with the substrate—something the bony skeleton cannot. This includes imprints of skin, and the size, extent, thickness, and curvature of the keratinous sheath that overlays the toe bones, as seen in Figure 16.8. Depending upon the size and shape of the claw sheath, some dinosaur feet were functionally larger, and their toes sharper than the bones would indicate! In modern birds this sheath can extend the functional length of the toes significantly, and depending upon the curvature, it can greatly increase the efficiency of grasping. Additionally, footprints can reveal information about the digit pads beneath the toes, and the shape of the instep. From looking at the curvature of the toes, we may even tell if a single footprint was made by a left or right foot. Footprint data suggests that the digits of the hadrosaur hindlimb were encased in a keratinous sheath, much like the toes of modern horses and other animals (Figure 16.9). Part of the evidence for this is morphological—the surface vascularity we see on their bones is often correlated to a keratin covering. However, in addition to this osteological data, footprints left by their hind feet are three-toed and blunt-ended, consistent with a hoof-like sheath on these digits (rather than claws). Additionally, manus prints for hadrosaurs suggest that their fingers were Figure 16.7  This tridactyl (three-toed) footprint was found in Dinosaur Valley State Park. Can you assign this

print to a particular dinosaur group (e.g., theropod, sauropod, ornithopod)? What can you say about how this dinosaur was using its foot? Is this digitigrade or plantigrade? Was it digging its front toes in deeper than the back of the foot? Where is the rest of the foot? What direction is it going? Is it a right or left track? Is this a true track, undertrack, or overtrack? There is much information to be had from an individual track! (Courtesy of D. Turner, https://commons.wikimedia.org/wiki/ File:Dino​saur_​Valle​y_Sta​te_Pa​rk_-_​Track​ 2.jpg​.)

16.1  On the Move: Footprints and Trackways

383

Figure 16.8  (A) This mummified bird foot shows the extension of the claw sheaths over where the toe bones end (arrows). (B) A similar feature is seen in the foot of the first identified bird, Archaeopteryx. Keratin is not normally

not completely separated digits, but were actually covered in a fleshy mitt, binding them more closely together than you would expect from the bones themselves.

mineralized in birds, and these claw sheaths are not predicted to have high preservation potential; however, more and more keratin structures are being found with fossil bones in ancient vertebrates. These originally unmineralized features tell us a lot about how these early birds used their feet. The claw sheaths show that the functional reach of the foot was greater than the skeleton alone reveals, and the curvature of the claw shows how they might have used these in walking, perching, or capturing prey. (A courtesy of K. Tiffany; B adapted from by E. Willoughby, https://commons.wikimedia. org/wiki/File:Berl​in_Ar​chaeo​ptery​x_-_d​etail​ _of_f​eet.j​pg.)

A footprint can also inform us on how the dinosaur used its feet. Dinosaurs, even the massive sauropods, had a digitigrade posture in their hindlimbs—that is, they walked on the “balls” of their hindfeet, and footprints can preserve this information (Figure 16.10). However, manus prints of sauropods such as titanosaurs (which you will recall from Chapter 9 have completely lost their digits) support that they walked on the tips of their vertically oriented metacarpals, more similar to an unguligrade posture than a digitigrade one. Finally, a single footprint can shed light on the type of environment the dinosaur was passing through, and verify that a particular taxon was indeed present and inhabited that type of environment. What can you

Figure 16.9  (A) The ungual (top) and hoof (bottom) of a modern horse.

The edges of this bone are bumpy and are filled with small openings for blood vessels. When we see this in bone, it is almost always covered in keratin. We know this is the case with horses, as the bone is tightly covered by the thick keratin hoof. (B) Brachylophosaurus foot (bottom) with enlarged view of one ungual (top). The Brachylophosaurus ungual is almost the same overall shape and texture as the horse, except these dinosaurs walked on three toes, not one. (Images are not to scale.) (A courtesy of K. Tiffany; B courtesy of M. Schweitzer, taken at the Museum of the Rockies, with permission.)

384

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

Figure 16.10  Various hindfoot postures observed in living mammals: (A) human, (B) monkey, (C) dog, (D) sheep, and (E) horse. The human

and monkey (A and B) show plantigrade posture, where the entire foot (phalanges, metatarsals, and tarsals) including the heel are in contact with the ground. The dog (C) shows a digitigrade posture, where only the digits are in contact with the ground, while the metatarsals and tarsals are lifted. The sheep and the horse (D and E) show unguligrade posture, where only the last phalanx in the digit (the ungual) is in contact with the ground. (Adapted from J. LeConte, https://flic.kr/p/oupvCG.) Figure 16.11  Trackways may preserve environmental information about the regions in which the dinosaurs were living. What can you say about the

environments in which these dinosaurs walked? What does the footprint in (B) tell you about this dinosaur and where it lived? (A courtesy of Glen Kuban; B Courtesy of the Utah Geological Survey.)

say about the animals that made the footprint in Figure 16.11? In what type of environment were they moving?

16.1.4.2 Trackways We can get all the information from a trackway that we can from a single footprint, and more. A trackway is two or more footprints in sequence from the same animal. Trackways can tell us the direction the animal was moving, as well as community information. How many different kinds of animals are represented in Figure 16.12? Do you think they interacted? Do you think they were present at the same time? How could you tell? Trackways can also tell us about animal posture—not whether it stood straight or slouched, but what it did with its legs and tail, and how they were oriented relative to the body. Knowing what you know about key synapomorphies of dinosaur posture (Chapter 7), what two features in Figure 16.13 allow you to eliminate the trackmaker as a dinosaur? What other behavior can you deduce from this trackway? Trackways can tell us about movement within a group as well. Do you think the animals in Figure 16.12 were all present at the same time? Were they moving together? How about the animals in Figure 16.14? Trackways such as these have the potential to show:

16.1  On the Move: Footprints and Trackways

385

Figure 16.12  You can probably guess why this region is named Dinosaur Ridge. These Mesozoic sedimentary

rocks testify to the presence of a dinosaur community, because scientists have identified 325 dinosaur footprint at this site, made by about 37 individual dinosaurs. The sediments represent a tidal flat that bordered the ancient Western Interior Seaway. How many different types of prints do you see? (Courtesy of J. St. John, https:// flic.kr/p/dByJid.)

Figure 16.13  What do you see in this trackway that tells you it was not made by a dinosaur? What direction are the hands and feet pointing, relative to the midline of the body? What kind of gait does this imply— erect, semi-erect, or sprawling?

(Courtesy of NeilsPhotography, https://flic. kr/p/4zDaL5.)

• Whether dinosaurs are traveling together: In Figure 16.14, at least some of these sauropod trackmakers were most probably moving together because the tracks run in parallel and all show similar depth and clarity. • Possible interactions between groups: The presence of footprints from other dinosaurs may reveal reactions to the presence of others (see below). • A lack of evidence for tail dragging: Unlike crocodiles or lizards, which do drag their tails. As you know from functional morphology studies (Chapter 13), bones are useful in determining the maximum potentials of movement. Trackways, however, show how they actually moved. For example, trackways can show how fast dinosaurs habitually walked or ran, which is different from the fastest speed of which their bodies are capable. Think about a time where you ran as fast as you possibly could. Do you move that fast

386

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

Figure 16.14  Three parallel trails of Lower Cretaceous sauropod tracks, along with (mostly) parallel trails of a large theropod—probably Acrocanthosaurus. What do these

parallel trails suggest about the sauropod lifestyle? Can you tell which are manus (front) prints and which are pes (rear) prints? What direction are they moving? Is the theropod moving in the same direction? Notice that, unlike trails in Figure 16.12, the most prominent sauropod trail in this photo shows no manus prints. Why not? Do you see tail marks? Why or why not? What might this “missing information” indicate? Were the dinosaurs that made these tracks all present at the same time? (Courtesy of Glen Kuban.)

while shopping for groceries? Walking to work? How often do you actually move at your top possible speed? Trackways record dinosaurs at the speed of their daily life, not (usually) the moments of their absolute limits. Although trackways can inform us at the speed at which different dinosaurs moved, and the gait they employed, to get this information from footprint data, we rely on measurements taken directly from the trackways themselves. There are four measurements (Figure 16.15) that we need to calculate an estimated speed for dinosaurs from trackways: • Foot length: The length of the foot (toe to heel) is sometimes more accurately taken from trackways than the skeletal foot, because the skeleton lacks soft tissue that affects its dimensions (e.g., the keratin claw sheaths). • Leg length/hip height: The length of the dinosaur’s leg can be estimated from a single footprint by multiplying the foot length by four. This is only an approximation, and in cases where the trackmaker can be narrowed down to a specific group, these data can be more accurately estimated from the skeleton. However, in cases where that is not possible, quadrupling the foot length gives a workable estimate. Try it on yourself! • Stride length: The length of two steps, which in a trackway is (for example) the distance from the heel of a right footprint to the heel of the next right footprint. • Relative stride length: This is a value calculated by dividing the measured stride length by the estimated leg length.

16.1  On the Move: Footprints and Trackways Figure 16.15  The diagrams here show some of the key measurements commonly taken on a bipedal trackway, which are useful for studying the efficiency of gaits and estimating the speed of the trackmaker using a formula developed by R. McNeil Alexander.

(Courtesy of Glen Kuban.)

These measurements can be plugged into a mathematical formula developed by R. McNeil Alexander to give an estimate of the speed the trackmaker was traveling when it left the trackway. They can also be used a bit more simply to give us a more general idea of their speed. For example, a relative speed (stride length/leg length) of less than two indicates the animal was probably walking, two to three, it was likely trotting, and greater than three indicates the animal was running. These hypotheses are based on observations of these ratios in living animals. Trackways can be used to compare average dinosaur speeds across taxa. For reference, the average human walks at about 3 mph, but the Olympian gold medalist Usain Bolt has been clocked running at 27.8 mph (44.74 kph)! Conversely, trackways support a range of speeds for dinosaurs, from only 2–3 mph (3.2–4.8 kph) for sauropods and ankylosaurs to ~10 mph (~16 kph) for most theropods. Rare trackways have shown that some theropods could move at estimated speeds of 25–27 mph (~42 kph) (Figure 16.16), giving Usain a “run” for his money! Is there data to support the possibility that a running Tyrannosaurs rex could have kept pace with a jeep going 35 mph? Not so far. However, the likelihood of finding a trackway recording the top speed of a T. rex or any other dinosaur is extremely rare, because as mentioned above, most animals spend the majority of their time walking relatively slowly—much

387

388

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

Figure 16.16  Some theropod trackways may show a running gait. This trackway, from Glen Rose,

Texas, was probably made by the large theropod Acrocanthosaurus, the “Terror of the South”. It shows a pace (remember the difference between pace and stride) of almost six feet. Combined with measurements of foot length and an estimate of hip height, Alexander’s formula indicates a running speed for this dinosaur of about 25 mph! So much for the slowmoving, tail-dragging dinosaurs of the past! (Courtesy of Glen Kuban.)

slower than at their possible top speeds. Only rarely do they need to exert the energy required to achieve full speed, like when trying to catch prey or evade a predator. This is reflected in the low average speeds determined from trackways. In addition, the substrate that is best for preserving tracks is the worst for running fast. Imagine sprinting in mud versus on asphalt. Your speed would definitely be higher on the asphalt and much more reflective of your actual top speed, but asphalt would leave no evidence of your sprint. Mud would record your tracks, but it wouldn’t represent your maximum speed very well. The same is true for dinosaurs, and so maybe T. rex could catch a 35-mph jeep after all. Sometimes, trackways can confer phylogenetic information. For example, one skeletal trait that is used to differentiate diplodocid sauropods (e.g., Diplodocus) from titanosaurs (derived macronarians like Rapetosaurus) is their stance. Diplodocoids are hypothesized to have had a narrower stance, with their feet placed closer to the midline. Conversely, based upon the way the head of their femora are angled, titanosaurs are hypothesized to have had a wider stance (i.e., “wide-gauge” posture), with their feet more widely separated. Thus, when we find sauropod tracks that are narrow, this is consistent with a diplodocid trackmaker, whereas footprints spaced more widely from the midline are more consistent with a titanosaur trackmaker (­Figure 16.17). Trackways can also inform us as to whether dinosaurs moved in groups, like herd animals today. For example, when we see parallel tracks of the same shape (and therefore, presumably made by animals of the same species) with little or no overlap (as in Figure 16.14), we can hypothesize that these individuals may have walked side by side, going in the same direction. On the other hand, if the tracks greatly overlap, perhaps they were walking behind lead animals—like cows or bison do today—or were following the same path at a different time.

16.1  On the Move: Footprints and Trackways

389

Figure 16.17  Drawing depicting the skeletal reconstructions of the hips and hindlimbs of (A) diplodocoids and (B) titanosaurs, with the corresponding trackways. Based on

differences in their femoral anatomy, diplodocoids are hypothesized to have a narrower posture, and therefore trackways closer to midline, than titanosaurs. (Courtesy of S. Hartmann.)

If trackways seem to consist of only one type of animal, they may reveal whether or not there was any kind of internal organization, reflecting herd or social structure. Some ornithopod trackways seem to show large prints on the outside of the group, with smaller, but similarly shaped tracks, on the inside. Could this mean when dinosaurs traveled in packs, they kept the young inside the herd for protection like a modern elephant or buffalo (Figure 16.18)?

Figure 16.18  Some herd animals, like these elephants, keep their young in the center of the group when they migrate to protect them from stalking predators. It is reasonable to think that

dinosaurs may have as well. (Courtesy of M. Fuchs, public domain.)

390

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

16.1.5 Ichnotaxonomy In Chapter 11, we discussed the difference between trace fossils and body fossils. Tracks and trackways are examples of trace fossils—fossils that record behavior. The study of trace fossils, including trackways, is called ichnology. The classification of trace fossils, rather than phylogeny, is called ichnotaxonomy. In ichnotaxonomy, trace fossils get their own names and classifications. Why do you think it is that a taxon—a unique and identifiable group of organisms, is not the same as an ichnotaxon? In part, it is because more than one animal can make very similar tracks (Figure 16.19). Similarly, the main problem in dinosaur trackway interpretation is identifying with certainty which dinosaur made which tracks; assigning a trackmaker to a particular track pattern is exceedingly difficult. For example, we know that theropod dinosaurs all have three toes, and these consist of two-to-three phalanges on each, ending in a clawed ungual (Figure 16.20). However, all theropods have this pattern! Of course, size can be taken into account, but how can we differentiate tracks from a juvenile T. rex and a full-grown ornithomimid? Also, we know that dinosaurs changed many features when they grew from young to adult, making it difficult to say with certainty whether skeletal variation represents

Figure 16.19  The difficulty with trackways is knowing for certain who made the tracks. Which of the six birds

shown here are responsible for the trackway on the right?

Figure 16.20  (A) Cast of the foot of an ornithomimid, compared with (B), a theropod trackway. Could this particular

dinosaur have left these tracks? Which other dinosaurs may have? (Courtesy of K. Tiffany, B courtesy of Glen Kuban.)

16.1  On the Move: Footprints and Trackways Figure 16.21  This diagram shows several major dinosaur groups, the typical track shapes they make when well preserved, and the track names (ichnotaxa) commonly associated with each. However, because many

dinosaurs within a group had very similar feet (which increase and possibly change as they grow), and many variables track formation and preservation such as sediment consistency and composition affect the depth and quality of prints (see Figures 16.3 and 16.4), it is often only possible to associate a set of tracks to a group rather than a particular species, genus, or even family, or a particular ichnotaxon. (Courtesy of Glen Kuban.)

a separate species or an immature form of a familiar adult. The same is true of footprints—in addition to expanding in length, dinosaur feet may have changed shape in ways that make it difficult to assign. Other factors that make assigning a track to a particular trackmaker difficult include taphonomic processes that make many tracks indistinct or distorted (discussed above). Of course, the difficulties of assigning tracks to trackmakers haven’t stopped us from trying, and paleontologists have been able to link certain patterns to certain groups of dinosaurs—at least at higher taxonomic levels. To do this, we use the shape (skeletal morphology) of the foot bones to estimate what it might look like when muscles and tendons are included, then try to match that to what we find in the fossil record. Through this process, we can classify ichnotaxa like the ones in Figure 16.21. Just like we can classify theropods, ornithopods, thyreophorans, etc., based upon their shared derived morphological traits, we can also identify features by which to classify trackways and footprints. Some of the features we use to classify footprints include: • Number of digits • Orientation, placement, and angle between digits • Relative size of digits • Shape of digits (straight, curved, etc.) • Overall size • Arrangement of digit pads (see below) When a trackway (and not just an individual footprint) is present, we can also use: • Spacing between tracks • Speed • Pace • Posture Figure 16.22 shows how this might work using a modern example.

391

392

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

Figure 16.22  This bird trackway might be potentially analyzed as follows: number of digits = four; orientation = three anterior-facing digits, one posterior-facing digit (anisodactyl); angle between digits = ~90o; relative size of digits = anterior digits approximately equal in size, posterior digit is shorter; digit shape = digits are straight; overall size = medium; spacing between tracks = overlapping.

(Courtesy of W. Baxter, https​://ww​w.geo​ graph​.org.​uk/ph​oto/5​76255​6.)

Examples of the patterns that emerge in trackways assigned to various groups: • Sauropods: These quadrupedal dinosaurs make trackways with forefoot (rarely complete) and hindfoot prints. The hindfoot, or pes, is larger than the forefoot and is roughly triangular with the broadest part toward the front, and it bears three large claws and two smaller, blunter ones that angle away from the midline of the foot. On the other hand, the forefoot is slightly smaller, almost round, and does not preserve claw prints, consistent with skeletal data suggesting the distalmost digit is lost in most sauropods (Figure 16.23). • Ornithopods: These facultative quadrupeds sometimes preserve fore prints along with their hind prints. The former are only made when the animal is walking quadrupedally and is somewhat kidney-shaped. Their hind prints show three broad and blunt toes (Figure 16.24). • Theropods: Members of this group usually show three toes which are narrower and longer than those of three-toed ornithopods. Theropods have narrow, sharp claws, and a middle digit that is longer than the other two. Well-preserved prints may show digit pads (Figure 16.25). Manus prints have not been observed in theropod trackways, confirming their obligate bipedality. Although we can assign footprints to a group such as “theropods”, we cannot assign them more specifically to a taxon such as Tyrannosauridae. Figure 16.23  (A) Forelimb (left) and hindleg (right) of sauropod dinosaurs. (B) In sauropod tracks, the footprint is shaped like a broad triangle, widest in the front. In most cases, impressions of claws can be detected. Manus prints are almost round, unless distorted, usually from being stepped upon by the rear foot on the same side as the animal continues to walk. (C) Example manus and pes prints from a sauropod. Compare with the diagram in (B). Is

this a right footprint or a left footprint? (A courtesy of K. Tiffany; B and C courtesy of Glen Kuban.)

16.1  On the Move: Footprints and Trackways

The fact is, feet look pretty different with skin on, and the only way we can be sure that a particular dinosaur made a particular trackway is to find the skeleton of one in the middle of the trackway. And that hasn’t happened…yet. Thus, these ichnofossils get their own taxonomic names, like Tyrannosauripus or Grallator.

393

Figure 16.24  (A) Ornithopod tracks are tridactyl (three-toed), like theropod tracks, but differ in that typically, they are as wide as they are long. Ornithopod digits are spread relatively far apart, and the toes are blunt-ended, with no visible claw. This is why we think that these dinosaurs had keratinous structures on their ungual (last) digit that were similar to hooves. Remember that these dinosaurs were facultative bipeds, so a manus print may or may not be included in ornithopod trackways. If manus prints are present they are usually smaller and may or may not show digits. Interestingly, in trackways, these dinosaurs often show a “pigeon-toed” gait (B), with feet turned slightly inward, whereas theropod feet are oriented straight ahead. (Courtesy of Glen Kuban.)

Although we can infer certain behaviors from tracks, one thing that has not been definitively observed in a dinosaur trackway, as mentioned above, is evidence of tail dragging—robust evidence that our early reconstructions of dinosaurs as tail-draggers were totally incorrect. Additionally, although it has been proposed that some sauropods could perhaps have reared up on their hindlegs (as depicted in the iconic Jurassic Park scene), the trackways we have recovered have not recorded this behavior. This does not indicate that sauropods never did so, as unlike tail-dragging, rearing would have been an infrequent behavior for sauropods, even if they did do it. It is important to remember that just because biomechanical studies of dinosaur bones show that they could have behaved in a certain manner does not mean that they did. Thus,

Figure 16.25  Theropod tracks are also tridactyl, but the toes are longer and narrower than those of ornithopods.

Some tracks, such as this one, show sharp claws on the end of the digits, and the middle claw points toward the midline of the foot—allowing us to determine if the foot is a right or left. “Toe pads” may preserve as impressions, giving additional evidence about soft tissue anatomy of the foot. If present, they help assign a track more precisely to ichnotaxon. Rarely, these tracks can be preserved with skin impressions (inset). If skin impressions are present, we know for certain that this is a “true track” rather than an over- or underprint, because it shows direct contact of the sediment with skin. (Courtesy of Glen Kuban.)

394

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

tracks and trackways are additional, important indicators of actual behavior.

16.2 DINOSAUR GRAVEYARDS: MASS DEATH ASSEMBLAGES After reading this section you should be able to… • Summarize the evidence for herding in various dinosaur groups from mass death assemblages.

A large herd of zebra on the Serengeti, or cows (or bison) in Montana, might be familiar images that spring to mind when thinking about animals that gather in groups. However, living, moving, migrating, and nesting in such herds are a derived trait for terrestrial vertebrates, and are relatively rare in today’s world—especially outside of mammals. When extant “reptiles” do come together in groups, the groups are relatively small, usually short-lived, and generally for the purposes of mating. Not many travel in large groups over long distances. In a way, this is fortunate for humanity—you don’t have to worry about thousands of migrating crocodiles when you travel to Florida, and the concept of millions of migrating snakes is probably unpleasant for most of us! However, even though herding and migration aren’t common for terrestrial vertebrates, it does happen, and it can be spectacular. Hundreds to thousands of caribou migrate across the tundra every year, and when Lewis and Clark first traveled across the prairies of the Midwest, they reported herds of bison so numerous that they couldn’t see the land for the back of the animals. Some species of birds, of course, move in large flocks as well, and in the past, flocks of passenger pigeons (now extinct) were so thick they could block the sun. But what about dinosaurs? If crocodiles do not form large groups, but birds sometimes migrate and/or nest in large groups, the phylogenetic bracket suggests non-avian dinosaurs could have followed either strategy. Is there evidence that dinosaurs migrated in herds? What indicators of group dynamics might we find in dinosaurs? We have already discussed trackway data, and trackways provide evidence for monospecific herds of dinosaurs moving together over long distances. But given the limitations of interpreting footprints, what other evidence exists to support the hypothesis that some species moved in herds? We know that when extant animals migrate in herds (particularly large mammals like water buffalo or caribou) the entire herd or large portions of it can sometimes be destroyed in a disastrous event, such as a flash flood while crossing a river. In such an event, the bodies of these drowned herd animals can pile up until the river is clogged (Figure 16.26). As the carcasses rot, the bones jumble together and are buried in a massive collection of many individuals of the same species. This type of death assemblage is exactly what we see for some dinosaur groups. It is hard to explain such massive accumulations of bones, all belonging to a single type of dinosaur, if they didn’t live together and move together, at least at some point in their lives. We occasionally see cases of massive accumulations of herbivorous dinosaurs—species of ceratopsians and many types of hadrosaurs, and smaller groups of sauropods. However, this pattern is not observed in all dinosaur clades. There are only a few examples of predatory dino-

16.2  Dinosaur Graveyards: Mass Death Assemblages

395

Figure 16.26  (A) A herd of wildebeest migrating across the Masai River. During such migration, it’s not uncommon for quite a few to perish (B). Sometimes, in cases of stampedes

or flash floods, many hundreds may die, and may even clog the river. (A courtesy of C. Michel, https://commons.wikimedia. org/wiki/File:Migr​ating​_wild​ebees​t_on_​ the_M​asai_​Mara.​jpg; B courtesy of shankar s., https://commons.wikimedia.org/wiki/ File:Dead​_wild​ebees​t_in_​the_M​asai_​River​ _(751​35834​26).j​pg.)

Figure 16.27  (A) A block taken from the Ghost Ranch quarry, showing the close proximity in which numerous individuals of Coelophysis died. (B) An articulated Coelophysis from the Ghost Ranch quarry. Monospecific

saurs being found in such large death assemblages. Close to a thousand small Triassic coelophysoids have been found in large bone beds at Ghost Ranch in Arizona (Figure 16.27). In another case, bones from close to 50 Jurassic Allosaurus were found in a massive deposit called the Cleveland-Lloyd quarry. But these are the exceptions to the rule. Coelophysoids were early dinosaurs, and very small. Living in groups might have been selectively favored so that these could hunt larger prey more effectively. In the case of allosaurs recovered from the Cleveland-Lloyd quarry, it has been proposed that, rather than living and traveling in such large groups, these animals were instead caught in a “predator trap”. There is evidence from the sediments that river channels may have occasionally overflowed, filling connected channels with fine-grained muds that trapped the dinosaurs unlucky enough to be caught in them. In addition to the many Allosaurus present, there are other predatory dinosaurs, and many herbivorous dinosaurs, including sauropods, stegosaurs, and ornithopods. This distribution has led some to argue for a muddy dinosaur trap—in which when some large prey dinosaurs get stuck, and the predators that come to eat them also get stuck—and also that Allosaurus, at least, may have hunted in packs, explaining the atypical predator to prey ratios. Beyond these, we have no other definitive evidence of theropods living or migrating in large groups. For example, we do not often see trackways with multiple theropods represented. Similarly, predators today do not usually form large herds, but are rather solitary animals, or at most form small hunting packs like wolves, lions, coyotes, and hyenas.

bone beds like these support the idea that some dinosaurs lived in groups. Although such behavior is unusual for theropods, or, in fact, vertebrate carnivores alive today, these dinosaurs were small enough that perhaps group behavior to facilitate pack hunting was favored, allowing them to take down larger prey. (A adapted from Paleeoguy, https://commons.wikimedia. org/wiki/File:CMNH_Coelophysis_Block. jpg; B courtesy of M. Ryan, https://flic. kr/p/9abCAu.)

396

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

16.3 INJURIES AND SICKNESSES: PALEOPATHOLOGIES After reading this section you should be able to… • Define paleopathology. • Infer what a specific injury can tell us about the behavior of an organism. • Differentiate between interspecific and intraspecific combat. • Describe evidence for disease that can be found in dinosaurs.

Everyone reading this text has been sick or injured at some point in their life. Such occurrences, whether they are relatively minor inconveniences or life-threatening events, stimulate biological responses to fight illness and heal wounds. But what about dinosaurs? Although you may have never thought about it before, dinosaur lifestyles would have resulted in diseases and injuries as well, just like all animals today. However, unlike humans and the animals we associate with, dinosaurs did not have medical doctors or veterinarians to turn to for sutures, antibiotics, surgery, or other services to augment their natural healing process. What kinds of injuries did they sustain, and how did they heal? How can we tell if an injury was fatal? Importantly, what can this information tell us about dinosaur behavior—who they interacted with and how they lived? The study of injuries and illness in extinct organisms is called paleopathology. It uses many of the same techniques and approaches as modern medical diagnostics or forensics to diagnose pathologies in animals long after they have died, using the marks these pathologies have left on their bones. Pathologies can arise from either injury or disease. The patterns revealed by injuries of an organism can shed light on either predator–prey interactions, or alternatively, interactions between members of the same species arising from competition for mates. Conversely, pathological patterns that arise from disease states, such as infections, cancers, or the like, inform on the paleobiology of the individual bearing them. Pathologies are common in dinosaur fossils. Broken bones, offset fractures, arthritis, and various diseases are present in almost all dinosaurs by the time they reach adulthood. Even the earliest dinosaurs, including specimens of Herrerasaurus, show signs of pathology. But how do we recognize pathologies in dinosaurs, and what can these tell us about the not-so-easy life these animals led? Moreover, can a better understanding of dinosaur diseases shed light on our own?

16.3.1 Injuries We can observe many dinosaur specimens bearing the marks of injuries. The majority of these are the result of bites or bone fractures, but the relative expression of this type of injury is no doubt influenced by the fact that both are injuries that leave clear and distinctive marks on the bone. Unless soft tissues are preserved, only injuries that cause trauma to the skeleton itself can be observed in dinosaurs. For example, a case of influenza, or a cut that caused fatal bleeding but missed all the bones, or even a cancer that did not invade the bone, would not leave evidence on the skeleton, and thus would be invisible to a dinosaur ­paleopathologist.

16.3  Injuries and Sicknesses: Paleopathologies

397

If many of the dinosaur specimens we unearth are broken by taphonomic forces, how can we tell when a break is the result of an injury sustained during life? One way is to look for signs of healing. If an animal sustains an injury that didn’t instantly kill it—that is, if it lived for some time after the injury occurred—its body will attempt to repair the damage. However, once an animal dies, life processes such as healing cease. Thus, if we find evidence that a broken bone has started healing, we know that it must have been alive both when the break occurred, and for some time after. One example of diverse and extensive injuries in a dinosaur—and evidence of their initial healing—can be observed in an almost complete, subadult specimen of Allosaurus, which was found in 1991 on the border between Montana and Wyoming (Figure 16.28). Nineteen of the bones of this theropod dinosaur showed signs of fracture or infection. The most common injuries seen in this individual (and most other dinosaurs) are injuries to the spine and ribs—such as bite marks, fractures, and bony overgrowth (e.g., osteoarthritis). This one young animal exhibited all these injuries, and many others. Like all vertebrates, this young Allosaurus possessed ligaments running along its spine, which contributed to its stability. Ligaments are usually flexible, because they function to stabilize joints and so must move when the joints do. But, in this individual, some of the ligaments supporting the spine had become ossified (that is, turned to bone) (Figure 16.29, blue arrows)—rendering them stiff and brittle. This would have been extremely painful and debilitating for this subadult dinosaur. We know that in living vertebrates, trauma will induce this type of hyper mineralization in tendons and ligaments. How do you think this might have affected this Allosaurus’s ability to catch its dinner?

Figure 16.28  This almost complete skeleton of a juvenile Allosaurus, on display at Montana’s Museum of the Rockies, shows many pathologies, even though it had not yet reached adult size. (Adapted from T. Evanston,

https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=27​36373​7.)

Figure 16.29  The vertebrae, ribs, and ilium of a subadult Allosaurus fragilis.

Blue arrows show where the ligaments that help to stabilize the spine have ossified (turned to bone) in response to an injury. The yellow arrow shows a deep depression in the ilium, probably the result of a bite. However, this was not a lethal injury, as the bony callus surrounding it indicates the bone had begun to heal. (Courtesy of R. Hanna (2002). Multiple injury and infection in a sub-adult theropod dinosaur Allosaurus fragilis with comparisons to allosaur pathology in the Cleveland-Lloyd Dinosaur Quarry collection. Journal of Vertebrate Paleontology, 22(1), 76–90.)

398

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

A second injury resembles a bite in the blade of the animal’s hip (the ilium) (Figure 16.29, yellow arrow). This “bite” is covered with a thickened overgrowth of bone—bone growth that would not be present if this fracture had occurred postmortem. When bone is injured, the body responds in a predictable manner. First, the tissues around the bone (the periosteum) become inflamed and swollen, and often a hematoma (pooling of blood outside of blood vessels) forms. Next, new bone begins to be deposited very rapidly to stabilize the broken parts. This new bone is very porous and fibrous because it is laid down so rapidly, and is not very strong. Next, the line of fracture becomes less distinct, as healing takes place, then a soft callus forms and gradually mineralizes. This is what causes bumps you can feel through your skin in a healing fracture. Unlike humans who, when they break their bones can go to a doctor to align the broken ends, dinosaurs (and other animals) can’t set their bones. The formation of the callus holds bones that can be widely offset during an injury steady while remodeling occurs. Gradually, remodeling results in a reduction in the callus. The smaller the callus, the greater the time elapsed between injuring and healing. This sequential process (from inflammation to remodeling) is the body is trying to compensate for these injuries, and there is no reason to think that a similar cascade did not occur in dinosaurs. When the bone is infected, callus will often form through rapid bone deposition because the body is trying to limit the spread of infection (see below). Beyond the injuries in its spine, this Allosaurus shows many other broken bones that are in various stages of healing, including multiple examples of callus formation. Figure 16.30 shows a healing rib with a large callus. This particular type of injury—broken ribs with fracture calluses—is quite common in dinosaurs. What do you think this can tell us about dinosaur behavior? This dinosaur also shows other broken ribs in various stages of healing, and several ribs show bifurcation, or splitting. Although this type of bone morphology may be a developmental anomaly, it may also be the result of a blow to the side strong enough to pull the muscle away from the bone. In addition to this evidence for damage to the ribs, several vertebrae have bony overgrowths—the result of injury or disease. The neural spines (projections of the vertebrae that protect the spinal cord) show woven bone growth in response to severe injury (Figure 16.31). This changes the shape of the bone, causing them to rub against vertebrae on either side, which would have been incredibly painful.

Figure 16.30  Two ribs from this young dinosaur in different stages of healing. The callus is much larger on the

top rib, indicating that: (1) it was greatly offset when broken, and (2) these were not lethal injuries, as healing had begun to occur. The rib on the bottom is almost completely healed, and the callus is much smaller as the bone has remodeled to be closer in alignment. (Courtesy of R. Hanna.)

16.3  Injuries and Sicknesses: Paleopathologies

399

Figure 16.31  This neural spine (the part of your vertebrae you can feel if you run your thumb down your back) is normally smoothly curved on the surface, as indicated by the dotted line. This dinosaur suffered some

kind of trauma to its spine, because several vertebrae show this very painful bony overgrowth—a healing result. (Courtesy of R. Hanna.)

In addition to the many injuries sustained by this dinosaur, there is ample evidence of secondary infection, called suppurative (seeping or oozing) osteomyelitis (a type of bone infection) in many of its fossils. This could have been a result of its injuries, or it could have been caused by systemic infection. The most prominent example is seen in its foot. Figure 16.32 shows that the middle toe of this dinosaur’s left foot is greatly expanded because of extreme bony overgrowth. The dinosaur must have severely damaged this digit, which then became infected. The rapid deposition of bone as unorganized overgrowth was an attempt by the body to contain the infection. As seen in Figure 16.32A, the huge bony overgrowth would have caused the bone to dig into the sides of the neighboring toes, making it extremely painful to walk. For comparison, a normal toe bone is shown at the top of Figure 16.32B, with the infected one below. If the infection could not be contained, it would become systemic, and might explain the holes we see in other bones, such as the scapula. So what caused these injuries? We can’t say for certain, but we do know that allosaurs were the dominant predators of Jurassic sauropods. A potential hypothesis that has been put forth is that these injuries were caused when the hungry young dinosaur was trampled and kicked by a sauropod in self-defense, or in defense of its young. From assessing the evidence of such injuries, we can make inferences about interactions between dinosaur individuals, such as intraspecific combat (i.e., between members of the same species) and interspecific combat (i.e., between members of different species). For example, intraspecific face biting has been observed in many living organisms,

400

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

Figure 16.32  (A) An articulated foot of a subadult Allosaurus fragilis, showing a pathology (arrow) on the proximal middle phalanx and shaft.

(B) A normal toe bone from the other foot (top) compared with this badly infected bone (bottom). How do you think infections and damage such as these affect the potential of the bone to persist in the rock record? (Courtesy of M. Schweitzer, photographed at the Museum of the Rockies, with permission.)

Figure 16.33  (A) Face biting in wolves as a show of dominance. (B) Skull bones (top) and interpretive drawing (bottom) show bite marks to the bones of a theropod that are consistent in size and shape with those of the same species of dinosaur (arrows and numbers). (C) Reconstruction of what face biting may have looked like in theropods 70 million years ago. (A courtesy of T.

Jansen, https://commons.wikimedia.org/ wiki/File:Wolves_in_Norway.jpg; B courtesy of J. Peterson, et. al.; C courtesy of L. Rey.)

including canines, birds, and crocodiles (Figure 16.33A). Many theropod skulls show evidence of face biting as well, and in the bones of the skull of a juvenile tyrannosaurid, tooth marks are preserved in the nasal and premaxillary bones (Figure 16.33B). By analyzing the bite marks themselves, they could determine if the teeth that made them were serrated, and by matching the serration patterns, they hypothesized that the “biter” was likely a member of the same species as the “bitee”. The researchers proposed that this was a sign of intraspecific competition, an idea that was “fleshed out” by paleoartist Luis Rey (Figure 16.33C). Because many animals today battle each other for territory or mates, it probably isn’t stretching things to hypothesize similar behavior occurred in dinosaurs. Intraspecific conflict was not limited to theropods; we can also observe evidence of within-herd competition in ceratopsians, where the frill of one dinosaur has holes in it consistent with the tip of the nose or eye horns of another individual. As discussed in Chapter 8, intraspecific competition has also been proposed for pachycephalosaurs, and based upon what we see in living animals, intraspecific competition was most likely commonplace in dinosaurs.

16.3  Injuries and Sicknesses: Paleopathologies

Figure 16.34  (A) One of the most spectacular dinosaur specimens ever recovered shows dinosaur behavior. These dinosaurs are preserved, upright, in three dimensions. This Velociraptor was intent on a Protoceratops for dinner, but the Protoceratops had other plans. (B) Although the raptor had its arms wrapped around the neck of the Protoceratops, the little ceratopsian managed to get its mouth around one arm. This death battle probably would not have favored the Protoceratops,

even if it hadn’t been interrupted by a sudden dump of sand that covered both animals. (A courtesy of Y. Tamai, https://commons.wikimedia.org/wiki/File:Fighting_ dinosaurs_(2).jpg; B courtesy of cobalt, https://commons.wikimedia.org/wiki/File:Velo​ cirap​tor_a​nd_Pr​otoce​ratop​s_-_F​ighti​ng_di​nosau​rs.jp​g.)

However, we have many more examples of interspecific than intraspecific combat. Probably the most spectacular evidence for this comes from the famous “fighting dinosaurs” of Mongolia. A small protoceratopsian dinosaur is engaged in a battle to the death with a hungry velociraptor, and it is all preserved as it happened, in three dimensions (Figure 16.34). Fossils like this are exceedingly rare, but when they do occur, they are a snapshot, preserving forever interactions between species. Except for exceedingly rare fossils like this, we must infer intraspecific interactions from bony evidence. One excellent example of this is an Allosaurus vertebra with an odd split in one of its transverse processes. This split was consistent in size with known stegosaur tail spikes, and a cast of a tail spike fits perfectly within this opening in the vertebral processes (Figure 16.35). From this fossil, we can infer that these two dinosaurs most probably came in contact with each other—and it probably wasn’t a friendly encounter. It also shows that this small-brained,

Figure 16.35  Allosaurus vertebrae (shown from two angles) with one transverse process showing an odd open split. This is not a normal feature of

these vertebrae, and it was proposed that perhaps it was a healed wound from an unfortunate battle with a stegosaur. When a cast of a tail spike from this plant-eater was inserted into this opening, the fit was perfect, supporting the idea that these two species interacted. (Courtesy of D. Czajka, photographed at the Utah State University Eastern Prehistoric Museum.)

401

402

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

Figure 16.36  A tail vertebra from an Edmontosaurus was found with a T. rex tooth embedded in it. This is

evidence that these two species interacted in interspecific combat—a battle that the Edmontosaurus survived, as this vertebra shows signs of healing. (Courtesy of D. Burnham and R. DePalma.)

slow-moving plant-eater could hold its own against a hungry predator— at least in this case! It is also not uncommon to find the tips of theropod teeth embedded in ceratopsian frills or the pelves of hadrosaurs, so we can conclude that theropods such as Tyrannosaurus rex occasionally dined on these groups. In one instance, we even see the tip of a T. rex tooth firmly embedded in a healing Edmontosaurus tail vertebra (Figure 16.36). Broken tendons and damaged neural spines support the predator–prey relationship of these dinosaurs. However, unless there are signs of healing, as in the T. rex–Edmontosaurus example, many of these specimens do not tell us if the animal was alive when the munching began, and therefore can’t shed light on whether the interaction was predation or scavenging. Sometimes, pathologies can lead to even more complex behavioral hypotheses. Healed fractures in several adjacent ribs of various types of dinosaurs, and the presence of broken and healing T. rex furculae, has led some to propose that perhaps T. rex could hunt by using its head as a battering ram, hitting its prey with enough force to break the ribs and knock it over. Once down, large animals would become easy prey. A biomechanical study even suggested that if a T. rex could hit a Triceratops in just the right place, it could effectively render this tank-like dinosaur immobile. The broken ribs we sometimes see in Triceratops, and the broken clavicles in T. rex, might be explained by such a scenario.

16.3.2 Disease Whereas injuries are typically caused by physical trauma such as cuts, impacts, and falls, diseases don’t need physical trauma to manifest— although they can certainly occur as a later consequence of an injury. Diseases are abnormalities in the regular biological functions that arise most directly from something other than an injury. They impair biological functions in ways that produce specific, observable effects, but only sometimes are these translated into bone. Diseases can come from a variety of sources, including from infection by microbes such as fungi or bacteria (e.g., ringworm and tuberculosis), through the effects of one’s environment (e.g., radiation), or from the influences of genetics (e.g., sickle cell anemia or cystic fibrosis). Although diseases are not directly caused by injury, they can very often be associated with them. For example, while a cut doesn’t cause an in-

16.3  Injuries and Sicknesses: Paleopathologies

fection itself, if it is deep enough, it allows bacteria into direct contact with bone tissues that would normally be protected by many layers of skin. This can result in a painful infection that prolongs the time it takes the original cut to heal, or it can progress into something far worse than the original injury. We can also recognize some diseases in dinosaurs that aren’t injury-related at all. Evidence for such a disease was identified in a specimen of Tyrannosaurus rex in 2009. A lower jaw from a T. rex was found that was riddled with small holes (Figure 16.37). Many possibilities were raised as to what these holes might indicate. Were they bites from another T. rex during intraspecific competition? Bites from a smaller theropod that somehow was able to attack this giant? Were they a bacterial invasion of the bone? The smooth edges of these lesions ruled out bite marks or random breaks. Closer examination of other theropods shows the presence of these holes in many specimens, all with similar morphology and distribution. The smooth-edged holes are surrounded by patches of thickened bone, suggesting that the bone was responding to invasion by producing new periosteal bone. It turns out that a condition that plagues modern birds may explain these mysterious holes (Figure 16.37B). Living birds can be infected with a parasitic organism called Trichomonas gallinae. Infection by this eukaryotic parasite is a relatively common problem across many different types of birds, and can be passed from adult carriers to their young, or transmitted from infected birds to raptor species that prey on them. This disease causes lesions in a bird’s oral cavity that create holes in the bones of the face. The morphology of these holes and the phylogenetic bracket suggest the possibility that Trichomonas infection may have had roots deep in the dinosaurian tree! What evidence could we use, do you think, to conclusively identify the presence of this organism? Other diseases have also been described in dinosaurs. Different cancers that affect the bones have been diagnosed in dinosaurs, including osteosarcomas, osteoblastomas, and metastatic cancer. Indeed, some of the diseases that plague humans have been around a long time! The identification of certain diseases in dinosaurs may shed light on human and animal pathologies we face today. Perhaps by studying diseases, infections, and healing strategies in dinosaurs, particularly at the

403

Figure 16.37  (A) Lateral (top) and medial (bottom) views of the lower jaw of a T. rex that has been punctured by many small holes (white arrows) that sometimes penetrate completely through the bone. These are inconsistent with bite marks; the raised edges of these holes suggest an immune response that aids in isolating and then fighting off a parasite. Similar holes are found in living birds, including this osprey (B). An X-ray view of the lower jaw of

this osprey (B, bottom) shows that these pathologies penetrate all the way through the bone. These holes can be traced to infection by the Trichomonas parasite in birds. Crocodiles can also suffer from infection by this bone-destroying parasite. (Courtesy of Wolff et al.)

404

CHAPTER 16    How Do We Interpret Dinosaur Behavior?

molecular level, we can someday learn more about the effects and possible treatments in humans.

16.4 WHAT WE DON’T KNOW 16.4.1 Did Dinosaurs Hunt in Packs? The movie Jurassic Park portrays raptors as clever pack hunters, but there is no solid evidence in the fossil record that they, or other carnivorous theropods, exhibited this behavior. Trackways and fossil sites imply that some carnivorous theropods were probably at least social and didn’t kill each other on sight. Some trackways have preserved a record of deinonychosaurs moving in the same direction at the same time (see Li et al., 2008 reference below), but this doesn’t prove they were engaged in hunting behavior at the time. And other workers have made the argument that based on fossil evidence, raptors like Deinonychus were likely more combative than cooperative (see Roach and Brinkman 2007). Additionally, dead prey tends to attract nearby predators, so death assemblages with multiple predators doesn’t provide evidence that they hunted together. Questions to consider: • What would we need to find in the fossil record to provide convincing evidence that dinosaurs hunted in packs? • If convincing evidence of pack hunting is found in one species, how broadly could we apply this behavior to other species? • Did dinosaurs feed like Komodo dragons, where the largest, most senior eat first, and smaller individuals are often maimed or killed competing for food?

16.4.2 Are Dinosaur Pathogens Related to Pathogens That Are Active Today? We don’t know what specific pathogens cause bone and tooth damage that we see in dinosaur fossils, and maybe we can study modern diseases more thoroughly to see if there are specific bone and tooth indicators of disease that affect other parts of an organism. Most studied disease agents today that are well characterized are unique to mammals, specifically humans, so how can what we know of modern pathogens be extended to dinosaurs? If we can link pathogens in dinosaurs at the molecular level to pathogens that invade bird and reptile groups today, we may be able to address questions of when a particular pathogen invaded a lineage. This is important because the longer a pathogen and a host co-evolve, generally speaking, the less lethal the pathogen becomes. Questions to consider: • Because of the unique physiology of dinosaurs and the very different environmental conditions of the Mesozoic Period, were pathogens distinct from those of today? • Did dinosaurs have varied responses to the same pathogen, or were some groups more susceptible to certain diseases than others? • Can we identify in the fossil record, at the molecular level, any dinosaur pathogens that cause disease?

16.4  What We Don’t Know

405

CHAPTER ACKNOWLEDGMENTS We thank Dr. Martin Lockley, Brent Breithaupt, Dr. Ann Ross, and especially Glen Kuban for their generous reviews, suggested improvements, and supplied images for this chapter. Dr. Lockley is a Professor Emeritus at the University of Colorado at Denver. Dr. Breithaupt is the Regional Paleontologist for the Bureau of Land Management in Cheyanne Wyoming. Dr. Ross is a board-certified Forensic Anthropologist and Professor in the Department of Biological Sciences and North Carolina State University.

INSTITUTIONAL RESOURCES Falkingham, P. L., Marty, D., and Richter, A. (2016). Dinosaur Tracks: The Next Steps. Indiana University Press, Bloomington, Indiana. Farlow, J. O. (2018). Noah's Ravens: Interpreting the Makers of Tridactyl Dinosaur Footprints. Indiana University Press, Bloomington, Indiana. Texas parks and wildlife: Dinosaur valley tracks: 112 million years in the making. https://youtu.be/FlvEOXXCqrI The Natural History Museum of London: Dinosaur footprints: How do they form and what can they tell us? https​: //ww ​w.nhm​.ac.u​k /dis​cover​/dino​saur-​footp​rints​ .html​.

LITERATURE Hanna, R. R. (2002). Multiple injury and infection in a sub-adult theropod dinosaur Allosaurus fragilis with comparisons to allosaur pathology in the Cleveland-Lloyd Dinosaur Quarry collection. Journal of Vertebrate Paleontology, 22(1), 76–90.

Milner, A. R., Harris, J. D., Lockley, M. G., Kirkland, J. I., and Matthews, N. A. (2009). Bird-like anatomy, posture, and behavior revealed by an Early Jurassic theropod dinosaur resting trace. PLoS One, 4(3), e4591.

Krauss, D. A., and Robinson, J. M. (2013). The biomechanics of a plausible hunting strategy for Tyrannosaurus rex. In Tyrannosaurid Paleobiology, 251–262. Indiana University Press, Bloomington, Indiana.

Peterson, J. E., Henderson, M. D., Scherer, R. P., and Vittore  C. P. (2009). Face biting on a juvenile tyrannosaurid and behavioral implications. Palaios, 24(11), 780–784.

Li, R., Lockley, M. G., Makovicky, P. J., Matsukawa, M., Norell, M. A., Harris, J. D., and Liu, M. (2008). Behavioral and faunal implications of Early Cretaceous deinonychosaur trackways from China. Naturwissenschaften, 95(3), 185–191. Maxwell, W. D., and Ostrom, J. H. (1995). Taphonomy and paleobiological implications of Tenontosaurus-Deinonychus associations. Journal of Vertebrate Paleontology, 15(4), 707–712. McCrea, R. T., Tanke, D. H., Buckley, L. G., Lockley, M. G., Farlow, J. O., Xing, L., Matthews, N. A., Helm, C. W., Pemberton, S. G., and Breithaupt, B. H. (2015). Vertebrate ichnopathology: Pathologies inferred from dinosaur tracks and trackways from the Mesozoic. Ichnos, 22(3–4), 235–260.

Roach, B. T., and Brinkman, D. L. (2007). A reevaluation of cooperative pack hunting and gregariousness in Deinonychus antirrhopus and other nonavian theropod dinosaurs. Bulletin of the Peabody Museum of Natural History, 48(1), 103–138. Wolff, E. D., Salisbury, S. W., Horner, J. R., and Varricchio, D. J. (2009). Common avian infection plagued the tyrant dinosaurs. PLoS One, 4(9), e7288. Xing, L., Lockley, M. G., Zhang, J., Milner, A. R., Klein, H., Li, D., Persons, W. S., & Ebi, J. (2013). A new Early Cretaceous dinosaur track assemblage and the first definite non-avian theropod swim trackway from China. Chinese Science Bulletin, 58(19), 2370–2378.

17 17

HOW DO WE KNOW ABOUT DINOSAUR REPRODUCTION? MATING AND PARENTAL CARE AMONG DINOSAURS

R

eproduction and parental care both fall under that mysterious category of biology called “behavior”. As we discussed in the previous chapter, behaviors such as these are rather difficult to interpret using only skeletons (and in some cases, eggs and clutches) of animals over 65 million years old that no human has ever observed alive. Yet, we know for certain that dinosaurs reproduced—otherwise, they would not have dominated the landscape for ~135 million years! But did they lay eggs or give live birth? Did they abandon their young like turtles, or care for them to varying degrees, like birds? Like other aspects of interpreting behavior from extinct animals that now reside only in the fossil record, determining reproductive modes is rather complicated. It is helpful at this point to review the “extant phylogenetic bracket” (EPB, Chapter 4), because we rely on this to generate hypotheses about reproductive behavior in dinosaurs. In fact, there was probably a lot of variation in reproductive strategies between early dinosaurs and their later descendants (150 million years is a lot of evolutionary time), as well as among different phylogenetic groups of dinosaurs—just like there was likely variation in their physiology (i.e., metabolic strategies, Chapter 18). Moreover, physiology and reproduction are closely linked; as we shall see, an increase in metabolic rate from the ancestral ectothermic state causes necessary and radical shifts in reproduction.

17.1 MALE OR FEMALE: BIOLOGICAL SEX DETERMINATION

IN THIS CHAPTER . . . 17.1 MALE OR FEMALE: BIOLOGICAL SEX DETERMINATION 17.2 EGGS

After reading this section you should be able to…

17.3 NESTS AND LAYING STRATEGIES

• Describe two secondary sex characteristics that leave bony correlates and could be useful in determining the biological sex of dinosaurs.

17.4 PARENTAL CARE 17.5 WHAT WE DON’T KNOW

408

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

• Discuss limitations in using fossil evidence to determine biological sex in dinosaurs. • Differentiate between primary and secondary sex characteristics.

• Define medullary bone, and explain how it provides evidence of sex determination. When attempting to reconstruct mating behaviors and reproductive strategies, it is important to have a way to distinguish male and female individuals of a species—particularly because in all vertebrates, it is the female of the species that produces the eggs. Biological sex also has implications for understanding population dynamics, herd (or flock) structures, and parental care. For example, the male to female ratio within the human population is roughly 1:1, but in herd animals like elk, the ratio is about 1:5; these differences are significant in explaining the biology and social dynamics that have evolved in these different species. Given this disparity among living groups, how can we, from a temporal distance of at least 65 million years, determine the sex of a dinosaur? In most living animals, males and females are distinct. The males differ from females, at some level, in appearance, and so we say these populations are dimorphic (two shapes). However, sex determination relies for the most part on soft tissue structures that are highly unlikely to be preserved in the rock record. In fact, for many groups, including the nearest extant relatives of dinosaurs—crocodiles and birds—the genitalia are internal, which makes it difficult to determine biological sex even when they are alive with their soft tissues intact (Figure 17.1). How can we differentiate extinct male and female dinosaurs when this isn’t apparent in their extant relatives? It seems like an impossible task. But it turns out that in many living groups (including mammals) there are some bony correlates that are associated with biological sex. Additionally, similar bony features that can be observed in fossils of related species are likely to have the same meaning as in their extant counterparts. For example, almost all mammals (including humans) give live birth, and this results in measurable differences in the pelvises (or pelves) between adult females and males. In these cases, sex can be determined by the angle of the joints of the pelvis (Figure 17.2). However, dinosaurs, crocodiles, and birds, did not give live birth, so we must look to other bony correlates for egg-laying animals. Just what would it take to identify sex in a dinosaur population? First, we would need a large enough population sample to be sure that the trends we see are significant, and are truly dimorphic—not just instances of individual variation. Second, we would need to be certain we have enough Figure 17.1  Crocodile genitalia are internal, making sex determination of even living species difficult—and potentially dangerous! (A) is a female crocodile and (B) is a male crocodile.

(Courtesy of J. Lang.)

17.1  Male or Female: Biological Sex Determination

409

Figure 17.2  Humans display sexual dimorphism in pelvic structure, which is associated with the requirements of passing the baby’s large head during birth. Male pelves (left) have a much

narrower joint, and the angle of the “v” below the pubic symphysis (arrow) is much less than 90 degrees. In females, this joint space is greater than 90 degrees. (Courtesy of K. Tiffany.)

animals in that population that are likely of reproducing age. And third, there would need to exist some significant variation within the population that presumably occurs with maturity. Many living groups, including birds, reptiles, and mammals, exhibit sexual dimorphism. In Chapter 3, we described two kinds of sex characteristics: primary, which are present at birth (e.g., genitalia), and secondary, which don’t show up until they are needed—that is, they don’t develop until the animal reaches sexual maturity, and therefore are not present or obvious in juveniles. For example, not too many seven-year-olds can grow a beard! Although primary sex characteristics tend to be generally soft tissue–based, there are some secondary sex characteristics that leave bony correlates. These include size disparity and ornamentation.

17.1.1 Size Disparity Living animals across many groups show differences in size or robustness that are linked to biological sex. For example, male moose are significantly larger than females, and the same is true in alligators and crocodiles. However, in other reptiles, as well as some mammals, the females are significantly larger. Female blue whales are larger than the males, and in sea turtles (which can grow very large), females are also usually larger. But many factors influence this size disparity. In species where male-on-male combat occurs in competition for mates, larger size may be favored in those males. In contrast, when males have to travel further to find mates, as in some sea turtles, males are smaller to increase their mobility—and hence, their ability to locate females. Alternatively, larger females may be favored because increased size makes them able to produce more young, and care for them better. The problem with applying this idea to dinosaurs is that we don’t have enough of any particular species to tell if size differences are truly due to sex differences or if they might be linked to phases of growth or individual variation. Additionally, since there aren’t any hard and fast rules that apply across living species, there was probably equal diversity of driving forces that determined the ultimate size in dinosaurs, meaning that every lineage could potentially be different.

17.1.2 Ornamentation In many birds today, sex can be discerned because of wide variation, not only in size, but also in color, plumage patterns, and feathery ornamentations on their heads. Much of this ornamentation is not usually apparent in their skeletons, but occasionally it is, as in the case of the hornbill (Figure 17.3). Dinosaurs were different, in that many dinosaurs displayed intricate ornamentation as part of their skeletal structure, such as frills, domes, spikes, and crests. And, if they were like today’s birds, these structures may have been covered in keratin, and thus may

410

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

Figure 17.3  Although many ways that sexual dimorphism expresses in birds is not apparent in their skeletons (i.e., feather plumage or coloration), sometimes it is. There are significant differences in the skulls of the female (A) and male (B) black-casqued hornbills. (Courtesy of Polyoutis, https​://

co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=76​55295​9.)

have been brightly colored and linked to display (see Chapter 14). However, if these features were indeed secondary sex characteristics, they would not appear in young individuals—or perhaps they would be present, but miniaturized. How the crests of hadrosaurs or frills of ceratopsians correlate to bird feathery crests or other ornamentation used in sexual display is unclear. As difficult as it may be to determine sex from the skeletons of dinosaurs, that doesn’t stop us from trying! There have been several ideas put forth that may allow us to “sex” a dinosaur, with varying degrees of evidence to support them. These have included differences in skeletal “robustness”, skull features, and bones of the tail, and the presence of specialized bony tissues. For some dinosaurs like T. rex, it has been proposed that certain features of their skulls may be linked to dimorphic traits. Indeed, there does seem to be two “morphs” within Tyrannosaurus rex specimens (Figure 17.4). One form is more robust, with a deeper jaw and bony ridges over their eyes. The other form has a more gracile skull, and it is narrower. However, to identify such characteristics in dimorphism, it should be present in roughly half the skeletons (assuming a 1:1 sex ratio in the population) and should be either absent or diminished in juveniles. Remember, though, only a few T. rex skeletons are complete, and most are represented by 50% of the skeleton—or less. To find a complete T. rex skull is incredibly rare. Looking to juveniles of the species may shed light on some of this, but are there any juvenile T. rex specimens with which we can compare adult forms? Well, that depends upon who you ask.

Figure 17.4  It has been proposed that there are two different “morphs” observed in Tyrannosaurus rex skulls: a gracile form (A, C) in which the skull and jaws are elongate, and the bony ridges over the eyes are less pronounced, and a more robust form (B, D) in which the lower jaws are shorter, but deeper, the skull is thicker with pronounced bony ridges over the eyes. However, if these features are

indicative of sexual dimorphism (and not individual variation or taphonomic artifact), which would be the female form, and which the male? (A adapted from S.R. Anselmo, https://en.wikipedia.org/wiki/File:Sue_TRex_ Replica_Skull.JPG; B adapted from P. Bakke, https://flic.kr/p/8s1QhP; C adapted from J.M. Luijt, https://commons.wikimedia.org/wiki/ File:T-Rex.jpg; D adapted from EncycloPetey, https://commons.wikimedia.org/wiki/ File:UCMP_Trex_skull_left.JPG.)

17.1  Male or Female: Biological Sex Determination

411

The bones and skull of a tyrannosaurid dinosaur housed at the Cleveland Museum of Natural history were first identified in the 1940s. They were re-described in the late 1980s by Robert Bakker, who noted that the bones of the skull showed fusion, and so proposed it was an adult member of a new tyrannosaurid species. However, even though it was much smaller, it had many traits in common with Tyrannosaurus rex. Thus, he named it Nanotyrannus (“Dwarf Tyrant”) and proposed a new sister group, closely related to, but separate from the great “Tyrant Lizard King”. However, since this description, other scientists continue to study the specimen, and have added histology to the list of features used to characterize it. As discussed in Chapter 18, histology can be used to determine not only how fast dinosaurs grew, but also whether or not they were still actively growing. Microscopic inspection revealed that this Nanotyrannus was still growing rapidly, and thus not yet a fully mature adult. As a result, many now think that Nanotyrannus is actually a juvenile T. rex., although not all agree. The skull of another, and much more complete specimen, was found in 2001 and is housed at the Burpee Museum in Illinois. This specimen (nicknamed “Jane”) has a narrow and gracile skull, as well as other features not seen in larger specimens of T. rex, such as differences in number and position of teeth (Figure 17.5). But again, many of the T. rex specimens found to date are incomplete, and only a few have skull material. So, are these two smaller specimens of different species, or juvenile forms of T. rex? Yet another factor confounding the issue of sex determination is that most dinosaurs, like crocodiles and many other reptiles, continue to grow after reaching sexual maturity (although the rate of growth slows significantly). So, is it possible that some of the features we assign to sexual dimorphism might really be a sign of skeletal maturity and aging? In other words, could crests, domes, or horns simply get bigger as they get older, rather than being limited to either males or females? Many dinosaurs exhibit different types of head ornamentation. Indeed, between dinosaur groups like saurolophines and lambeosaurines, centrosaurines and chasmosaurines, there is very little difference in their Figure 17.5  (A) The small, slender skull of “Jane”, a specimen that is proposed to be a juvenile T. rex. (B) The larger and more robust skull of “Sue”, the most complete specimen of T. rex discovered to date. How many

of the features seen here could be explained by the idea that “Jane” is a subadult—a Tyrannosaurus rex still growing? (A courtesy of Zissoudisctrucker, https​://up​load.​wikim​ edia.​org/w​ikipe​dia/c​ommon​s/4/4​a/Tyr​ annos​aurus​_Rex_​Jane.​jpg; B courtesy of K. Tiffany, photographed at the Field Museum.)

412

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

Figure 17.6  (A) Full skeletal mount of an adult Hypacrosaurus. (B) Full skeletal mount of Parasaurolophus. These

dinosaurs have been assigned to different genera, largely because of the features of the skull—they show very little variation postcranially. (A courtesy of Etemenanki3, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​id=64​85167​5; B courtesy of K. Tiffany, photographed at the Field Museum.)

post-cranial skeletons. These groups are instead differentiated primarily by distinctive features in their skulls (Figure 17.6). Among living animals today, we have species that have antlers and horns, but few or none that modify their skulls to the extent that some dinosaurs did. Are these modifications associated with sex? Or are they selected for some other reason? How can we know? If the highly ornamented skulls exist to identify animals of the same species where ranges of closely related species overlap, these features will not help to differentiate the sexes. The biological definition of a species, remember, has two parts: (1) those organisms that can mate with each other to (2) produce viable, fertile offspring, to the exclusion of other groups. Therefore, if an organism invests energy in an attempt to reproduce, it would be good for them to know they had their eyes set on a member of the right species! Otherwise, it might result in wasted energy and no viable offspring. To that end, animals of very closely related, but distinct species that live in the same area or occupy the same ecological niche will sometimes possess exaggerated features to distinguish them from each other. These can include differences in coloration (Figure 17.7), scent, or vocalization patterns—none of which would preserve in the fossil record. Some closely related birds, for example, produce different calls when there is an overlap in their range compared with when there isn’t such an overlap. There is a further issue with identifying biological sex in dinosaurs, in that even if we could say for certain that there were two “morphs” of dinosaurs within a single species, how would we tell which was female

Figure 17.7  The bay breasted warbler (A) and the black-throated green warbler (B) are two very closely related bird species that inhabit overlapping ranges. They use color to discern mate appropriateness. (A courtesy

of Dan Pancamo, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​id=15​13140​0; B courtesy of John Harrison, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​id=60​ 38051​.)

17.1  Male or Female: Biological Sex Determination

413

Figure 17.8  Female (left) and male (right) common pheasants differ in size, plumage, and color. How many

of these features are likely to survive fossilization? (Courtesy of ChrisO, https​:// co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=23​67271​.)

and which was male without soft tissues or behavioral clues? Look at the birds in Figure 17.8. They are clearly very different. But which is which? So, what other skeletal features might contribute to information on biological sex? One possibility is the presence (or absence) on the skeleton of a small bone that attaches to the ventral (downward) surface of the very first caudal vertebra after the pelvis. It has been proposed that this little v-shaped bone, called a chevron, might be the key to differentiating males and females. In female crocodiles, it was argued, the first chevron (the one closest to the body) is angled up and backward, pointing away from the pelvis toward the tail (Figure 17.9); conversely, in males it is angled downward, like all the others. This backward-facing angle to the chevron would give more room for an egg to pass, and seems to be specific to females. Figure 17.9  The small v-shaped chevron attaching to the first caudal vertebra may be an indicator of sex in crocodiles and dinosaurs. If female (A), the chevron would be angled backward to make more room for egg passage. If male (B), it would be oriented straight down, as are all the rest of the caudal chevrons. (A

courtesy of the Australian Museum, https​:// au​stral​ianmu​seum.​net.a​u/lea​rn/an​imals​/rept​ iles/​estua​rine-​croco​dile/​#gall​ery-285-4; B adapted from P. Williams, https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=29​ 17737​7.)

414

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

However, as is the case with almost all skeletal traits in fossils, it is not so black-and-white. Additional studies found little evidence that chevrons are significantly different between males and females in living crocodilians, so these may not be definite indicators of sex. Even if they did indicate sex in crocodiles, most birds do not have chevrons, or if present, they are greatly reduced. Furthermore, chevrons in birds do not have a direct link to function, whereas in crocodiles, they serve to protect arteries, veins, and nerves, and some have linked the function of these small bones to greater load-bearing in the tail—which of course living birds don’t have. Additionally, we must take taphonomy into account. If we were to find such a retroverted chevron in a dinosaur, was it because it was positioned like that in the living animal, or because taphonomic forces deformed it? Because the chevrons are small and not well fused to the body of the vertebra, it is easy for them to become lost, distorted, or removed from the original biological position. Thus, this bony trait is not specific enough, or unambiguous enough, to tell male from female. There are, however, two traits that may allow the unambiguous determination of a female dinosaur, at least in theropod dinosaurs closely related to birds: medullary bone and eggs inside the body cavity. These traits arise out of some basic biology principles. We know from the phylogenetic bracket that all dinosaurs laid eggs, because both birds and crocodiles lay eggs. We also know that (most) dinosaurs had eggs with well-mineralized shells, rather than the leathery shells of some other reptiles, because both birds and crocodiles produce mineralized eggshells to one degree or another. Furthermore, from discoveries in the rock record, we know that many dinosaur groups laid large clutches (15–30 or more eggs). Finally, we know that, as in all modern animals, reproduction comes with a cost. The calcium needed to make eggshells is derived directly from their bones, so when eggs are being produced, the dense cortical bone of the reproducing female fills with resorption pits (Figure 17.10, also called erosion rooms), or small holes where the mineral has been released from the bone into the blood, where it is carried to the shell gland for deposition on the egg. All of these things are true for birds and crocodiles, but birds have two features not found in crocodiles. First, birds have hollow bones. Thus, although crocodiles show resorption pits in their bones, they have a lot more bone to draw from than birds, so diet can compensate more readily for the minerals needed to produce the eggshells. Additionally, crocodile babies grow slower within the egg, thereby requiring less mineral at lay. Conversely, birds grow very fast, and have a higher metabolic rate, both requiring more mineral than is needed by crocodiles and other reptiles. Laying birds must compensate somehow when calcium is drawn from their very thin bones to make the eggshells, or their bones would shatter with physical activity—in fact, this is a serious problem for birds grown commercially and bred to reproduce continuously. Additionally, birds are endothermic. Because of their high metabolic rates, they contract their heart and breathing muscles much faster, and when muscles contract, they use calcium. Birds also grow faster, and deposit bone more rapidly, again requiring more calcium. Because bird metabolic rates are many times higher than any living crocodiles can attain, they require many times more calcium in a given time than crocodiles or other ectotherms. They need more minerals for body processes, including blood clotting and muscle contraction, in addition to producing eggs for fast-growing babies. Birds can lay bone down faster than any ectotherm, faster than mammals, and even while reproducing. To put this in perspective, it is estimated that when birds are in lay, in a single day, they use more calcium than a human female would if she were pregnant and nursing for two full years. That is a lot of bone resorption, and if it is not offset, birds and their thin bones would be in trouble!

17.1  Male or Female: Biological Sex Determination Figure 17.10  Reproduction increases demand for calcium, particularly in animals with hard-shelled eggs, that can be seen by the presence of large erosion rooms in the microstructure of bone. (A) and (B) are histological sections of bone from an ostrich and alligator (respectively) that were known to be in active shelling of eggs. Thus, erosion cavities (arrows) can

be seen in these animals. Similar structures have been observed in Tyrannosaurus rex (C) and other dinosaurs. (Courtesy of M. Schweitzer, et. al. 2005 and 2007.)

Birds compensate for this tremendous bone loss during reproduction by building a special type of “reproductive” tissue, called medullary bone. Only birds, among all living animals, produce this type of bone, and they begin to produce it with the first signs of ovulation. Just as in mammals, the hormone estrogen triggers ovulation in birds. However, in birds, the spike of estrogen that releases the egg from the ovary also stimulates bone cells to begin laying down medullary bone. When bird estrogen levels rise in response to ovulation, their bodies begin to deposit this bone on the internal surfaces (i.e., medullary cavity) of the long bones, and sometimes other bones throughout the skeleton (Figure 17.11). Bone deposition is extremely rapid and the collagen fibers within the bone are randomly organized as a result, giving it unique characteristics. It is also very vascular; medullary bone must be infused with blood vessels, which are needed to carry the calcium stored in this new medullary bone through the body to the shell gland, where it is used to make eggshells. The presence of this tissue in birds is an unambiguous indicator that a bird is female, and that it is in a “pregnant” reproductive state. Wouldn’t it be cool if we could find this in a dinosaur? There are some things to consider. First, this tissue is only present in birds during lay. In

Figure 17.11  A cross-section through the long bone of a hen in lay shows the dense trabecular network of medullary bone. (Courtesy of M.

Schweitzer.)

415

416

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

most living birds, that is usually about two weeks, but varies depending on the number of eggs laid. If the birds lay twice a year, that is about four weeks total. Think about it: if dinosaurs were similar, an adult female dinosaur would have to die during the short window of time while she’s producing eggs, and die in exactly the right environment to preserve its skeleton; 65 million years later, a dinosaur paleontologist would have to stumble across the bones of this dinosaur. Then, the fragile medullary bone would have to be retained during recovery and preparation of the bone, and then someone would have to recognize it as medullary bone. What are the chances? This very thing happened in 2003! Skeletal elements of a T. rex had been discovered at the end of the field season in 2001. The bones were protruding from the face of a very steep outcrop of sandstone, in the Hell Creek Formation of Montana. New methods were being developed to chemically analyze fossil bone, and some had been previously used on a different T. rex. But because the bones of this new T. rex seemed to be preserved extremely well, it was decided that this “fresh” dinosaur specimen would be analyzed. That decision was made before anyone noticed there was something really weird about these bones. The very first bone examined (Figure 17.12) showed a distinct bone tissue on the inner surfaces of the femur. It was so completely different from the surrounding bone that a microscope wasn’t even needed; it could be seen in the hand sample. Yet it was undeniably bone— vascular bone tissue that had all the hallmarks of very rapid deposition. Comparing this never-before-seen bone tissue with living birds, it was apparent that it had all the microscopic features of medullary bone. For example, it was fibrous, and the fibers were randomly oriented in a pattern referred to as “woven bone”, meaning it was deposited very rapidly. It was also highly vascular, with vessels infusing the entire tissue. It arose from the endosteum, a very thin connective tissue that lines the medullary cavities of the long bones, and contains (in living animals) the cell precursors to osteocytes that produce the bone matrix in all vertebrates. But, as you know by now, morphology is never sufficient to make this logical leap! If coupled to chemical evidence that supported the identification of this tissue as medullary bone, scientists could say for the first time that a female Tyrannosaurus rex in the process of laying eggs had been discovered! To do this, investigators had to rely on what was known of medullary bone in birds, which, it turns out, was not a lot at that time. These new dinosaur tissues had to be compared with medullary bone in modern birds, and even though there are lots of living birds to study, medullary bone had only been characterized in a few groups—and mostly only for species humans utilize for food and agriculture. Among living birds, ostriches and emu belong to a basal branch of the avian tree (Palaeognathae, see Chapter 19) so it was reasoned that maybe their medullary bone was different than more derived birds. Ostrich and emu, two Figure 17.12  (A) Cross-section and (B) internal view of medullary bone observed in fossils of a Tyrannosaurus rex. (Images courtesy of M. Schweitzer et.

al., 2016.)

17.1  Male or Female: Biological Sex Determination

representative paleognaths, were chosen for comparison. These birds were confirmed to be in lay, and their long bones (along with a laying hen) showed medullary bone—but it was structurally distinct and varied widely in each of these groups. Ironically, the data supporting the presence of medullary bone in T. rex was also the first officially photodocumented occurrence of medullary bone in ostrich and emu as well! We already talked about the need for this bone type in birds with thin bones, but why is it present in ostriches, who don’t fly and have far more robust bones? First, one must realize that “thin” is relative. Although the cortical bone of an ostrich is thick (~ 5 mm) compared with flying birds like the hen (~600 um), it is still thin relative to its length, in particular when its weight is taken into account. An adult ostrich can weigh over 300 lbs., bigger than most humans. T. rex cortical bone is even thicker—~ 1.5 cm at mid shaft, although its bones are still hollow. However, the femur of a T. rex must support 7–8 tons of animal, from its slowest to its quickest gait. Compared with the overall mass of the animal, that is relatively thin bone. Remember also that the ancestors of T. rex were small, active, and agile, with hollow and relatively thin bones. Thus, even if T. rex cortical bone might have gotten relatively thicker as it increased in mass over time, it retained the ability to produce medullary bone, just as it retained its ancestor’s hollow bones. Additional testing on this same specimen a few years after its discovery showed that in addition to the histology and distribution, the medullary bone in T. rex retained distinct chemical signatures found in modern medullary bone, but not common to other bone types. Medullary bone in living birds has a different chemical composition than the adjacent cortical bone. Chemical tests showed that the T. rex medullary bone was similar in composition to medullary bone in birds, but different from the chemistry of the cortical bone surrounding it. This provided strong support that it was, in fact, medullary bone in this dinosaur’s limb bones. We can say with confidence, then, that at least one T. rex specimen paleontologists have recovered can confidently be identified as female. With that knowledge, a comprehensive study of the rest of the skeleton may show more traits that we can link to biological sex that would be present even when the animal was not in lay (e.g., the presence of bony ridges over the eyes). With a broad idea of what medullary bone looked like in dinosaurs, scientists have begun to look for this tissue in other specimens. A Mesozoic bird called Confuciusornis sanctus is very common in deposits in China, represented by hundreds of specimens, and is clearly dimorphic (Figure 17.13): one morph has long thin tail feathers, and the other has very short ones. Based on microscopic sections of one of the long bones, it has been proposed that the tissues in the inside of this ancient bird bone were morphologically consistent with medullary bone, and that the short-tailed birds were the female morph. Recently, additional specimens enantiornithines (basal birds nicknamed “opposite birds” that have no living descendants, see Chapter 19), have been studied for the presence of medullary bone. One of these birds had an egg still inside its body—and medullary bone. This reproductive tissue seems widely distributed within birds and their ancestors, and its presence can be used as a marker for the female sex. The other trait that can be unambiguously linked to biological sex is, of course, the presence of an embryo inside the mother—whether in an egg, like non-mammalian vertebrates, or in a uterus, as in mammals. If we can see eggs inside of the body cavity, it seems safe to say that the animal is both female and “pregnant”. As you can imagine, it is at least as rare to find this as it is to recover a dinosaur with delicate medullary

417

418

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

Figure 17.13  (A) Short-tailed and (B) long-tailed specimens of Confuciusornis sanctus from China.

It has been proposed that the short-tailed specimens are female based upon the tentative identification of medullary bone in this specimen; however, the identification of this bone type in one specimen is still controversial. (A courtesy of J. St. John, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=36​90738​3; B courtesy of Tommy https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=24​11530​7.)

bone in place. However, this, too, has happened! Fossil birds from the Mesozoic of China have been found with multiple egg follicles in the body cavity (Figure 17.14). Even more amazing, eggs preserved in three dimensions have been found inside the body cavity of oviraptor specimens (Figure 17.15), and with additional specimens being recovered, it may be that more are preserved in this manner. These finds tell us that reproductive physiology in some of these early birds and dinosaurs was similar to that of living birds. Furthermore, the identification and validation of some of these important characters can give us a better picture of when these traits first arose—and in whom. Regardless of our ability to differentiate male and female dinosaurs, there obviously were both male and female dinosaurs. And just as obviously, they figured out how to recognize and mate with each other. Otherwise, they would not have been so dominant in the Jurassic and Cretaceous. Of course, there are a lot of fanciful interpretations of how that might have occurred (Figure 17.16). Some of these stagger the imagination, because sexual reproduction between two enormous sauropods would not have been a trivial feat—imagine the physics involved in these interactions between two 60-ton animals. However, for that, we will have to be content with the artistic interpretations, as it is one behavior that we are very unlikely to find preserved in the rock record!

Figure 17.14  Jeholornis, a fossil bird from China, was found with ovarian follicles in its body cavity (inset).

This very important fossil shows that by 125 million years ago, these animals have achieved the very avian quality of having only one functioning ovary. (Courtesy of X. Zheng, et al. 2013.)

17.1  Male or Female: Biological Sex Determination

419

Figure 17.15  This pelvis from an Oviraptor was preserved in three dimensions, and contained a pair of eggs within the body cavity. This

specimen was important in shedding light on the evolutionary history of reproductive physiology in maniraptorans. Living birds only retain one ovary and oviduct, and therefore shell and lay eggs one at a time over the course of days to weeks. Conversely, crocodiles shell and lay many eggs, all at once. This fossil shows that the Oviraptor had two functioning oviducts, like crocodiles and other vertebrates, but that it shells and laid them sequentially, over a longer time period, like birds. The fossilized eggs also show a slight asymmetry, with one end of the eggs more pointed than the other, more like birds than reptiles. (Adapted from Sato et al., 2005.)

Figure 17.16  Artistic rendering of what Tyrannosaurus rex copulation might have looked like. There is no

actual data to support (or falsify) this fanciful rendition. However, we do know this occurred, even without direct evidence. (Courtesy of L. Rey.)

420

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

17.2 EGGS After reading this section you should be able to… • Describe the physical constraints on vertebrate amniote eggs. • Compare and contrast crocodilian and bird egg-laying strategies. • List and explain features of eggshells that allow assignment to a taxonomic group.

We may never know for certain which dinosaur morphology defined male or female, and we probably won’t ever know exactly how dinosaurs mated. But one thing we do know is that for 150 million years, dinosaurs figured it out, because they did produce the inevitable end product: baby dinosaurs! And to get baby dinosaurs, you have to hatch some dinosaur eggs.

17.2.1 Physical Constraints of Eggs In Chapter 7, we discussed the role of the amniotic egg in freeing animals from their ancestral ties to water for reproduction. This huge evolutionary leap allowed terrestrial vertebrates to occupy virtually every niche and habitat in almost every ecosystem on the planet. The amniotic membranes protect the egg from desiccation (drying out) and from microbial invasion, as well as providing a way to get rid of waste products and supply the embryo with its metabolic needs. These functions, however, require a fine balance. The shell (and membranes) must be thin enough to allow the passage of oxygen from the environment to the embryo, and of CO2 from the embryo to the outside air. The shell must also be thin enough for the hatchling to peck its way out, but at the same time, it must be thick enough to support the weight of the shell against gravity. As a result, there is an absolute limit to how big an egg can possibly be, and how thick the eggshell can be, regardless of the species producing the egg. You might think that, because the long-necked sauropods were the biggest terrestrial organisms to ever walk the earth, they must also have possessed the largest eggs. Surprisingly, it is not these gigantic dinosaurs, but a very recently extinct bird that holds the record for the largest egg. The eggs of the elephant bird of Madagascar had eggs bigger than a human head (Figure 17.17)! Because the size constraints on eggs are dictated by physics, not phylogeny, they apply equally to dinosaur eggs as to birds and crocodiles—meaning that even a 60-ton sauropod had to begin life small enough to fit inside an egg no bigger than your head.

Figure 17.17  The egg of the elephant bird (right) shown here next to an ostrich egg for scale (left). The elephant

bird holds the record for the largest egg— even including the eggs of the largest non-avian dinosaurs. (Courtesy of K. Tiffany, photographed at the Field Museum.)

17.2  Eggs

17.2.2 Egg Production and Shelling Birds have many reproductive features in common with their crocodilian cousins, which they inherited from their shared archosaurian ancestor. Because both of these groups produce hard-shelled eggs, it is highly likely that their common ancestor did as well. However, the manner by which crocodiles and birds produce eggs is very different. First, crocodiles shell their eggs (i.e., biologically deposit the shell around the embryo) and then lay them en masse. That means that all of their eggs, all 10–80 of them (depending on species), are shelled and laid at the same time, within an hour or so. On the other hand, birds shell and lay their eggs one at a time, usually separated by at least 24 hours. Large birds, like the ostrich, can lay as many as 50 eggs per nest, but wait 3–5 days between each one. Thus, it can be weeks before they are done laying and can focus on incubating the eggs. You might think that if there are 40 or more days separating first and last egg, the embryos would hatch over the same number of days, causing problems for the mom who would have to keep an eye on active babies while sitting on the nest for the unhatched ones. However, even though birds don’t synchronize the laying of their eggs, many do synchronize the hatching, so the eggs all hatch within a relatively short period of time. Birds achieve this by not sitting on the nest to brood until all the eggs are laid. The transfer of heat from mom to developing eggs is a trigger for development. Thus, waiting for the last egg to be laid before starting incubation ensures that the babies will all hatch together. Another difference is in the ovaries of birds. Most vertebrates (including humans) have two functioning ovaries that produce eggs, each of which is connected to an oviduct that carries the eggs to the uterus (in birds, the shell gland functions as the uterus). However, in almost all birds, only one ovary produces eggs and in most, the second ovary is lost during development. This loss might have been selectively favored as an advantage for flight. But when did this happen in their evolutionary history? Well-preserved specimens in the fossil record can tell us. For example, the fossil bird in Figure 17.14 had apparently already lost one functioning duct, and thus had the condition expressed in modern birds, with only a single ovary. On the other hand, Oviraptor apparently retained both oviducts (Figure 17.15), like crocodiles. Furthermore, the evidence we have suggests that the ovaries of most dinosaurs produced, shelled, and laid a pair of eggs together, then waited a period of 24 hours or more, before producing the next pair of eggs, continuing until all eggs were laid. Based upon the orientation of the eggs in the oviraptor and the way they are arranged in the nest as pairs, this group seems to represent a transitional stage, between the single oviduct and sequential lay of modern birds and the dual oviducts and en masse shelling of crocodiles.

17.2.3 The Challenge of Identifying the Egg-Layer Just as studies of dinosaur trackways are hindered by not knowing for sure who made the tracks, eggshells in the fossil record have the same problem. Unless the eggs are inside the body of the dinosaur, or unless they contain embryonic remains that can be definitively assigned to a particular dinosaur, there is no way to tell for certain which dinosaur produced which egg. This has led to some embarrassing cases of mistaken identity in the history of paleontology and is a great example of why science must avoid assumptions. In the early 1920s, Roy Chapman Andrews was sent by the American Museum of Natural History (AMNH) in New York to lead a large expedition to the deserts of Mongolia to look for evidence of early humans and

421

422

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

Figure 17.18  This model of an Oviraptor stealing the eggs of other dinosaurs to eat was before its “reputation rehabilitation”.

Its behavior isn’t the only inaccurate thing about this model—notice that it has teeth, even though Oviraptor was toothless (see Chapter 19)! (Courtesy of HombreDHojalata, https​://co​mmons​.wiki​ media​.org/​w/ind​ex.ph​p?cur​id=19​86063​6.)

the origin of the human lineage. Instead, they found skeletal remains from many small ceratopsian dinosaurs, belonging to Protoceratops. This dinosaur had been described previously, and eggs assigned to this small ceratopsian were well known; in fact, these little dinosaurs provided the first hard evidence that dinosaurs did indeed lay eggs. On this expedition, however, Andrews discovered and collected a partial skeleton (skull, neck, and forelimb) of a theropod lying on top of the eggs that were thought to belong to Protoceratops. The remains were then described by Henry Fairfield Osborn of the AMNH in 1924. Believing this to be evidence that a hungry theropod was caught in the act of stealing the eggs of the small herbivorous Protoceratops, Osborn named the new dinosaur Oviraptor philoceratops (ovi= egg; raptor = thief; philo = lover) or “egg-stealing lover of ceratopsians”. This species of dinosaur gained infamy as an evil, gluttonous monster, preying unmercifully on the poor defenseless babies of this harmless plant-eater (Figure 17.18). For decades, this picture of the oviraptor dominated the minds of the public and scientists alike. Additionally, this egg-stealing lifestyle had been inferred for many other theropods. Then in 1994, 70 years after its initial description, scientists from the AMNH announced the discovery of supposed “Protoceratops” eggs— with the embryos of Oviraptor inside! The presence of these embryonic bones, with distinct skulls and toothless jaws, sealed the identification of these eggs as belonging to Oviraptor, not Protoceratops. Later, this same group of scientists from the United States and Mongolia found one of the most spectacular dinosaur fossils ever recovered. It was a type of oviraptor, Citipati, very clearly brooding its eggs, its arms stretched out just as in modern birds, to protect the 20 or more eggs underneath (Figure 17.19). This find revolutionized not only how we thought about the “evil” oviraptors, but about all dinosaurs in general. It showed that the behavior of oviraptors had been misrepresented; they were not heartless egg stealers, but protective mothers. In addition, this specimen sheds light on the physiology of oviraptors. It was a very strong indicator of endothermy in this dinosaur lineage (Chapter 18). Animals do not engage in true brooding if they don’t have heat to contribute to the developing eggs. Since that initial find, other dinosaurs have been found in similar positions, associated with nests and eggs. It is not just oviraptors that brooded their eggs; similar evidence has been found for troodontids and dromaeosaurs as well. Thus, this may have been an ancestral trait of all Pennaraptora (see Chapter 19).

17.2  Eggs

423

Figure 17.19  This spectacular specimen is solid evidence that this dinosaur brooded its eggs, just like modern birds. Rather than being an

“egg thief”, this shows the oviraptor Citipati caring for its young. (Adapted from Dinoguy2, https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=10​90758​.)

17.2.4 Eggshell Structure and Classification Examples of eggs being found inside a dinosaur, or underneath a brooding one are very rare, as you may imagine. In those cases, the egg-layer is fairly clear. But how can we identify the species or group the eggs belong to when they’re not associated with a parent? The most definitive way to identify the taxonomic origin of an egg is if it has a dinosaur embryo inside, which itself can be phylogenetically defined. Indeed, as mentioned above, embryonic bones, including skulls, have been found inside some dinosaur eggs. The Oviraptor eggs could be positively assigned to that species, based upon features already present in the embryos. We also have eggs containing embryos of the maniraptorans Troodon and Therizinosaur, as well as several different types of hadrosaurs and giant titanosaurids (Figure 17.20). But what about the cases in which we don’t have an embryo or a parent dinosaur, only eggshell? Just like we can’t say for certain that a theropod footprint was definitively made by Tyrannosaurus rex (unless one died directly at the end of the trackway), we can’t conclusively assign isolated eggshells to a particular species. Therefore, like trackways are classified by ichnotaxonomy into ichnotaxa, eggs also have their own classification system. Ootaxonomy is the science of eggshell classification, in which we assign specimens of eggshell to an ootaxon. Ootaxa are given different (but related) scientific names from the species they are associated with. Features used in ootaxonomy to classify eggshells include: • Overall morphology: One basic feature of eggs is their overall size and shape. Eggs and eggshell show a lot of variation in the modern world. For example, ostrich eggs are very large with thick shells, while some hummingbird eggs are the size of the tip of a human thumb (Figure 17.21)! Dinosaurs eggs also varied in size and shape (Figure 17.22). Many theropod eggs were elongated ovals, while hadrosaur and sauropod eggs were more spherical. Figure 17.20  (A) Embryo of Citipati in its egg. (B) Protoceratops hatchling. Specimens of dinosaur embryos

and hatchlings shed light on dinosaur reproduction and growth. (A adapted from Dinoguy2, https://commons.wikimedia.org/ wiki/File:Citipati_embryo_IGM100_971. jpg; B courtesy of Dinoguy2, https:// commons.wikimedia.org/wiki/File:Amnh_ protoceratops_hatchling1.JPG.)

424

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

Figure 17.21  These eggs show the relative sizes of (left to right) hummingbird eggs, chicken eggs, and ostrich eggs. Additionally, compare

the ostrich egg here with the one in Figure 17.17 to get an idea of how big these eggs are to an elephant bird egg (the largest eggs known). (Courtesy of C. B. Beach.)

Figure 17.22  These images show various morphologies that are known for dinosaur eggs. In Panel D, you

can see the profound difference in size a shape between a theropod egg (left) and a titanosaur egg (right). (A–C courtesy of G. Todd, https​://co​mmons​.wiki​media​.org/​w/ind​ ex.ph​p?cur​id=88​14976​2; https​://co​mmons​ .wiki​media​.org/​w/ind​ex.ph​p?cur​id=88​ 14979​1; https​://co​mmons​.wiki​media​.org/​w/ ind​ex.ph​p?cur​id=88​14989​0; D courtesy of K. Tiffany.)

• Surface ornamentation: Bird eggs have microscopic textures on their surfaces, even though they appear mostly smooth. Next time you have a chicken egg, take a magnifying glass to see if you can see a pattern. These patterns are easier to see in some eggs than others, and many dinosaur eggs have macroscopic textures that stand out better than those seen in living birds. These textures were also far more varied in dinosaur eggs than in birds today, and these variations in surface patterns can be diagnostic to particular groups. For example, in some cases, ridges run vaguely parallel. In other cases, raised bumps dot the surface (Figure 17.23). These textural features seem to be related, in some cases, to the pores that penetrate the shell and supply oxygen to the developing embryo. • Pore structure: Among the many functions of eggshells, the two most relevant here are to support and protect the developing embryo, and to supply oxygen and allow diffusion of toxic CO2). These requirements constrain the shell structure. The size, shape, and orientation of the pores that allow the passage of gases can be an indication of who laid the egg, at a broad level. Sometimes these pores are too small to see with the naked eye (check out your chicken eggshell for example), but other times, they are visible. Because of their function in gas exchange, pores must extend all the way across the thickness of the shell. To evaluate the size and

17.2  Eggs

425

Figure 17.23  These eggshells, seen under the microscope, show the variation in surface texture for different dinosaur egg types. On the

smooth textured shell (top) the pores are relatively easy to see. The bottom images show two different surface textures, one with shallow ridges on the left, and more of a knobby texture on the right. Features like this are used to assign eggshells to particular groups of dinosaurs. (Courtesy of the University of California, Berkeley, Museum of Paleontology, https​://uc​mp.be​ rkele​y.edu​/imag​es/eg​gshel​l/2_t​extur​es_60​ 0.jpg​.)

shape of pores we have to cut a section of the shell thin enough to see the structure under a microscope. The results show many variations; pores can be straight, branching, or can form an interconnected network) (Figure 17.24). These features allow us to assign eggshell to general categories. • Mineral structure: Biomineralized tissues are organic tissues produced by an organism, where the biological components (usualFigure 17.24  Categories of eggshell microstructure. This table shows how

we recognize and categorize fossil (and modern) archosaur eggshell, based upon the organization of the shell unit, pore structure and distribution, surface texturing, size, shape, and other features. The two closest living groups to dinosaurs (crocodiles and birds) show very different organization, and all dinosaurs, whether saurischian or ornithischian, are morphotypically more similar to birds. Within Aves, ratites differ from more derived living birds. Interestingly, there is very little structural difference between the shells of living ratites and maniraptoran dinosaurs. (Table modified from Mikhailov et al., 1996.)

426

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

ly proteins) have a profound effect on the orientation, size, and shape of the mineral crystals. We have already talked about this a little bit in talking about bone histology, but the same holds true for biomineralized eggshell. Like bone, the mineral in eggshell is constrained in shape and size by its association with the protein component of the shell matrix. Using the orientation of crystal shape as well as the mineral incorporated (e.g., calcite, aragonite) can tell us about both taphonomic alteration and the group of creatures, broadly, to which the eggshell belonged. Eggshell types are distinct at a broad level. For example, we can always tell turtle eggshells because of their microstructure and the way the crystals of aragonite mineral that make up the shell are arranged. Some lizard eggshells are also distinct, and are made of calcite instead of aragonite. Knowing the microscopic features of eggshells in living groups, then, we can apply these to extinct egg-layers as well. What we find is that the more closely dinosaurs are related to birds, the more their eggshell microstructure resembles that of birds. Advanced ornithopods, which are not on the avian lineage, have pores that are either straight or angled. Conversely, theropods close to the bird lineage like Oviraptor have a sharp boundary between the internal mammillary layer and the overlying layers; this is the same structure seen in basal living birds, like ratites (ostrich and emu). More advanced living birds have these same features, but also show an organic complex rich in lipids on the surface of the eggs that serves to prevent drying out and protect from microbial invasion. This layer is called the cuticle. Cuticles have occasionally been observed in some theropod eggs as well. In addition to helping identify species or taxonomic group of origin, the microstructure of eggs and their pore distribution can be used to suggest certain environmental parameters that were faced by the egg-layers. We can use these features to measure conductance, or rate of water and gas loss from the internal egg to the environment through the shell. If too much water leaves the shell, the developing embryo dries out; if not enough, the embryo can drown, particularly in very humid environments. It may seem obvious, but embryos need oxygen! Furthermore, the higher the metabolic rate of the developing embryo, the more oxygen is required. Thus, birds (and dinosaurs) that bury their eggs have more and larger pores because oxygen has to pass through soils to get to the embryo. Virtually all non-avian dinosaurs laid their eggs on the ground (it would have been very hard for a T. rex or a sauropod to build a nest in a tree!). Further, most dinosaurs either buried their eggs in soils or with vegetation, and this is reflected in the relatively large pores preserved in their shells. Conversely, the eggshells of Oviraptor and Troodon, species that have been found in brooding positions and which clearly did not bury their eggs, have pores that are smaller and less dense across the surface of the shell.

17.3 NESTS AND LAYING STRATEGIES After reading this section you should be able to… • Differentiate between a nest and a clutch. • Describe evidence for nest-building in dinosaurs.

Producing the egg is one thing, but what happens when it is time to lay it? We know that dinosaurs laid eggs because we have lots of clutches that we can assign to dinosaurs, but just how did they accomplish it?

17.3  Nests and Laying Strategies

When we consider the living archosaurs—crocodiles and birds—there are broad differences in the strategy of these two groups. Did dinosaurs intentionally build complex nests like many birds, or did they lay their eggs in simple scrapes in the ground? Alternatively, dinosaurs could have buried their eggs with vegetation like some crocodiles, or left their nests open to the environment. Most living birds lay their eggs in a nest of some kind, as do most crocodiles, alligators, and many other reptiles. But what exactly is a nest? It may be rather easy to define for living animals, but how many of the characters we use to identify a modern nest can be translated to fossils? A nest can be a structure made of twigs or grass in tree branches, daubs of mud that are placed by birds under overhangs or bridges, or something as simple as a shallow pit in the ground. For the purposes of this discussion, a nest is any structure built intentionally to hold eggs and provide protection for offspring. A clutch, on the other hand, is a group of eggs produced by a female at roughly the same time. A clutch of eggs can occupy a nest, but does not necessarily do so. Nest-building has been around for a long time, and both crocodiles and most birds build them. Therefore, it appears that nest-building is an ancestral trait within Archosauria, and is therefore likely non-avian dinosaurs built them. If dinosaurs built nests for their eggs, how would we recognize these in the fossil record? Would we expect them to preserve? And what kind of nests did they build? What criteria can we use to define a dinosaur nest? We can safely say that most dinosaurs built nests on the ground, and furthermore, many buried their eggs (see below), once laid. Oviraptor (Figure 17.19) pretty obviously had a structure built into the sediment for its eggs, so that it could brood them. But in the late 1990s, more light was shed on the question of dinosaur nest-building in other species. A vast nesting ground was discovered in the badlands of Argentina, and determined to be the product of titanosaurid dinosaurs. Clutches of eggs were scattered over about ten square miles of territory. And what is more, these clutches were found on four different stratigraphic layers! This distribution was used to propose that these giant titanosaurids exhibited site fidelity—that is, that they returned to the same place to lay their eggs over and over. But were these clutches associated with nest structures? And how could a researcher recognize a nest structure after it has been subjected to taphonomy? What criteria can we use? Based upon the wealth of evidence at the titanosaur nesting grounds, a series of criteria have been proposed by Luis Chiappe and colleagues, to recognize nests in the fossil record. Criteria for recognizing nest in the fossil record: • Crosscuts pre-existing sediments: The nest should exhibit a depression that cuts across pre-existing sediment layers. • Eggs: The depression should show the presence of eggs, eggshell, and/or an accumulation of baby bones. • Elevated ridge: The structure may possess an elevated ridge, above the sediment layers, that lacks the layered structure of the surrounding sediment—indicating that sediment had been disturbed by the dinosaur. • Infilled: To be preserved and recognized, the depression will be secondarily infilled with a sediment that is different in some measurable way (e.g., color, grain size) from the sediment it is built within.

427

428

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

Figure 17.25  A–E shows the sequence of events proposed to result in the preservation of nest structures at Auca Mahuevo, a titanosaurid nesting ground discovered in Argentina. Some of the nests discovered there show features of nests that indicate intentional nest-building. (A) Undisturbed sandstone. These cross-bedded sandstones were laid down in sequences, with time passing between them as indicated by the angular unconformity (see Chapter 2). (B) Bioturbation of these sediments by nesting sauropods, altering the sediment layers. The sediment bedding patterns are truncated, and there is a rim of “massive”, structureless sediment that is elevated above the underlying layers. In addition to this depression and rim, the presence of eggs/ eggshell contributes to recognizing structures as a nest. (C) Secondary infilling of the nest by sediments that differ from the surrounding or original sediments. This has been interpreted as a flooding event that inundated the nesting ground after the eggs were laid. (D) Entire sandstone unit being covered by muddy sediments of different structure and chemistry than the original sediments, usually reflected by a color change. (E) Exposure from differential weathering of sandstone and mudstone and exposing the eggs within. (F) One of these nests in the field. Note the elevated rim surrounding egg clutches (R) and the difference in color between the inside and outside of this rim. (Courtesy of L.

Chiappe, et. al., 2004.)

These features are illustrated in Figure 17.25. Some of these features may be unique to these nests, but others might characterize most ground-based nests. These titanosaur nests, the Oviraptor nest, and a few others (e.g., brooding troodontids, the “good mother” Maiasaura nests first described in the late 1970s) support the idea that dinosaurs built nests intentionally to protect their eggs; and if the dinosaurs were altricial, to protect their young until they gained independence. But for the vast majority of dinosaurs for which we have fossils, eggs and nests have not been characterized. Did they not make nests, or did they just not survive in the fossil record? Because we have recognizable nests from sauropods, theropods, and ornithischians, as well as evidence from the extant phylogenetic bracket, it seems safe to say that nest-building behaviors were common to dinosaurs—although as in birds, this trait may have been lost in some lineages. As discussed above, based on eggshell porosity, we can also suggest that most dinosaurs buried their eggs in the ground. From this, we can hypothesize that they dug holes of varying sizes and complexities, laid their eggs, and then buried them with either sediment or vegetation. However, a buried nest like this is highly subject to taphonomic processes, and would be difficult to preserve or recognize, except, of course, for the presence of an egg clutch within it.

17.4 PARENTAL CARE After reading this section you should be able to… • State what is meant by parental care and discuss the costs and benefits of caring for young. • Differentiate between precocial and altricial development. • Describe evidence of precocial or altricial development in dinosaurs. • Define neoteny and explain how it can be used to make inferences about parental care.

Dinosaurs could discern male and female, recognize their own species, produce eggs, and make nests to put them in. But the evidence discussed thus far doesn’t address whether dinosaurs cared for their young once they hatched. The answer to this question, like most of this

17.4  Parental Care

chapter, begins in phylogeny and the dinosaur family tree; parenting behavior probably varied greatly within this group, just as it does among birds today. First, though, let’s define what we mean by parental care. Parental care means any behavior of parents toward their offspring that increases the chance of their survival—at a cost to the parent. Think again of the adult Oviraptor found brooding its nest. In the end, its efforts to care for its eggs contributed to its inability to escape whatever ultimately killed it and its young, preserving this “unselfish” act forever in the fossil record. By definition, then, it is apparent that parental care is “expensive” in terms of resources and energy (just ask your parents!). It may come at a cost to the parents’ own survival rates; the parents must expend great amounts of energy foraging for food that is then passed to the offspring and is not available to sustain the parent. Additionally, noisy and helpless young attract predators, jeopardizing the safety and survival of a parent that remains in the vicinity. Beyond survival, it also reduces the parent’s ability to invest in additional offspring and mating opportunities. So why would this strange strategy be selectively advantageous, enough to propagate throughout the animal kingdom? What are the advantages of this behavior? The most obvious result of parental care, regardless of the cost to the parent, is that it increases the survival rates of the young. With intense parental care, young offspring can grow larger before they gain independence, giving them an advantage over competitors (see below discussion on altricial and precocial strategies). Furthermore, the more time spent in proximity to parents means that advantageous behavioral patterns (e.g., hunting in cats, song patterns in birds) can also be passed on. All of these provide a competitive advantage to animals that possess them, providing strong selective pressures to maintain this expensive strategy in a lineage. Both groups of extant archosaurs, crocodiles and birds, exhibit some parental care. Although crocodiles don’t brood their eggs, they guard their nests carefully, and stay close by while the eggs are incubating. Sometimes, they will even rest their big head on the eggs to protect them. After hatching, the mother carries the babies in her mouth to the nearest water source and maintains a close physical presence, continuing to provide some degree of protection for weeks or months after hatching. Then the babies are on their own. On the other hand, most birds brood their eggs, using their bodies to provide heat and protection, and some provide food for the babies as they grow. So if parental care (at some level) is found in both crocodiles and birds, phylogenetic bracketing allows us to infer that it was present in the common ancestor of these two groups, and thus most likely in dinosaurs as well, as the Oviraptor demonstrates.

17.4.1 Developmental Strategies Just as there are different physiological strategies among different groups of vertebrates (Chapter 18), different species of birds produce young that hatch at different stages of development. These differing developmental strategies are adaptive for different lifestyles. For most birds, it is advantageous to have young that are very independent early on, while for others, very helpless young that require more parental input is the norm. There are two main types of developmental strategies observed in living birds: • Precocial young: Precocial babies are mostly independent when they are born or hatched—they are capable of securing their own food, require little (if any) parental care, and leave the nest early

429

430

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

Figure 17.26  A newly hatched quail chick (A) is much more independent and capable of running and foraging soon after hatching than the altricial robin hatchling (B), which remains helpless and utterly dependent on its parent. (A courtesy of T. Wills, https​://

co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=32​68979​; B courtesy of K. Tiffany.)

(Figure 17.26A). This strategy provides an advantage to the parents, because rather than having to put in the energy to care, feed, and protect the young, they can forage and put energy into reproducing again. Producing precocial offspring is a very ancestral trait, and is not limited to birds or reptiles; the young of most vertebrate taxa are precocial. Fish, for example, don’t spend a lot of time caring for their young. • Altricial young: Altricial babies are hatched or born completely helpless—often blind and “naked” (Figure 17.26B). They can’t see, and they can’t hold their head up or exhibit much muscle control. They are completely reliant on their parents to meet all of their needs for survival. In most cases, they can’t even regulate their body temperature! But with the intense parental input required by altricial young comes advantages of more prolonged growth, as well as behavioral flexibility and learning from parental behavior. These two developmental strategies—precocial and altricial—represent two ends of a continuous spectrum, and different species can fall anywhere on it. Some babies might be able to run the minute they are born, but still need their parent to provide food for months or years after their birth, whereas others rely on their parents primarily for protection until they grow large enough to protect themselves. At what point in the spectrum would you put humans? What developmental strategy did dinosaur babies employ? Did they have altricial babies that required intense parental care, or precocial young that ran off to fend for themselves soon after hatching? What evidence is present in the fossil record? We already talked about Oviraptor as evidence that this dinosaur, at least, brooded its eggs, but this doesn’t tell us how mature the baby dinosaurs were at hatching. Although phylogeny is extremely helpful in inferring aspects of dinosaur biology, it does have its limits. Birds show parenting and hatching strategies across a wide spectrum, and crocodiles bury or cover their eggs, but still employ parental care. But these models don’t fit across all dinosaurs. Some dinosaurs had to do things very differently from birds, because when the parent weighs several tons, it is pretty safe to say it probably didn’t sit on its nest. So, when there is no direct evidence in the fossil record for such behavior, how robustly can we investigate if, and to what degree, parental care was delivered? In 1979, paleontologists reported the first evidence of dinosaur eggs outside of those found in Mongolia by Roy Chapman Andrews. More than 50 years after his monumental discovery, crews led by Jack Horner of the Museum of the Rockies in Montana discovered an area filled with concentrations of eggshell and some embryonic bone. They proposed that the hadrosaurid whose remains dominated the site be named Maiasaura

17.4  Parental Care

peeblesorum (Maia = good mother; saura = lizard) was just that—a good mother who cared for her young. However, recent evidence is mounting that, like birds, parental care in most dinosaurs probably involved both parents. We don’t often think of males brooding, but in most birds, males share at least some brooding duties, and in some bird species, it is the males that brood exclusively. Histological evidence for many dinosaurs, including Oviraptor, Troodon, and others, support the idea that it may be the males that are sitting on top of the eggs! The evidence put forth for parental care in Maiasaura includes: • Trampling in the nest: The structures identified as nests contained eggshell, but the shell was broken into tiny bits, suggesting that the shells were broken and trampled by the babies after they hatched. This type of trampling would be expected if the baby dinosaurs remained in the nests for a period of time after they hatched, but not if they immediately left it. If they did stay in the nest for an extended period, they would be dependent on the parents to bring them food. However, the broken eggshells could also have resulted from taphonomic processes during fossilization, so by itself, this would not be sufficient evidence for parental care. • Age of young in the nest: In some of the clutches, the baby bones were bigger than newly hatched, and much bigger than those of embryonic remains still in the egg. These data indicate that the baby dinosaurs remained in the nest for some time. If so, it suggests that they were being brought food instead of leaving the nest to forage. • Fragility of babies’ skeletons: Microscopic examination of the ends of the babies’ bones showed that they were not fully mineralized but remained cartilaginous. Cartilage is not as rigid or stable as bone, so it was argued that the presence of these issues might indicate that the babies were not capable of keeping sustained pressure on their leg bones, as would be required for long-distance movement. This pattern of bone growth is also found among altricial birds. • Wear patterns of the babies’ teeth: The teeth in the tiny jaws of the baby dinosaurs already showed signs of wear, meaning that they had begun to process food. Combined with the evidence that the bone tissue in their legs was not yet fully developed, this suggested that the babies were likely not walking long distances to get food, but rather being brought food by their parents while they remained in the nest. This was supported by the presence of fossilized plant matter that was also observed within the nests (although rotting plants might also have been used to produce heat for the developing embryos). Together, these data seem to make a pretty strong case for parental care, and indicate that this one dinosaur at least, had somewhat altricial young. However, even within hadrosaurs, not all species seem to have employed this level of parental care. Hypacrosaurus, a hadrosaurid dinosaur closely related to Maiasaura, had eggs nearly five times larger and young with more robust bones. These young had fully ossified bone ends, as opposed to the cartilage of Maia hatchlings. This supports the idea that its babies were much larger and more developed when they hatched, and were probably more independent and precocial, showing that there is no “hard and fast” rule for dinosaur reproduction, but that developmental strategies can vary within dinosaurs, even within a closely related group.

431

432

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

Maiasaura may have had altricial young, but it is difficult to get a broader picture of developmental strategies across Dinosauria as a whole, as the extant phylogenetic bracket (EPB) approach doesn’t address this clearly. On one end, crocodile babies are fairly precocial—they are well developed and relatively independent by the time they hatch. The most basal of living birds (e.g., ostrich, emu, chickens) as well as some more derived forms, have precocial babies also. Other groups even further removed from dinosaurs, like turtles, snakes, and lizards, mostly have precocial young as well. This distribution points to precociality as an ancestral trait. Therefore, it is reasonable to hypothesize that most non-avian dinosaurs had precocial young, even if they did show evidence of providing some parental care. Remember, the scale from precocial to altricial is a sliding one. Embryos of allosauroids, oviraptorids, troodontids, and sauropodomorphs, support the idea that precociality is basal for dinosaurs.

17.4.2 Evidence for Parental Care What evidence can we use to investigate behavior like parental care in the fossil record? Perhaps patterns of development may hold a clue. In species that care for their young, babies tend to share a suite of features we characterize as being “cute”. In some animals, infant features differ in proportion, sometimes greatly, when compared with the adult form. In kittens, for example, their eyes are proportionally larger, their face is shortened, and their snouts are smaller (Figure 17.27) than in the adult. Their jaws are also smaller, and they don’t protrude toward the front of the face as do adult cat jaws. All of these features combine to make them “cute” in their mama’s (and most human) eyes, encouraging an infusion of care and protection. Puppies are similar. Young dogs, even wild forms like wolves, have relatively big eyes, shorter noses, and jaws that are small relative to the size of the head. Their floppy ears contribute to the idea of their semi-helpless “cuteness”. Humans are an excellent example of the profound morphological changes an individual can undergo from birth to maturity. Figure 17.28 shows a diagram of the overall proportional changes a human experiences. For a newborn, the head is about a quarter the size of the whole body, while in the adult form, the head is about half of that, approximately one-eighth of the total body length. Infant humans also have very large eyes and cheeks relative to the rest of their face, and their jaws recede, rather than taking on the more defined jaws in adults. As you are probably aware, humans stay relatively helpless and dependent on care from their parents longer than virtually any other species. In extant animals, we observe a correlation between these features (head proportionately large relative to body, large eyes, shortened face and jaws)

Figure 17.27  (A) A kitten compared with (B) an adult cat. Notice the

differences in the proportions of their eyes, snout, and ears as they age. (B courtesy of K. Tiffany.)

17.4  Parental Care

433

Figure 17.28  Schematic representation of proportional changes during human development. (A) Human at birth (0 years old); (B) 2 years old; (C) 6 years old; (D) 15 years old; (E) 25 years old. Notice that the

head goes from being a quarter of the body length to one-eighth of the body length. What bones in the human skeleton do you think grow slowest, and which grow faster? (Courtesy of Choulant, Wellcome Collection gallery, https://commons.wikimedia.org/ wiki/File:Male​_figu​res_s​howin​g_pro​porto​ ns_in​_five​_ages​._Wel​lcome​_M000​0429.​ jpg.)​

and parental care: the longer these features persist in an animal’s development (ontogeny), the younger, and perhaps more helpless, it looks. The longer it looks like a juvenile, the longer parental care is extended. This makes sense in the context of altricial young; the longer they appear young and helpless, and the slower they grow out of it, the longer their parents care for and protect them. So, how can we use this knowledge of living organisms to hypothesize strategies used by dinosaurs? When we look at the EPB for dinosaurs, we see an interesting pattern. Birds that care for their young have young that express these “cute” features, regardless of where the babies are on the spectrum of precocial to altricial. For example, baby chickens are mostly precocial, but they still receive some parental care, and the chicks show some of the “cute” juvenile features, when compared with adult birds (Figure 17.29). At the other end of the EPB are crocodiles. These animals also provide parental care, as discussed above, and their young are also “cute”… for crocodiles. They have a shortened face, big eyes, and shorter jaws (Figure 17.30). However, crocodiles are rare among reptiles. Snakes, lizards, and turtles generally provide no parental care at all, and their young also look like miniature replicas of themselves. There’s (arguably) nothing cuddly about them! These “cute” features are seen in the other end member of the extant phylogenetic bracket of dinosaurs. In Figure 17.31, a juvenile Canada goose is compared with the adult form. Pay close attention to the proportional size of eyes, snout, and jaws, relative to the rest of the head, in each. Which one is “cuter”? How does this knowledge inform on studies of dinosaurs? With the discovery of dinosaur embryos and hatchlings, we are able to compare the Figure 17.29  (A) An adult chicken compared with (B) a chick. What

juvenile (i.e., “cute”) characteristics can you identify in the chick? (A courtesy of Z. Cebeci, https​://co​mmons​.wiki​media​.org/​w/ ind​ex.ph​p?cur​id=39​92667​3; B courtesy of K. Tiffany.)

434

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

Figure 17.30  (A) Adult American alligator, compared with a hatchling (B). The hatchling shows proportionate

differences in snout, jaw, and eyes, relative to the adult. The baby is much “cuter”. These features may correlate to parental care. (A courtesy of K. Tiffany, photographed at the North Carolina Zoo; B courtesy of the National Park Service.)

Figure 17.31  (A) The juvenile Canada goose shows a shorter snout, bigger eyes, and rounder head than the adult goose (B). (A courtesy of B. Matsubara,

https​://co​mmons​.wiki​media​.org/​w/ind​ ex.ph​p?cur​id=63​92424​8; B courtesy of R. Lawton, https​://co​mmons​.wiki​media​.org/​w/ ind​ex.ph​p?cur​id=89​1652.)

Figure 17.32  (A) A juvenile ceratopsian shows a similar pattern of development as is seen in the goose and crocodile. Notice the shortened snout, small jaws, bigger eyes, and relatively rounder face relative to the adult skull (B). (Images not to scale).

(A courtesy of T. Evanson, photographed at the Museum of the Rockies, https​://co​ mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=27​37660​9; B courtesy of M. Schweitzer, photographed at the Museum of the Rockies, with permission.)

features of some dinosaurs with their known adult forms, and observe that most dinosaurs for which we have embryos also exhibit these “cute” features. Compare the juvenile ceratopsian with the adult skull shown in Figure 17.32. Notice the relatively big eyes, shortened snout, and flattened forehead in the juvenile form, similar in pattern to what is seen for both crocodiles and birds. As much as there can be skeletal correlates to parental care, juvenile features retained later in development may correlate to more parental care. And, for a few rare cases, the evidence seems to support parental care for significantly long periods after hatching. Intentional nest-building, babies that stay in the nest after hatching, and neotenous features are consistent with at least some degree of parental care. However, Maiasaurus may have taken this to the extreme (for dinosaurs) in terms of altriciality; most dinosaurs we have data for, including basal sauropodomorphs, sauropods, lambeosaurids, allosaurids, oviraptors, troodontids, and many enantiornithine birds, probably had young that were more on the precocial side of the scale—though probably all had some level of parental care.

17.4.3 A Final Note on Physiology and Reproduction One more thing to consider when discussing reproduction in dinosaurs is the effect of emerging endothermy on reproductive strategies.

17.5  What We Don’t Know

Remember, the ancestral state—the one most widely distributed across all vertebrates, is ectothermy (Chapter 18). Endothermy is derived, and among all living terrestrial vertebrates, it is restricted to birds and mammals. If dinosaurs possessed an elevated metabolic rate, above the rate of living ectotherms (as much evidence suggests), this physiological strategy would have a profound effect on their reproduction, in addition to all their other systems. When we think about this characteristic in terms of the phylogenetic bracket around Dinosauria, we see that although members of Crocodylia exhibit temperature-dependent sex selection (TDS), meaning that their sex is determined by temperature of incubation, in birds, genetics plays a role in sex determination—although it’s a bit more complicated than what we observe in mammals. First, all living birds have genes for sex determination, however, not all birds have sex chromosomes. In basal birds, like ostrich and emu, these sex genes are not clustered on a single chromosome, but spread throughout the genome. More derived birds do have sex chromosomes; however, we observe a different pattern from that of mammals. A genetically male mammal has one X and one Y chromosome, versus XX in a female, but a genetically male bird has two of the same chromosomes (ZZ), versus ZW in a female. In birds, this genetic system can be influenced by temperature in different ways. In some birds, incubating at too high or too low a temperature leads to embryo death—but female embryos may be more susceptible than males at one end of the spectrum, whereas males succumb more at the other, creating uneven distribution in the next generation.

17.5 WHAT WE DON’T KNOW 17.5.1 How Did Larger Dinosaurs (e.g. Sauropods, Theropods, etc.) Copulate? Not only would large size present a challenge to the act of copulation, but many dinosaurs also had large tails, spines, spikes, and armor, all of which might get in the way during the act. We also don’t know what their reproductive organs looked like, as they were soft tissue and we have yet to find any preserved impressions in the fossil record. Crocodiles and modern birds both have a cloaca, a single orifice that serves both waste and reproductive purposes, so we can be pretty sure that dinosaurs did as well. Additionally, male crocodiles have a penis inside the cloaca, and some male bird species have a phallus, but for most species of birds, both the males and females just have cloaca. Questions to consider: • How likely are we to find evidence of copulation in the fossil record? • What type of reproductive structures did male dinosaurs have, and did it vary among different groups?

17.5.2 How Did Sauropods Lay Their Eggs on the Ground? Biomechanically, it doesn’t seem that large sauropods dinosaurs could crouch close enough to the ground to lay their eggs, and if they couldn’t, the eggs would surely break when hitting the ground from hip height of a sauropod. Long, fleshy, extensible, tube-like ovipositors have been proposed in the movies, but are highly unlikely, because they are not observed in crocodiles or modern birds (visualize a slide for eggs!). If sauropods did possess such a feature (see the Walking with Dinosaurs link in Institutional Resources for a fanciful portrayal of such a feature

435

436

CHAPTER 17    How Do We Know about Dinosaur Reproduction?

in Diplodocus), it would have been soft tissue without likely bony correlates, so we cannot know definitively if they had such structures. Questions to consider: • What other possible strategies could sauropods have used to lay their eggs on the ground other than crouching or an ovipositor tube? • What fossil evidence could we find that would help answer this question?

17.5.3 There Are Many Things We Don’t Know about Dinosaur Eggs and Egg-Laying! Even though we have recovered many fossil dinosaur eggs and nest sites, there is still a lot we don’t know about dinosaur eggs beyond how sauropods laid eggs on the ground. Some recent chemical evidence suggests that some dinosaurs may have employed pigment in their shells, like many modern birds, which is a derived trait and aides in camouflage or preventing parasitism by other species (see Weimann et al., 2017 and 2018 references). But when did this trait arise in dinosaurs? Also, uncertainties in dinosaur metabolic strategies (see Chapter 18) lead to a lot of questions about egg-laying as well. In living birds, the temperature at which the eggs are brooded has significant effects, including influencing the rate of development of the young. This leads to the question of when was brooding incorporated into the dinosaur lineage, and how did advanced metabolic strategies affect this timing? Questions to consider: • How long did it take from when the egg was laid to when a hatchling emerged? What kind of data would be needed to inform on this? • How many times per year could dinosaurs lay eggs? Just once, or once a season? Did long-lived dinosaurs like sauropods lay fewer times per year than shorter-lived theropods? • Did all dinosaurs employ egg pigmentation or only the more derived maniraptorans? Do you think pigment is more important for eggs laid on the ground or in trees? • What causes variation in eggshell structure among larger phylogenetic groups? • Were dinosaur eggs subject to predation by insection and/or bacteria like some bird eggs today?

CHAPTER ACKNOWLEDGMENTS We thank Dr. David Varricchio for his generous review and suggested improvements to this chapter. Dr. Varricchio is a Professor of Paleobiology, Taphonomy, and Ichnology in the Department of Earth Science at Montana State University.

INSTITUTIONAL RESOURCES Dinosaur eggs, by the American Museum of Natural History. https​: //ww ​w.amn​ h.org ​/dino​saurs ​/dino​saur- ​eggs.​ Fossil eggshell by the University of California Museum of Paleontology: https​: //uc​ mp.be​rkele​y.edu​/scie​nce/e​ggshe​ll/eg​gshel​l3.ph​p. The making of Walking with Dinosaurs in HQ Part 6 | BBC: https://youtu.be/nDKY4xSdtyk.

17.5  What We Don’t Know

437

LITERATURE Brusatte, S. L., Carr, T. D., Williamson, T. E., Holtz Jr, T. R., Hone, D. W., and Williams, S. A. (2016). Dentary groove morphology does not distinguish ‘Nanotyrannus’ as a valid taxon of tyrannosauroid dinosaur. Comment on: “Distribution of the dentary groove of theropod dinosaurs: Implications for theropod phylogeny and the validity of the genus Nanotyrannus Bakker et al., 1988”. Cretaceous Research, 65, 232–237. Chiappe, L. M., Schmitt, J. G., Jackson, F. D., Garrido, A., Dingus, L., and Grellet-Tinner, G. (2004). Nest structure for sauropods: Sedimentary criteria for recognition of dinosaur nesting traces. Palaios, 19(1), 89–95. Larson, P. (2013). The case for Nanotyrannus. In Tyrannosaurid Paleobiology, 15–53. Indiana University Press, Bloomington, Indiana. Mikhailov, K. E., Bray, E. S., and Hirsch, K. F. (1996). Parataxonomy of fossil egg remains (Veterovata): Principles and applications. Journal of Vertebrate Paleontology, 16(4), 763–769. Sato, T., Cheng, Y. N., Wu, X. C., Zelenitsky, D. K., and Hsiao, Y. F. (2005). A pair of shelled eggs inside a female dinosaur. Science, 308(5720), 375–375. Schmerge, J. D., and Rothschild, B. M. (2016). Distribution of the dentary groove of theropod dinosaurs: Implications for theropod phylogeny and the validity of the genus Nanotyrannus Bakker et al., 1988. Cretaceous Research, 61, 26–33.

Schweitzer, M. H., Wittmeyer, J. L., and Horner, J. R. (2005). Gender-specific reproductive tissue in ratites and Tyrannosaurus rex. Science, 308(5727), 1456–1460. Schweitzer, M. H., Elsey, R. M., Dacke, C. G., Horner, J. R., and Lamm, E. T. (2007). Do egg-laying crocodilian (Alligator mississippiensis) archosaurs form medullary bone? Bone, 40(4), 1152– 1158. Schweitzer, M. H., Zheng, W., Zanno, L., Werning, S., and Sugiyama, T. (2016). Chemistry supports the identification of gender-specific reproductive tissue in Tyrannosaurus rex. Scientific Reports, 6, 23099. Wiemann, J., Yang, T. R., Sander, P. N., Schneider, M., Engeser, M., Kath-Schorr, S., Müller, C. E. and Sander, P. M. (2017). Dinosaur origin of egg color: Oviraptors laid blue-green eggs. PeerJ, 5, e3706. Wiemann, J., Yang, T. R., and Norell, M. A. (2018). Dinosaur egg colour had a single evolutionary origin. Nature, 563(7732), 555–558. Yun, C. G. (2015). Evidence Points out that “Nanotyrannus” is a Juvenile Tyrannosaurus Rex (No. e1052). PeerJ PrePrints. Zheng, X., O’Connor, J., Huchzermeyer, F., Wang, X., Wang, Y., Wang, M., and Zhou, Z. (2013). Preservation of ovarian follicles reveals early evolution of avian reproductive behaviour. Nature, 495(7442), 507–511.

18 HOW DO WE KNOW IF DINOSAURS WERE WARMBLOODED, COLDBLOODED, OR SOMETHING IN BETWEEN?

18

DINOSAUR PHYSIOLOGY AND METABOLISM

I

t has been a long (and fascinating!) scientific road from the first recorded discovery of a dinosaur bone in the 17th century to our current models of how dinosaurs functioned and grew. Along that road, dinosaur scientists have invented or borrowed a variety of techniques that have allowed us to shed light on many aspects of dinosaur biology, such as how quickly a baby dinosaur reached maturity, how fast a dinosaur could run, or how much force a dinosaur could muster with each bite. This chapter will visit many landmarks of dinosaur physiology, metabolism, and growth. As always, we begin this discussion with clear definitions.

18.1 FUEL IN THE TANK: WHAT IS METABOLISM? After reading this section you should be able to… • Define and differentiate: ectothermy, endothermy, homeothermy, and heterothermy. • Describe the thermoregulatory strategies used by common birds, mammals, and cold-blooded “reptiles”.

IN THIS CHAPTER . . . 18.1 FUEL IN THE TANK: WHAT IS METABOLISM? 18.2 COSTS AND BENEFITS: ECTOTHERMY VS. ENDOTHERMY 18.3 HOW CAN WE KNOW WHAT KIND OF METABOLIC STRATEGIES DINOSAURS USED? 18.4 SO, WHAT KIND OF METABOLISM DID DINOSAURS HAVE? 18.5 WHAT WE DON’T KNOW

440

CHAPTER 18    Dinosaur Physiology and Metabolism

Metabolism is the sum of all the chemical reactions an organism undergoes to function. It can be separated into two processes: • Catabolism: The reactions that break down food products. • Anabolism: The reactions that build biomolecules for the body. A peanut butter sandwich cannot circulate through your system, no matter how well you chew it. Therefore, nutrients that are taken in have to be broken down into their component molecules through catabolism. Through this process, the fats, carbohydrates, and proteins we gain by eating a sandwich are broken down through physical (chewing) and chemical (stomach acids) pathways to fatty acid chains, simple sugars, and amino acids. (To remember that catabolism is the destructive part of metabolism, just think of what cats do to furniture!) Once broken down into these simple forms, the body can then use them (anabolism) to make new proteins and enzymes, fats for cell membranes, and even DNA for dividing cells. (Incidentally, this is why some people take anabolic steroids—to build muscle mass). Visualize this process as a Lego™ project. If you have a Lego™ house, breaking the house apart into the individual blocks used to make it is catabolism; using those separated blocks to build a car is anabolism. Paired together, the destruction of catabolism and the construction of anabolism make up metabolism, and these metabolic processes are required for an organism to function. If an organism cannot take in enough food for these processes to continue, it goes into “starvation mode” catabolism—it begins to break down its own tissues to survive. An organism’s fats and eventually muscle are broken down to provide the amino acids and energy needed to function. Metabolism must occur in all living things, even bacteria. In fact, the ability to metabolize is one of the criteria an organism must have to be considered “alive”, although this occurs at different rates and under different conditions and pathways in different organisms. It is an expensive process, requiring energy intake—and producing heat as a waste product. Of course, the more heat given off, the more waste! This helps to explain where the familiar terms “warm-blooded” and “cold-blooded” come from. Warm-blooded animals operate at higher energy levels. They need to take in far more resources to generate the energy required to survive, but they also give off far more waste heat than cold-blooded animals. However, the terms “warm- and cold-blooded” are misleading. The temperature of an animal’s blood (and body) is always at least equal to the environment. What really divides “warm” and “cold” blooded animals is not their blood temperature, but how, and from where, they obtain the energy to power metabolism. When an animal derives the energy it needs for metabolism from the environment—for example, by basking in the sun to absorb heat—they are ectothermic (ecto = outside, therm=temperature). When an animal can produce this energy from food it takes in instead, we say they are endothermic (endo = within). We usually equate ectothermy with “cold-bloodedness” and endothermy with “warm-bloodedness”, but it is important to remember that the metabolisms we observe in nature span a continuum, rather than a hard division between these states. Ectothermic vertebrates usually have a low body temperature in the early morning, and warm up slowly as environmental temperatures rise. They reach their peak function when the daytime temperatures are at their highest, and their body temperatures begin to fall once again as night approaches and temperatures cool off (Figure 18.1). This relationship with the external environment is why terrestrial animals that are

18.1  Fuel in the Tank: What Is Metabolism?

441

Figure 18.1  Graphing activity levels of (A) ectothermic and (B) endothermic organisms over a 24-hour period.

Warm-blooded animals can maintain a high activity level regardless of the time of day or the temperature, but ectothermic animals are sluggish in the morning and night-time, with peak activity correlating to peak daytime temperatures. (Courtesy of J. D. Harris.)

ectothermic don’t usually live in cold locations or at high elevations. For example, no crocodiles live in the wilds of present-day Alaska. Knowing this cyclical nature of activity in ectotherms comes in handy in the field when we look for fossils because we know to be extra alert on cool mornings. If we surprise a rattlesnake when it is cooler, it may not have the energy to get out of the way, or warn us off with rattles, and so it is more likely to bite without warning. But, more importantly, knowing the biological and behavioral implications of metabolism also helps us understand patterns in the fossil record. If we find the fossil skeleton of a crocodile in Alaska, when none live there now, we can say with confidence that Alaska must have been warmer when the animal lived there. Because they generate heat internally, endotherms can inhabit environments that vary widely in temperature, and thus can live in virtually any environment—as long as they can get enough food. They can also function equally well during the day or at night. There are two groups of living endotherms: mammals and birds. Although they both regulate their body temperatures through metabolic energy, they did not get there from the same evolutionary starting point. Thus, they are endothermic in very different ways. Mammals originally occupied a nocturnal (nighttime) niche, because they were small and didn’t have to directly compete with the dinosaurs with which they shared the planet. Dinosaurs were diurnal (daytime) animals, as are most of their bird descendants. Those few birds that occupy a nocturnal niche, like owls and kiwi, have attained that condition rather late in their evolutionary history, so that is considered a derived state for birds. But, of course, in nature, things are a little less definitive. There are some ectothermic snakes that, for a short time, can significantly elevate their body temperatures above environmental (ambient) temperatures by using their muscles to produce heat by “shivering”. Similarly, there are some mammals, like the naked mole-rat (Heterocephalus glaber), that have lost the ability to generate and/or maintain high body temperatures. Instead, like most reptiles, they use behaviors to regulate body temperatures. In the case of the naked mole-rat, they live underground in large groups to help regulate body temperatures, but they are functionally ectothermic (Figure 18.2). Obtaining energy for metabolism is only one part of the story, however, and for complex organisms, there is another part to metabolism. Whether they are endo- or ectothermic, animals must thermoregulate— maintain body temperatures at certain levels or within certain ranges for biological processes to continue. Animals that maintain their body temperatures roughly at the same temperature as the environment are called poikilotherms, or heterotherms (hetero = different). For example,

442

CHAPTER 18    Dinosaur Physiology and Metabolism

Figure 18.2  (A) The functionally ectothermic mammal, Heterocephalus glaber (the naked mole-rat) has adaptations for a life underground, including greatly reduced vision, as indicated by the very small eyes, and reduced hearing, as seen in the very small ears. (B) These animals live underground in groups to help regulate body temperatures. (A

courtesy of T. Txuani, https://commons. wikimedia.org/wiki/File:Rata_Topo.jpg; B courtesy of B. Mazur, https://commons. wikimedia.org/wiki/File:Nest_of_naked_ mole_rats.jpg.)

snakes and lizards are ectotherms that use the sun to fuel their metabolic processes. They can tolerate significant drops or elevations in their overall body temperatures, which correspond to daily changes in environmental temperatures. Unlike reptiles, most mammals must maintain body temperatures within a very narrow range, and all their metabolic reactions are optimized for that small temperature range. Thus, they are endothermic homeothermic (homo = the same). For example, the average body temperature of a human is about 98.6°F (37°C), and we stay very close to that value, no matter what time of day, whether sleeping or running a marathon. A body temperature just a few degrees higher or lower than this value usually indicates illness— an elevation in a human’s temperature by just a few degrees (e.g., 101–102°F or 38.3–38.8°C) is a fever, and a temperature of 104°F (40°C) is a medical emergency. If body temperature drops to 95°F (35°C) or below, a person becomes hypothermic, and their physiological body processes begin to fail. But, heterotherms can tolerate wide fluctuations in body temperatures. Although heterothermy is not very common in mammals, their body temperatures can fall significantly during hibernation or torpor. An example of a mammalian heterotherm would be bats, which maintain high body temperatures when active, but in torpor, their body temperatures drop to environmental levels. Heterothermy in birds is, surprisingly, rather common. Birds can tolerate greater temperature shifts than most mammals, and large temperature shifts in core body temperature over short time periods have been recorded. Some birds can tolerate a drop of 10°F or more in body core temperature in as little as an hour, and still function just fine—whereas you would be dead, or close to it. Like endothermy and ectothermy, we observe a continuum between homeothermic and heterothermic (or poikilothermic) strategies in vertebrates. Thus, we must describe the metabolic “category” of an organism using at least two factors; whether they produce heat internally (endothermic) or get it from the environment or behaviors (ectothermic), and whether they can tolerate fluctuation (heterothermic/poikilothermic) or must maintain temperatures within narrow ranges (homeothermic). Although most mammals are endothermic homeotherms, birds, the descendants of dinosaurs, are endothermic heterotherms, because although they do use their own metabolic processes to provide heat for themselves (endothermic), they can tolerate a far broader range of temperature fluctuations. Additionally, virtually all birds, when they hatch, are functionally ectothermic, and must gain heat from their environment (or their parents) to survive—that is why birds brood their young. Anywhere from 24 hours to two weeks after hatching, the hatchling physiologies mature, and they can regulate their own temperatures and provide their own heat. It is easy to confuse ectothermy with heterothermy, or endothermy with homeothermy, but it is important to understand the differences between them (especially for dinosaurs) because some ectothermic organisms can exhibit short periods where they maintain body temperatures in a narrow range, and some endothermic animals exhibit some degree of

18.2  Costs and Benefits: Ectothermy vs. Endothermy

443

Figure 18.3  This artistic depiction of a sauropod attacking a predator and protecting its baby is exhibiting behaviors normally associated with endothermic (warm-blooded) animals.

However, whether or not these enormous animals could have operated with elevated metabolic rates is not universally accepted. (Courtesy of F. Gascó, https://commons. wikimedia.org/wiki/File:Brontomerus_ utahraptor2.jpeg.)

heterothermy. For example, an organism can be an ectothermic homeotherm: they get their energy for metabolic processes through outside sources, but (if they are big enough) they can maintain a body temperature within very narrow ranges. This is also called mass homeothermy because this ability is tied to size. Remember, all metabolic strategies are a continuum. Under varying conditions, these strategies can adjust somewhat, and, of course, they may also lower some with age. The patterns we observe in living animals may shed light on the evolution of these strategies by illuminating selective factors that might favor a slight shift toward endothermy or homeothermy. It has been proposed that the very big sauropod dinosaurs may have fallen somewhere in the middle of this continuum, but this idea is still controversial (Figure 18.3). Summary of physiological concepts: • Endothermy: Acquires energy to function through metabolism (e.g., mammals, birds) • Ectothermy: Acquires energy to function from the environment (e.g., lizards) • Homeothermy: Can withstand a narrow range of body temperature (e.g., humans) • Heterothermy: Body temperatures fluctuate (e.g., lizards, birds) Humans are endothermic and homothermic. Lizards are ectothermic and heterothermic. Birds are endothermic and heterothermic.

18.2 COSTS AND BENEFITS: ECTOTHERMY VS. ENDOTHERMY After reading this section you should be able to… • Explain selective factors that may have resulted in the distribution of different metabolic strategies. • Discuss the advantages and disadvantages of endothermic and ectothermic strategies.

All metabolic strategies contain advantages and disadvantages. Otherwise, animals would probably all use the same mechanisms. For example, one thing to consider when discussing metabolism is the differences between resting metabolic rate (RMR) and active metabolic rate (AMR). In fully endothermic mammals, the RMR is significantly higher than for

444

CHAPTER 18    Dinosaur Physiology and Metabolism

ectotherms by as much as a factor of 10. This means that food intake to maintain this must compensate. Warm-blooded animals need to eat between four and ten times the number of calories as the average ectotherm. Additionally, endotherms can maintain high levels of activity for much longer than ectotherms, and it takes them less time to recover after energy is expended. For example, you can run a marathon (at least theoretically), and then walk to the car when you finish. Both are (fortunately) impossible for crocodiles.

What are the advantages and disadvantages of each approach? Advantages to ectothermy: • Decreased food requirements: Ectothermic vertebrates don’t have to eat very much. Snakes and crocodiles, for example, are perfectly happy with about one meal a week, so they don’t have to expend a lot of energy to get food. • Survival in marginal habitats: Because of low intake requirements, they can survive in rather marginal habitats. Crocodiles can live in brackish environments with not a lot of food or oxygen in the water, and rely on occasional stragglers coming down for a drink to provide them with a meal they can live on for a long time. • Small environmental range: Because their food needs are reduced, they can survive in much smaller areas, or ranges, so they don’t have to expend energy to move or migrate. Ectothermy is the basal state for physiology. The vast majority of animals on our planet employ ectothermy, and it has worked well and has been around for a very long time. So why change it? There are disadvantages to ectothermy as well. Disadvantages to ectothermy: • Limited energy: Ectothermy only fuels activity in short bursts, which are followed by long recovery periods. Ectotherms can’t chase down prey because their muscles run out of fuel very rapidly. If a crocodile “misses” its prey on the first attack, it is usually out of luck. Therefore, they lurk underwater, waiting to ambush their prey. • Limited temporal range: Their activity is generally restricted to daylight hours (e.g., diurnal), because they derive their energy from the sun and warmer temperatures of midday. Ectothermic animals are rarely active during the night. • Slow growth rates: They don’t have the metabolic energy to grow fast, therefore it usually takes them years to reach sexual maturity, delaying the ability to reproduce. • Restricted habitats: Their habitats are restricted to those with mild, warm temperatures that don’t fluctuate widely. • Limited size: Among living terrestrial vertebrates, ectotherms don’t grow as big as endotherms. Elephants, the biggest living terrestrial endotherms, are bigger than crocodiles, the biggest living terrestrial ectotherms. Furthermore, many endothermic mammals are in the size range of crocodiles, or larger, while most ectotherms are usually much smaller. However, the crocodiles of today are much smaller and less diverse than some of the giants of the past that may well have preyed on dinosaurs. So, did the crocodiles of the past have a different metabolism, allow-

18.2  Costs and Benefits: Ectothermy vs. Endothermy

ing them to grow larger in the warm climates of the Cretaceous? If so, what are the implications for how we interpret dinosaur metabolisms? Further below, we will look at some evidence for this option. All of these factors show that ectothermy could create some challenges, and as we saw in Chapter 3, one of the main forces driving evolutionary change is competition. Just a little bit more activity, just a slightly bigger geographical and environmental range, or just an hour longer of daytime function could allow an organism to do better than competitors in the great game of life by providing advantages ectotherms do not possess. Advantages to endothermy: • Wide environmental range: Endotherms can function in a much wider variety of environments. Mammals and birds, for example, live on every continent and in virtually every environment. Penguins live in vast flocks in regions where temperatures stay far below 0°F for months. • Expanded temporal range: Endotherms can function over a broad temporal range. They can hunt at night, as well as in the daylight hours. These two factors mean that endotherms are able to occupy niches that ectotherms never inhabit, and this results in decreased competition. • Increased energy: Because endotherm muscles function more efficiently, they can maintain high activity levels longer and do greater muscular work. They can, for example, chase down prey over long distances. • Rapid growth: Endotherms grow very fast, relative to ectotherms, and thus they can reach a large size faster than their ectothermic counterparts. This reduces their vulnerability as prey, but also means they can reproduce earlier than ectotherms. Most birds, for example, reach full adult size and can reproduce within their first year, although larger birds of prey reach full size before they can reproduce. So why are there still any ectotherms? It seems like with all these advantages, everyone should be endothermic right? Disadvantages to endothermy: • Increased food requirements: One of the biggest problems with endothermy is that endotherms have to eat a lot, and often. It is estimated that endotherms require five to ten times more food than an ectotherm of comparable size. If food is limited for any reason, endotherms are greatly compromised. When it is very cold outside, intake needs are even greater. • Heat loss: Endotherms lose heat to the environment—the heat produced by their own metabolic processes. Because their body temperatures are usually much higher than ambient environmental temperatures, there is a net outflow of heat—much like if you were to go outside when temperatures are below 0°F without a hat. This is metabolically expensive for the organism. • Overheating: In hot environments, the big problem for endotherms is overheating. Without mechanisms to help them shed heat, which themselves consume energy, they can die. • Water loss: Some of the mechanisms that help shed heat, like panting or sweating, result in great water loss. Thus, endotherms

445

446

CHAPTER 18    Dinosaur Physiology and Metabolism

are not common in very dry, hot environments where water is limited, or have special adaptations to compensate for water loss.

18.3 HOW CAN WE KNOW WHAT KIND OF METABOLIC STRATEGIES DINOSAURS USED? After reading this section you should be able to… • List and describe features that are found only in living endotherms. • Construct a hypothesis for dinosaur physiology based on what you know about dinosaurs and living animals. • Suggest pathways by which dinosaurs may have regulated their metabolism. • List osteological correlates to increased metabolic rates.

To discuss what we currently know about dinosaur metabolism, let’s look at how (and why) our views have changed over time. Early paleontologists, when examining the first dinosaur fossils back in the 19th century, “knew” that dinosaurs were reptiles. Because these fossils exhibited many skull features (e.g., they are diapsids, Chapter 7) and skeletal characteristics that living reptiles (and, we would later find out, birds) also have, this relationship made perfect sense, and is reflected in the name they gave these extinct giants: dino = terrible/awe-inspiring; saur = lizard. Terrible lizard. Early paleontologists assumed that, if dinosaurs were reptiles, they must have shared other aspects of physiology and behavior with reptiles as well. Thus, dinosaurs were envisioned as slow-moving, enormous lizards with splayed posture, which were not very active and spent many hours basking in the sun, as good ectotherms must (Figure 18.4). But some features of dinosaurs led others, like Charles R. Knight, to interpret at least the theropods a little differently. His painting of the “Leaping Laelaps” (1897) would fit right in with today’s modern reconstructions (Figure 18.5). As more dinosaurs were discovered, we began to understand that they just didn’t fit the mold of a “good reptile”, like those extant ones with which we are most familiar. Perhaps living reptiles are not the best comparison for trying to understand the biology of these great beasts. So, what kind of metabolism did dinosaurs have? Were they endothermic or ectothermic, heterothermic or homeothermic? How can we know

Figure 18.4  Historical rendering of a long-necked sauropod demonstrating splayed posture and dragging tail, like all “good reptiles” do. (Courtesy of

H. Harder; public domain.)

18.3  How Can We Know What Kind of Metabolic Strategies Dinosaurs Used?

447

Figure 18.5  This painting by Charles M. Knight recognized that the proportions and anatomy of these theropod dinosaurs did not fit with perceptions of cold-blooded, sluggish, and slow-moving lizards. Although

first named “Laelaps” after a mythical Greek hunting dog, this dinosaur has been reclassified as Dryptosaurus. (Courtesy of Charles R. Knight, public domain.)

this when we can’t directly take their temperatures? Dinosaurs could have been ectothermic heterotherms like lizards and snakes, endothermic homeotherms like most mammals, or endothermic heterotherms like many birds. There probably isn’t just one answer for all dinosaurs— just as there are a wide range of body temperature “set points” for mammals, there was almost certainly variation among dinosaurs as well, both across time and in phylogenetic groups. How can we find out? Can the fossil record actually provide evidence related to the metabolisms of once-living dinosaurs? Even if we were able to recover “true” dinosaur DNA, it wouldn’t answer this question, because this trait isn’t encoded in the genome of any animal. There is no single gene thus far discovered that controls body temperatures—no “endothermy gene”—even in living organisms whose genomes we can fully characterize. So, we have to rely on other aspects of organisms that are likely to be preserved in the rock record to draw any conclusions about dinosaur metabolism. Only if we can identify consistent skeletal correlates from living animals whose physiology we understand can we begin to apply these to dinosaurs. As we have discussed many times, we can only understand the past through the lens of the present. By looking at living vertebrates across the spectrum of sizes, phylogeny, and metabolic strategies, we can observe some “morphological correlates” to endothermy. These are traits that are only observed in endothermic vertebrates today, and that no ectothermic animals are known to possess. Thus, if we can observe these traits in the remains of dinosaurs, it supports the idea that their metabolic rates were elevated above those of living ectotherms. Here are some anatomical and behavioral features that only endothermic vertebrates possess, which we discuss in detail below. We limit this discussion to terrestrial vertebrates; because of the very different physical demands of underwater life, and because dinosaurs were all terrestrial animals, some of the patterns we observe in terrestrial vertebrates don’t hold when we consider aquatic vertebrates (e.g., fish, whales). • Upright posture • Bipedality • Herding and migration • Wide environmental distribution • Large size • Epidermally derived insulation

448

CHAPTER 18    Dinosaur Physiology and Metabolism

• Mechanisms to shed heat • Incubation and brooding • Rapid or continuous growth • Four-chambered heart • Large and complex lungs and efficient respiration

18.3.1 Upright Posture Fully upright posture doesn’t just mean that the animal walks on two legs. Rather, it means that their legs are positioned directly under their bodies. Lizards, turtles, and other ectothermic animals have splayed posture, where their legs come out to the sides of their hips, and their forefeet are oriented away from the midline of the body (Figure 18.6). This results in a sinusoidal motion when they walk that they inherited from their fish ancestors, which makes them appear to wiggle as they run across the ground. This lateral bending means that muscles on one side of the body do the opposite of the other side, resulting in compression of the lungs on one side. Thus, breathing is constricted when they are moving—not an optimal condition, as you can imagine. Because it is shared by a wide group of organisms, from amphibians to turtles and crocodiles, it is considered an ancestral trait for vertebrates. Interestingly, crocodiles have splayed posture when resting or walking slowly, but when they need to hurry they can use an intermediate “high walk” posture for short periods of time, where they bring their limbs much closer to the body than during splaying. Footprint data indicates that the ability to walk upright is a basal trait among archosaurs, supporting the idea that the earliest ancestor of crocodiles, dinosaurs, and birds was an active, terrestrial animal. Even if all one has to observe are bones, we can see direct evidence of posture. In ectotherms, the head of the femur is angled to the shaft of the bone (and often the shaft of the bone is curved) in a way that allows for splayed posture (Figure 18.7). Conversely, living endotherms, like mammals and birds, have their legs oriented directly under their body (Figure 18.8).

18.3.1.1 What About Dinosaurs? We know dinosaurs also had upright posture. Even in the earliest dinosaurs, their legs formed a right angle with the axis of their bodies (Figure 18.9). This greatly increases the efficiency of movement, and it has another important result—it decouples breathing from walking, allowing dinosaurs to breathe more efficiently while moving. Animals with splayed posture alternately compress their lungs as they move from

Figure 18.6  This bearded dragon walks with fore- and hindlimbs coming out from the body midline at about 90° (blue lines). The feet are also

oriented away from the body in a splayed posture. This trait is widely distributed among ectothermic vertebrates. What patterns would you expect to see in the trackway of this animal? (Adapted from Ssfadia, https://commons.wikimedia.org/ wiki/File:Bearded_Dragon_Lizard.jpg.)

18.3  How Can We Know What Kind of Metabolic Strategies Dinosaurs Used?

449

Figure 18.7  (A) An alligator with arms and legs splayed, similar to other reptiles. The orientation of the tail to the head hints at sinusoidal motion. (B) However, alligators are also capable of a “high walk”, where much less of their body contacts the ground, and their fore- and hindlimbs are oriented more directly under the body. (Public domain.)

Figure 18.8  Birds, like this ostrich (A), and mammals, like this elephant family (B), have their legs directly under the body. This means that their

footsteps are much closer to the midline, their breathing is no longer coupled to their walking, and their movements are much more efficient. (Public domain.)

Figure 18.9  A massive sauropod in skeletal (A) and artistic reconstruction (B). Like most endotherms, these animals

show legs straight under the body in a “pillar-like” formation. (A courtesy of K. Tiffany, photographed at the Field Museum; B in the public domain.)

side to side while walking, making extended activity difficult. Interestingly, early crocodiles also showed upright posture, and many other attributes of elevated metabolism. The ectothermic ambush predators we observe today had ancestors that were capable of much more efficient movement than their living descendants.

450

CHAPTER 18    Dinosaur Physiology and Metabolism

18.3.2 Bipedality Today, only warm-blooded animals are fully (obligately) bipedal, meaning they must walk on two legs all the time. Obviously, endothermic mammals can be quadrupedal as well, but no living ectotherm is an obligate biped. Bipedality is efficient, as it frees the forelimbs for other purposes, but it is very energy expensive. Thus, bipedality seems to require increased metabolic rates

18.3.2.1 What About Dinosaurs? The earliest true dinosaurs, Eoraptor and Herrerasaurus, were already obligate bipeds (Figure 18.10). Their skeletons show that their arms were much shorter and more gracile than their legs, and they could not have supported their weight for walking full-time on them. That means that bipedality was the ancestral state for all dinosaurs, even lineages that would lead to the big, long-necked sauropods and massive triceratops. These dinosaurs became quadrupedal later in their evolutionary lineages. However, many lineages of ancient crocodiles were also bipedal (Figure 18.11). This suggests the possibility that elevated metabolic rates may be ancestral, not only for dinosaurs, but also for Archosauria! If so, then did today’s crocodiles somehow “lose” high metabolic rates? What forces would select for this?

18.3.3 Herding and Migration Among living terrestrial animals, only endotherms live in large herds, with hundreds to thousands of members. Lizards might coexist in small groups, but most ectotherms are rather solitary animals. Only endotherms, of all terrestrial animals, migrate over long distances. These two behaviors, herding and migration, are connected, in that warm-blooded animals have to eat a lot, and often, thus depleting their environments and necessitating frequent movement for new food sources.

18.3.3.1 What About Dinosaurs? Evidence for this in dinosaurs comes from two sources already discussed in Chapter 16: bonebeds containing thousands of individuals,

Figure 18.10  Skeletal reconstructions of two of the earliest dinosaurs known, Herrerasaurus (A) and Eoraptor (B), were quite obviously obligate bipeds. This trait is not found in

any living ectotherm. (courtesy of D. Evans and the Royal Ontario Museum, ROM©.)

Figure 18.11  Artistic reconstruction of Poposaurus gracilis, an early crocodile. This animal was also an

obligate biped. (Courtesy of Smokeybjb, https://commons.wikimedia.org/wiki/ File:Poposaurus_gracilis.jpg)

18.3  How Can We Know What Kind of Metabolic Strategies Dinosaurs Used?

451

Figure 18.12  Large monospecific bonebeds have been used as evidence that at least some dinosaurs lived and migrated in herds. (Courtesy of J. St.

John, https://flic.kr/p/2heah6R.)

and trackways, showing dinosaurs of many different kinds, moving long distances in large, monospecific groups. Bonebeds: Today’s herding animals, like caribou or bison, can live in groups numbering well into the thousands. When Lewis and Clark crossed the great plains of the United States, they commented on the bison herds that were “impossible to count”. When animals migrate in herds this big, they can also die together in catastrophic events, resulting in “mass death assemblages”. They may get caught in sudden floods crossing a river, or trapped by wildfires, and all die together. The same things happened to dinosaurs sometimes, resulting in thousands upon thousands of dinosaur bones in a relatively narrow area. We measure how many individuals are represented in fossil bonebeds by choosing one (non-repeating) bone in the skeleton and counting the number of examples we find of that bone. For example, if we have 1,000 left femora, we can say there were at least 1,000 individuals represented there; no animal has more than one left leg, with one left femur. Dinosaur herds, then, are counted by the minimum number of elements (MNE). If we have a thousand dinosaurs that all died together, it is highly likely that they lived together as well, supporting herding behavior (Figure 18.12). Trackways: They represent “in situ” behaviors, because unlike bones, trackways are not transported. As we saw in Chapter 16, trackways can reveal much about animal behavior, and dinosaurs are no exception. Trackway data, like bonebeds, also show that various groups of sauropods, hadrosaurs, and ceratopsians traveled together in herds. Migration, herding behavior, and trackway data are used to infer behavior— and behavior, as we have seen, is dictated to some degree by physiology. These data suggest the possibility of an elevated metabolic rate for dinosaurs.

18.3.4 Environmental Distribution Theoretically, the environments open to endotherms are only limited by the food source. Because they are endothermic, both mammals and birds can live at the North Pole (polar bears) or Antarctica (penguins). But although penguins do just fine during an Antarctic winter, crocodiles are never seen there. Because an ectotherm’s body temperatures are dependent on the environment, they are restricted as to where they can live.

18.3.4.1 What About Dinosaurs? Geology tells us that during the time of the dinosaurs, at least toward the end of their reign, northern Canada and the southern tip of Argenti-

452

CHAPTER 18    Dinosaur Physiology and Metabolism

Figure 18.13  The little theropod dinosaur Nanuqsaurus (A) was found in what is today Northern Alaska (B). The presence of many dinosaurs in

this region, where no non-dinosaur remains have been found, suggests a shift in metabolism for these animals. (A courtesy of N. Tamura, https://commons.wikimedia. org/wiki/File:Nanuqsaurus_NT_small.jpg; B adapted from L. B. Martínez, https:// commons.wikimedia.org/wiki/File:Nanuqsaurus_distribution_map.png.)

na had night-time and winter temperatures too cold and dark for living ectotherms to survive year-round, and we do not find their fossils there. So, when we find dinosaur fossils in those areas—and we have—we can infer that dinosaurs could produce more metabolic heat to keep themselves warm than could turtles or crocodiles. Large bonebeds of Edmontosaurus have been identified on North Slope sediments that date to the Late Cretaceous. In 2006, a small tyrannosaurid was found, also on the North Slope (Figure 18.13). This dinosaur is related to the much larger Tyrannosaurus rex, and is called “Nanuqsaurus”, or “polar bear lizard”. Although global temperatures were warmer in the Mesozoic than today, this far North Slope dinosaur would have still faced cold, and long periods of darkness. No non-dinosaurian reptiles have been recovered from this region.

18.3.5 Large Size Only endotherms among living terrestrial animals reach extremely large sizes. In part, this is because endotherms have the metabolic energy required to grow rapidly; thus, they can reach full adult size much sooner than can most ectotherms. Elephants, living endotherms, attain an adult mass of about 5,500 kg on average. The largest living ectotherm, an adult bull crocodile, averages about 1,000 kg. The largest animal of all time, the blue whale, is an endotherm, but also lives in the ocean, so faces different metabolic challenges.

18.3.5.1 What About Dinosaurs? Some of these generalizations fall apart for dinosaurs because there are really no living comparisons. Sauropods could grow to be the size of 14 elephants stacked on top of one another. Evidence from bone histology (see below) shows that many huge sauropods grew from an egg slightly smaller than a basketball to their massive size in a relatively short time (about 20–30 years)! Tyrannosaurus rex is one of the most massive bipedal animals known. Again, data from bone histology shows that they reached that size far faster than other theropods, showing a steep and exaggerated growth curve that has them reaching full size in about 20 years. How did their metabolisms play into these observations?

18.3.6 Epidermally Derived Insulation Among living animals, only endotherms have insulation. This comes sometimes as fat layers under the skin (blubber), and sometimes in the form of specialized structures arising from the skin, like hair and feathers. These forms of insulation exist because if an animal produces heat as a waste product of elevated metabolic rates (as endotherms do), it is

18.3  How Can We Know What Kind of Metabolic Strategies Dinosaurs Used?

453

not efficient to lose most of it to the environment. In fact, it is prohibitively expensive, metabolically; the requirements for food intake to maintain their energy levels would be nearly impossible to attain without some means to prevent heat loss. This is particularly important for small animals, because their surface area/volume ratios are not favorable to retaining heat. Thus, insulation is crucial for many small or young endotherms. Conversely, we don’t have any living feathered lizards or snakes, nor do we see crocodiles with hair.

18.3.6.1 What About Dinosaurs? We have recovered skin from many dinosaurs, and we have recovered evidence of feathers or filamentous coverings in many more. However, neither skin nor feathers are highly likely to persist in the rock record. Studies on living endotherms suggest that if feathers or hair were present, they would be more likely to appear in small animals, because they would lose heat proportionately faster than adults. Although smaller, basal relatives of Tyrannosaurus rex (e.g., Dilong) had feathers, we have not recovered feathers with any full-grown T. rex. Because maintaining insulatory coverings is metabolically expensive, and because big animals do not lose heat at easily as small ones, perhaps T. rex began life as a fuzzy feathered hatchling, but shed feathers as it grew (Figure 18.14). Alternatively, it is possible that because feathers serve functions other than insulation (such as display or species recognition) they might have been present but restricted to limited parts of the body. Thus far, we have recovered skin from embryonic titanosaurs, which show no evidence for feathers (though this does not rule out endothermy). Many small theropods, however, have been found surrounded by a dark, filamentous layer proposed to be “protofeathers”, or in some cases (like Anchiornis), with what appears to be fully modern feathers (Figure 18.15; see Chapter 14). At least one ornithischian (Psittacosaurus) appears to have long filamentous structures—but not all over the body, just the tail. However, these may have been convergent structures, perhaps used for display rather than insulation. Outside of Dinosauria, even some small pterosaurs (e.g., Jeholopterus ningchengensis) show evidence of a “furry” covering. When these examples are included, we may conclude that perhaps some form of insulation was ancestral for all diFigure 18.14  Although we have no direct evidence of feathers in Tyrannosaurus rex itself, close relatives of T. rex, such as the much smaller Dilong paradoxus from China, have been found with feathers preserved on parts of its body. From

this, we might hypothesize that T. rex had feathers on at least part of its body. A slightly less scary version of T. rex, perhaps, until we remember that this animal was 40 feet long and weighed about 7 tons! (Courtesy of M. Hallett.)

454

CHAPTER 18    Dinosaur Physiology and Metabolism

Figure 18.15  Examples of feathered dinosaurs from different clades of theropods. (A) Sinosauropteryx, a juvenile theropod from China. (B) Caudipteryx, the “tail-feathered” dinosaur. (C) Anchiornis huxleyi, a Jurassic dinosaur millions of years older than the first bird. (D) Microraptor gui, the first dinosaur recognized with feathers on its legs, so was known as the “four-winged dinosaur”. The white arrows show

preserved feathers and the black arrows show a “halo” around the specimen where they appear to be absent. However, this is most likely taphonomic artifact, reflecting more rapid degradation of skin than feathers, as we see in today’s birds as well. Degradation of skin and muscle sets up very local reduction zones because the microbes use up the oxygen as they degrade. This results in a reduction halo. (A adapted from Sam/OlaiOse/Skjaervoy, https://commons.wikimedia.org/wiki/ File:Sinosauropteryxfossil.jpg; B adapted from Daderot, public domain; C adapted from Bjoertvedt, https://commons. wikimedia.org/wiki/File:Anch​iorni​s_hux​leyi_​ -_mid​dle_j​urass​ic_Li​aonin​g_IMG​_5202​_Beij​ ing_M​useum​_of_N​atura​l_His​tory.​jpg; D courtesy of D.W.E. Hone et al., 2010.)

nosaurs, or for Avemetatarsalia in general! Clearly, we need more fossil evidence.

18.3.7 Mechanisms to Shed Heat As animals become more massive, they approach the opposite problem. Surface area/volume ratios change, and it becomes difficult for them to lose heat to the environment as fast as they produce it. Elephants today live in fairly warm climates, and when they reach adult size, retaining heat is not the problem--getting rid of heat is. Thus, they wallow in mud holes and flap their ears to shed excess heat. Other mammals find other ways to get rid of excess heat. Humans, of course, shed heat by sweating. Dogs and cats will pant, and although they don’t have many sweat glands on their body, they will sweat through their feet on hot days.

18.3.7.1 What About Dinosaurs? Sauropods in particular had to adjust to account for this problem because they were the most massive terrestrial animals to ever live. Not only did they retain heat because they were so big, this effect was heightened by higher global temperatures. Even taking into account that metabolism slows as an organism ages, if sauropods were fully endothermic, how could they have functioned without “cooking” their brains and other organs with retained metabolic heat? However, these most massive dinosaurs descended from (or shared a common ancestor with) much smaller ones, and would have inherited the metabolic strategies of their ancestor with elevated metabolic rates. There is a lot of evidence to suggest that sauropods grew to attain their great mass from relatively tiny hatchlings—and they grew very fast, at rates only seen in endotherms. So how did they overcome this limit of physics? Sauropods, remember, had vertebrae in their very, very long necks that were filled with holes and air sacs, and many other parts of the skeleton showed this trait as well. These lightened the mass of the animal, and in the case of that long neck, made it possible to hold up their tiny heads, but could also have functioned in shedding excess heat. It has been suggested that the sauropods shed heat with their long necks through increased surface area, just as elephants do with their big ears. A recent study used three-dimensional CT imaging to show that many dinosaurs had another way to compensate for excess heat. As dinosaurs increased in size in different lineages, they developed different vascular patterns that functioned specifically to cool the brain. They looked at areas with moisture-laden tissues, such as the nasal cavity, mouth, and eyes, first in living animals, then in dinosaurs. In living animals, as water

18.3  How Can We Know What Kind of Metabolic Strategies Dinosaurs Used?

evaporated from these moist tissues, it resulted in significant cooling of blood on its way to the brain. This evaporative cooling is marked by the presence of vascular networks that are recorded by the bone. Smaller dinosaurs don’t show vascularization increasing in different parts of the brain differentially, but larger dinosaurs—the ones that would have to shed heat—did. Blood flow was greatly increased to the regions in the head where these moist tissues are located in living archosaurs. In massive sauropods, both nasal and oral cavities show increased vascularity, suggesting evaporative cooling may have played a role in their thermoregulation. On the other hand, intermediate-sized dinosaurs like ankylosaurs preferentially sent blood just to the nose. Other dinosaurs, like T. rex, were certainly massive enough to require such specialized areas in the head for cooling, but they weren’t apparent until researchers examined the antorbital sinus (or fenestra). They showed that indeed, the bone around this area recorded dense concentrations of blood vessels. When air circulated around this sinus every time the animal took in a breath, it cooled the blood before it reached the brain, an efficient air conditioning system! Additionally, although the tiniest adult sauropods were at least an order of magnitude larger than the largest mammals of today, not all dinosaurs were so big that heat retention would be a problem. Those most closely related to birds in particular wouldn’t have needed specialized mechanisms to shed heat if they were endothermic.

18.3.8 Incubation and Brooding Only endotherms brood their young. Brooding requires the ability to impart body heat to eggs, and to do this more efficiently, some birds develop “brood patches” on their chest when they lay their eggs. Their feathers fall off, and blood vessels under the skin become very close to the surface, making heat transfer to the eggs much more efficient. Some birds find other ways to convey heat to the young. Penguins don’t shed their feathers, for example, as this would be very deleterious in subzero temperatures. Instead, they cradle eggs on their feet and cover them with “pouches” of skin. Interestingly, in birds where both genders participate in brooding the young, males can also develop brood patches! But, if they don’t have the ability to raise body temperatures above that of the environment, like an ectotherm, there isn’t any point to brooding, because they have no extra body heat to convey to their young.

18.3.8.1 What About Dinosaurs? We know that sauropods and other large dinosaurs did not brood their young by sitting on nests. If a 60-ton mother sits on an egg, that is a rapid path to extinction! Instead, there is evidence that, like living crocodiles, they may have covered their eggs with vegetation that provided heat to the eggs as it decayed. But some dinosaurs, particularly those closest to living birds, did sit on their nests, and brooded eggs in a manner and pose identical to modern birds. We know this because we have fossils that caught them in the act! The most famous of these fossils (see also Chapters 14, 16, 17, and 19) was discovered in 1995 by crews from the American Museum of Natural History in New York, who joined with paleontologists in Mongolia to discover a beautiful oviraptor sitting on a nest filled with eggs, its arms perfectly positioned to protect them (see Chapter 17, for a more in-depth discussion). Since the discovery of this oviraptor, several other specimens of maniraptoran dinosaurs have been found in similar poses—behavior that no living ectotherms share (Figure 18.16).

455

456

CHAPTER 18    Dinosaur Physiology and Metabolism

Figure 18.16  The arms of this Citipati specimen are extending outward from the body, covering and shielding the eggs beneath. The feet and legs are

folded between them just as with modern birds that brood their eggs. This pose has only been observed in animals that brood— and brooding specifically occurs to provide heat to developing eggs. This spectacular specimen is direct evidence for elevated metabolic rates. (Adapted from Dinoguy2, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=10​90758​.)

18.3.9 Rapid and/or Continuous Growth Growth rates in living organisms correlate to physiology—generally speaking, the faster an organism grows, the higher the metabolic rate required. Endotherms, among living animals, are capable of much more rapid growth than ectotherms. This is particularly evident in larger animals. For example, elephants can go from a birth weight of about 200 pounds to several tons in the space of five to ten years or so. All birds reach their full adult size within 12 months or less. For many birds, adult size is synonymous with sexual maturity and the ability to reproduce, but larger birds may attain skeletal maturity before reproductive maturity, and this is reflected in their bone histology (histo=tissues, ology=study of). Although some small lizards can also reach adulthood within a year, larger ones, like the Komodo dragon, take at least five years to go from hatchling to adult. These animals start out with larger eggs (about twice that of chickens), and thus larger babies, which can reach 300 lbs. or more as adults. How do we tell how fast an animal grew when we can’t observe it growing? One way is to look at how fast their bone tissue was developed; the faster bone is deposited, the faster an organism grows. Thus, for this type of investigation, we look at the histological features preserved in the bones, particularly of young animals. This is because, regardless of physiology, most of the growth of an animal is in its early years; thus, all vertebrates, both endothermic and ectothermic, eventually slow their growth rate when they reach maturity, but this does not indicate a change in the metabolic strategy—only a change in their rate of growth. We assess how rapidly bone tissue was laid down by examining its organization at the microscopic level, and to see how this tissue organization can be used to shed light on dinosaur growth, we must look to living animals for comparison. Under the microscope, bones exhibit certain patterns that remain the same, or virtually so, for all terrestrial vertebrates. For example, bone tissues are all composed of protein (mostly collagen) and mineral, they are vascular, and they are secreted and maintained by bone cells called osteocytes (see Chapter 6 for review). Although all bones share these features, their relative abundance, organization, and orientation at the microscopic level are correlated to the metabolism of the animal that laid it down. Microscopic correlates for metabolism in bone include: • Collagen fibers: Direction, orientation, and packing of collagen fibers

18.3  How Can We Know What Kind of Metabolic Strategies Dinosaurs Used?

457

• Osteons: Size, density, and number of osteons • Vascularity: Orientation and relative number of blood vessels When bone is laid down slowly, the collagen fibers are laid down in a highly ordered arrangement. It takes longer to stack things neatly and organized in your closet than to just throw stuff in and shut the door. Then, bone mineral (apatite) aligns along those fibers, with the long axis of the crystal parallel to the length of the collagen fiber. This arrangement gives bone-specific characteristics that are recognized in polarized light (e.g., birefringence and anisotropy), which are retained in virtually all fossil bone. These patterns of mineral crystals inform on the direction and organization of collagen, even if this protein is no longer present. In slow-growing bone, collagen forms lamellae (stratified or layered patterns), which is referred to as lamellar bone. But, when animals grow very fast, the fibers are randomly organized, loosely packed, and go in different directions. We call this woven bone. The mineral crystals still align on the fibril but form a completely different pattern under polarized light, so it is easy to see under the microscope. We know that in living animals, the more random the fiber orientation, the more rapidly the bone was laid down, and rapid deposition of bone requires high energy input, seeming to be a straightforward correlation to elevated metabolic rates. However, this too is not all that simple. Deposition of bone is often interrupted by “lines of arrested growth” or LAGs (Figure 18.17), that record regular or cyclic periods in the animal’s life when bone growth slowed or stopped, much like tree rings record seasonal shifts in growth. These LAGs are commonly observed in vertebrates, including mammals, but are not obvious in birds that attain full growth in a year or less. For those few birds that take longer than a year to reach adult size, such as the kiwi, LAGs are present. When first noted, the presence of LAGs was taken by many to be tightly correlated to ectothermy, but as we observed more and more taxa, it appears that the presence of LAGs is a (ancestral) trait for all vertebrates. Furthermore, because each bone in a skeleton grows at different rates, the number of LAGs in each bony element may vary, even within a single skeleton! LAGs, on their own, cannot be used to interpret physiology; they can only indicate that growth was paused for a time, then resumed. It is the type and amount of bone deposited between these lines that can shed light on the rate of growth. Virtually all tetrapod bone is vascular (infused with blood) to some degree—although in slow-growing animals, or when growth has slowed with maturity, vascularity decreases. The degree of vascularization has

Figure 18.17  Schematic illustrating components of bone microstructure, such as lamellar bone, woven bone, lines of arrested grown (LAGs), and the different ways that vascular canals may be oriented. High vascularity,

fibrolamellar orientation, and laminar, reticular, and radial vessel orientation are correlated with rapid growth. A high degree of secondary osteons indicates remodeling, which is also correlated with rapid growth and elevated metabolic rates. (Courtesy of H. Woodward, A. K. Huttenlocker, H. N. Woodward, B. K. Hall, 2013)

458

CHAPTER 18    Dinosaur Physiology and Metabolism

been correlated to metabolism, and this makes sense—more blood vessels mean more nutrients are carried to the cells that produce bone matrix. Channels in which blood vessels lie are surrounded by bone cells (osteocytes) and collagen. In ectotherms, the vessels are simple holes that penetrate the matrix, but in the bone of more derived ectotherms and endotherms, these channels are at the center of structures called osteons. When bone is cut in cross-section, the osteons look like an archery target, with the center “bull’s-eye” housing an open space for blood vessels and nerves (Figure 18.18). In living endothermic animals, the bones show a lot of blood vessels. This is not so apparent in ectothermic bone. These osteons change as bone ages. As mentioned previously (Chapter 6), one function of bone is as a reservoir for minerals, especially calcium. Without calcium, vertebrates cannot live, because calcium is required for muscles (including the heart) to contract. The greater the metabolic demand, the higher the rate at which bone turns over, going through cycles of resorption and deposition (Figure 18.19). Metabolic demand is very high during growth, as it is an energy-intensive process. During growth, bone dissolves when demand is high, and then is redeposited as demand lessens to keep blood calcium levels constant. This is reflected in the bone microstructure. Small primary osteons (Figure 18.18) are formed when the bone is being laid down in young animals. Secondary osteons form when bone around the blood vessels dissolves to release calcium to the blood (Figures 18.17 and 18.18). The vascular channels expand greatly; then bone redeposits from the outside in, leaving dark “cement” (or “reversal” lines). Remodeled osteons are much larger than primary ones, and have dense “rings” around the outside, indicating that bone has gone through this process of resorption and redeposition, or remodeling. In most animals that have attained sexual maturity, we see both primary and secondary osteons. But, in virtually all animals except those that reach full size in under a year, bones record a cyclical pattern of growth, with the rapid growth phase interrupted by a time of non-deposition, or LAGs. (Figure 18.17).

18.3.9.1 What About Dinosaurs?

Figure 18.18  Image of modern bone taken with interference contrast microscopy. This image shows secondary

osteons (SO), marked by their well-defined cement lines (arrows). Secondary osteons look like a target, with the center canal housing blood vessels and nerves. A primary osteon (PO) is also present, which has a smaller canal for blood vessels and no cement line. Surrounding both types of osteons are layers of concentric osteocytes (e.g., arrowheads). Although not visible at this magnification, they have long filopodia extending to communicate to other cells. Osteons are the fundamental unit of endothermic bone microstructure. Although ectotherms can show osteons, these usually arise as a result of remodeling. (Courtesy of J. Reischig, https://commons.wikimedia.org/ wiki/File:Cross-cut_bone.jpg.)

How can we estimate how fast dinosaurs grew? First, populations of living endotherms usually show a bimodal distribution, where adults and very young are (typically) observed—not a continuum of size. This suggests that adult size is attained rapidly. In large bonebeds containing a single taxon of dinosaurs, we generally see the same pattern, suggesting that dinosaurs also attained adult size rapidly. However, although suggestive, this is not definitive, because small bones usually have low-

18.3  How Can We Know What Kind of Metabolic Strategies Dinosaurs Used?

459

Figure 18.19  Schematic showing the phases of bone remodeling. When

er preservation potential than large ones. Perhaps those representing young dinosaurs were not so readily preserved. We always have to remember taphonomy when trying to interpret any fossils we study. Fortunately, we have a more direct way to estimate growth rates: by looking at the microstructure of bone and comparing patterns with those seen in living bone.

calcium demand is high, cells (monocytes) are recruited from the blood. These fuse to form giant multinucleated cells called osteoclasts that secrete acid and enzymes to break down bone, releasing calcium into the blood. When calcium demand lessens, cells from the connective tissue surrounding the bone differentiate to become osteoblasts, which begin to secrete osteoid or unmineralized bone matrix. As the matrix mineralizes, these osteoblasts become trapped, and differentiate to become mature osteocytes once more. This process is more frequent in endotherms because calcium demand is greater due to increased muscle activity and other demands, and is marked by second, third, and fourth generation secondary osteons. (Adapted from SMART-Servier Medical art, https:// commons.wikimedia.org/wiki/File:Bone​ _rege​nerat​ion_-​_Bone​_remo​delin​g_cyc​le_2_​ -_Pre​-Oste​oblas​t_Ost​eobla​st_Bo​ne-li​ning_​ cell_​etc_-​-_Sma​rt-Se​rvier​.png.​)

Because the mineral crystals in bone align with the fibers, these retain the original pattern even after collagen degrades (Figure 18.20). Dinosaur bone varies a lot among different groups, but most dinosaur bone shows patterns more similar to birds and mammals than to living ectotherms. Mammals, and dinosaurs, have a haphazard, random organization of woven bone, which is consistent with rapid deposition. But they also show evidence of growth slowing or stopping, indicated by a distinct LAGs. Then, growth resumes and bone is again laid down rapidly once more. Because the bone of most dinosaurs shows microscopic charac-

Figure 18.20  (A) Ground section of the bone of a subadult Troodon formosus.

The top is the outermost surface, and the bottom defines the medullary cavity. The newest or youngest bone is at the top, where bone is laid down very rapidly (fibrous) and then quickly invaded by blood vessels (developing primary osteons, DPO), which will eventually become tightly encased in bone to become primary osteons (PO). Vessels are arranged in a longitudinal to radial pattern. Two lines of arrested growth (LAGS) interrupt the fibrolamellar bone of most of the cortex. In the inner layers, which represent the oldest bone, remodeling has begun, illustrated by the presence of erosion rooms (ER) and large secondary osteons with cement lines (SO). (Courtesy of D. Varricchio, 1993.)

460

CHAPTER 18    Dinosaur Physiology and Metabolism

teristics more similar to the bone of living endotherms than ectotherms, it suggests that most dinosaurs had metabolic rates that could sustain higher growth rates than today’s lizards and crocodiles. Although some histological evidence suggests that some sauropods may have grown a bit slower than the big herbivores of today, in many other dinosaur lineages, growth probably approximated, or even exceeded, the growth of living mammals, and came close to approaching the growth rates of birds, most of which go from hatchling to adult in less than a year.

18.3.10 Four-Chambered Heart Animals can have hearts with two (many fish), three (“reptiles” and amphibians), or four (mammals, birds) divisions, or chambers. The more chambers the heart has, the more efficiently it can pump. Further, if the chambers are fully separated, the heart can separate deoxygenated (used) blood from fresh, fully oxygenated blood efficiently. Oxygen fuels metabolism, and animals with fully separated blood have more stamina and can function at higher activity levels more efficiently for a longer time period without having to pause in activity. Living endotherms like mammals and birds have four-chambered, fully separated hearts, so there is no mixing of oxygenated and deoxygenated blood. Thus, the concentration of oxygen in blood flowing to their organs is high, and more oxygen is carried by the blood to distant parts of the body, making more available for fueling muscular work. The four-chambered heart that mammals possess evolved completely separately from those of birds (a convergence), because these groups are only distantly related (Figure 18.21). Intriguingly, living crocodiles and their distant relatives, turtles, are the only ectotherms with a three-chambered heart. Turtle phylogeny is contentious, but recent molecular studies place them as a sister group to Archosauria. Of course, crocodiles fall within Archosauria, making them the closest living relatives to modern birds. Thus, crocodiles share an ancestor in common with dinosaurs and birds. It could be that a four-chambered heart was achieved in this lineage before crocodiles diverged from dinosaurs and birds. Because basal crocodiles share other traits with endotherms (e.g., bipedality, upright posture), it is suggested that the common ancestor of crocodiles and birds may have attained an elevated metabolism. It seems that active elevated metabolism most likely arose at the base of all archosaurs. Most sauropsids (“reptiles”), however, are fully ectothermic and possess three-chambered hearts.

18.3.10.1 What About Dinosaurs? There are no fossilized dinosaur hearts, so how can we possibly know what kind of heart dinosaurs had? This trait can be inferred from fossil remains with confidence, even without preserved hearts. Two lines of evidence support the idea that dinosaurs had these efficient hearts: phylogenetic bracketing (see Chapter 4 and Figure 18.21) and morphological correlates for traits that only animals with four-chambered hearts possess. Indirect evidence for a four-chambered heart in dinosaurs comes from posture and bipedality, as mentioned previously. Getting blood to a head elevated above the center of gravity requires greater pressure than a three-chambered heart can generate. Assuming that the laws of physics were the same in the Mesozoic (a very safe assumption!), for very long-necked sauropods and any bipedal dinosaur, a four-chambered heart would be required to generate enough pressure to get blood to their brains. Thus, both more oxygen carried by the blood, and the pressure differential required to serve the brain, are evidence that dinosaurs required four-chambered hearts to function. We can’t say that

18.3  How Can We Know What Kind of Metabolic Strategies Dinosaurs Used?

461

Figure 18.21  This cladogram of vertebrates depicts where on the tree four-chambered hearts definitely arose. Among living animals, we know

that mammals and birds—the only living endothermic groups—both exhibit fourchambered hearts. But so do crocodiles! These separated hearts are required to generate the pressure differential needed for blood to circulate efficiently in active animals. But why are they present in crocodiles, which are ectothermic?

a four-chambered heart is absolute evidence for endothermy (i.e., not all animals with a four-chambered heart are warm-blooded) because crocodiles have them. But we can say that if an animal is endothermic, it must have a four-chambered heart.

18.3.11 Lungs and Respiration Respiration begins in the nose, and even here, we can see differences between endotherms and ectotherms right away. In addition to the vascular patterns mentioned above, the nasal areas of ectotherms are simple cavities of bone lined with tissue. But the nasal cavities of living endotherms are very complex, with all kinds of bony struts and scrolls (turbinates) that exist to increase the surface area available for air to move across (Figure 18.22). This is important because, for animals that live on land, the air they breathe in is harsh and dry compared with the warm, moist environment of the lungs where oxygen is exchanged into the blood. These nasal turbinates are lined with wet tissues that warm and moisten incoming air so that it begins to match the temperature and humidity of the lungs. Because endotherms take many more breaths than ectotherms over the same amount of time to get the required oxygen to “burn” metabolic fuel, it greatly increases the efficiency of breathing to process air this way. Interestingly, to date, no non-avian dinosaur has been found with nasal turbinates, though they are present in most birds.

Figure 18.22  Turbinates in the skulls of endotherms. (A) The scroll-like turbinates in a bison skull. (B) Turbinates in the nasal cavity of a bat. (C) Turbinates in a gray wolf skull. These bony struts are covered with moist and

highly vascular tissues, expanding the surface area so that when air is inhaled, it passes across these membranes and picks up both moisture and heat to protect the air passages from drying out. These are not found in ectotherms—or dinosaurs! (All courtesy of K. Tiffany, wolf skull courtesy of A. Heartstone-Rose.)

462

CHAPTER 18    Dinosaur Physiology and Metabolism

Breathing is a process we all take for granted because we do it constantly, but it actually involves complex physics; oxygen in air has to move across membranes of the lungs and into the blood through diffusion, a passive process that is based upon concentration gradients. Blood is much more viscous than air, and resistance to diffusion is great. Oxygen moves from the lungs, where it is high in concentration, into red blood cells, where the concentration is lower, until the cell is “fully loaded” with oxygen (Figure 18.23). When the blood reaches tissues, where oxygen concentration is lower than in the blood, oxygen moves out of the blood cells and into the tissues, again by passive diffusion. The higher the concentration of oxygen relative to the tissues, the faster this movement occurs. Think about the speed of a ball rolling down a steep slope, as opposed to a shallow slope—the ball moves faster the steeper the slope. When the concentration of oxygen is low and closer to that of the tissues, the “slope” is shallower, and the movement is slower. Animals with high metabolic demands need to keep this slope steep. They do this by increasing the surface area of tissues participating in gas exchange, and by keeping the “slope” steep. Thus, most ectotherms have simple and relatively undivided lungs, with surface area not much greater than the volume. Mammals and birds, however, have lungs that are deeply divided into progressively smaller units to greatly increase the surface area (as much as 70 m 2, or ~753 ft 2) in the regions where gas exchange occurs. Lung structures across terrestrial vertebrates vary greatly. In general, the higher the metabolic rate, the more complex the lungs, because the internal surface area of the lung must increase. For amphibians and some basal reptiles, lungs are simple, sac-like structures, with relatively little surface area for oxygen exchange. They are small, with low metabolic rates, and these lungs meet their needs. In addition, many amphibians also exchange oxygen across their skin, which is why it must always remain moist. Conversely, in mammals, lungs are divided into smaller and smaller units, ending in grape-like clusters called alveoli (Figure 18.23), where the air is only separated from the blood by a thin layer two cells thick. These divisions within the lung tissue result in a vastly greater surface area across which oxygen can diffuse. However, this efficiency is somewhat compromised by the two-way (bi-directional) flow of air in mammal lungs. Air in mammal lungs goes in and out

Figure 18.23  Diagram of the respiratory system of a representative mammal. Air is taken in via the nose and mouth, and enters the lung via bronchi

and bronchioles (left) but no oxygen is exchanged until air reaches the alveoli deep in the lung (middle). Separation between blood and air in the alveoli is only one cell layer thick so gasses can be exchanged efficiently and rapidly (right). Oxygen is downloaded to the blood cells and CO2 moves out of the blood and into the alveoli where it leaves with the next exhalation. Mammalian lungs are a two-way system where oxygen-rich air and CO2 rich air pass through the same pathway. (Alveoli artwork (left) courtesy of H. Fisher, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=24​36713​7; gas exchange (right) artwork courtesy of Delmalani18, https​://co​ mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​id=69​61393​8.)

18.3  How Can We Know What Kind of Metabolic Strategies Dinosaurs Used?

463

through the same path, so oxygen-rich air from the outside can mix directly with oxygen-poor air, making exchange gradients more shallow and oxygenation less efficient. Archosaurs like crocodiles and birds have different lungs entirely. Crocodiles have more complex lungs than amphibians and other reptiles, probably reflecting a higher ancestral metabolic rate, and their lungs are also heterogeneous, meaning they differ structurally from the proximal (headward) to distal parts. Mammal lungs, though more complex, are homogenous: structured the same throughout the organ. Crocodiles, like mammals, also breathe using a diaphragm—a tough membrane that separates the heart and lungs from the intestines. In mammals, the diaphragm is muscular; a hiccup is a muscle spasm of your diaphragm. Crocodile diaphragms, however, are passive and not very muscular. Instead of having muscles within acting to contract it, the diaphragms of crocodiles are worked by strong muscles attached to the pelvis. This means that although crocodile lungs are more complex than those of other ectotherms, their breathing is still coupled to their locomotion. Birds, however, exhibit a type of lung and respiratory system not seen in any other terrestrial animal. Birds lack a diaphragm completely, and they utilize unidirectional air flow. The only time air mixes in birds is at the very end of their nasal cavities and bronchi, so the air inside the lungs is always fully oxygenated, and not diluted by oxygen-poor blood as in mammals (Figure 18.24). This is accomplished in part by air sacs that arise from the lung. No oxygen is exchanged in these sacs, they simply “hold” the air until it can move to the lungs, like bellows. This unidirectional flow allows a much steeper oxygen gradient between the air in the lung and the blood that flows through it. The steeper the gradient, the more rapidly and completely oxygen moves into the blood cells in the lungs, and the more rapidly the oxygen moves from the blood into the low-oxygen environment of the tissues. So, not only does a four-chambered heart mean more oxygen is carried by bird blood, their lungs are at least ten times more efficient at transferring oxygen to the blood than mammal lungs.

18.3.11.1 What About Dinosaurs? Like hearts, lungs do not fossilize. So how can we investigate the lungs and respiratory systems of extinct dinosaurs? Again, we look to phylogeny, and the animals that bracket dinosaurs on their phylogenetic tree. However, it isn’t as straightforward as hearts, because while crocodiles and birds both have four-chambered hearts, their lungs—and the way they breathe—are very different. Both of these groups have unidirectional air flow, so we can infer that unidirectional air flow may have been present in all dinosaurs. However, where dinosaur lungs fit in complexity,

Figure 18.24  A schematic drawing of the inhalation and exhalation cycles of respiration in living birds. Birds are

unique among living vertebrates in that they lack a diaphragm and have rigid lungs. Air is moved through the lungs by numerous air sacs anterior and posterior to the lungs in a unidirectional flow, preventing the mixing of oxygen-rich and CO2-rich air. This, coupled with a continually high gradient between the air and the blood (maintained by a countercurrent system in the lungs), means that in birds, oxygen is exchanged at a rate about ten times higher than the average mammal. (Adapted from L. Shyamal, public domain.)

464

CHAPTER 18    Dinosaur Physiology and Metabolism

Figure 18.25  Hypothesized reconstruction of a dinosaur respiratory system with air sacs, similar to what is observed in birds.

As discussed in Chapters 9 and 19, the bones of saurischian dinosaurs show definitive evidence of pneumaticity, which, in birds, arises from these air sacs. (Courtesy of CNX OpenStax, https://commons. wikimedia.org/wiki/File:Figure_39_03_01ab. jpg.)

and whether or not (or when) they lost a diaphragm, is less clear. What we do know for certain is that all saurischian dinosaurs have hollow, pneumatic bones, like birds (see Chapter 19), as do pterosaurs. Pneumatic bones in birds arise from the extensive system of air sacs that is key to their respiratory system (Figure 18.25). Thus, the presence of pneumatic bones across members of Avemetatarsalia (though curiously, not in ornithischian dinosaurs) suggests that members of this group might have had respiratory systems more similar to birds than crocodiles. This may explain, in part, how they obtained the “fuel” for rapid growth and efficient movement.

18.4 SO, WHAT KIND OF METABOLISM DID DINOSAURS HAVE? All we have to answer this question is the presence or absence of the skeletal correlates listed above that are present in animals with elevated metabolic rates. Most dinosaurs across all lineages had some of these traits. Further, many of these traits, like upright posture and bipedalism, were ancestral for all dinosaurs, and some were ancestral in archosaurs as well. However, some important traits linked to endothermy are missing in dinosaurs. In particular, dinosaurs have not been found to possess respiratory turbinates. Not all dinosaurs exhibited insulatory structures (sauropods, for example) or brooding, but many did. Thus, the answer isn’t cut and dry. The best we can say is that all dinosaurs had metabolic rates elevated above that seen in living lizards, snakes, and turtles—above even that of living crocodiles and alligators, which as we discussed here are very different from lizards, despite being ectothermic. Additionally, dinosaurs most closely related to birds seem to have attained the same metabolic levels, showing all the traits that are linked to elevated metabolism in living birds.

18.5 WHAT WE DON’T KNOW We can now make a lot of inferences about dinosaur metabolism, and these can be supported with many lines of evidence. Our picture of these creatures has changed from slow-moving, water-bound, low functioning brutes to active animals that filled many diverse niches. But there are still many things we don’t know about dinosaur metabolism.

18.5.1  Did All Dinosaurs Have Similar Metabolic Rates? Dinosaurs originated about 240 million years ago, in the Triassic. They were small, bipedal, and from what their bones and morphology tell us,

18.5  What We Don’t Know

probably very active. But over the next ~160 million years, they diversified in many ways: they got very big and very small, they lived in warm moist climates and dry, hot ones, and some even lived in places with long and cool nights. So, did dinosaurs (as a group) have a range of resting body temperatures to accommodate their different lifestyles and environments, or were they all uniform in metabolic strategies? Questions to consider: • How might you investigate (perhaps subtle) differences in metabolism within an extinct group when its nearest extant relatives (crocodiles and birds) represent opposite ends of the metabolic spectrum? • What sort of physiological evidence would you need to compare between dinosaur species, and how likely is that evidence to be preserved?

18.5.2 Did Sauropods Change Their Metabolic Rate as They Aged? Bone histology shows that young sauropods grew very fast, at rates only shown by fully endothermic animals today. After all, there was a size limit to how big their eggs could be because the bigger the egg, the thicker the shell has to be; the thicker the shell, the less oxygen can diffuse to the developing embryo. Yet, sauropods attained a mass many times greater than the largest warm-blooded animals today within a relatively short period of time (~30 years). From what you have learned of the evidence that exists, how could sauropods “fight” the laws of physics, where surface area to volume ratios become unfavorable for shedding heat the larger they grew? Questions to consider: • Could sauropods have possessed some novel biological mechanism to shed heat? How would you go about testing this hypothesis in species for which we have no living analogs? • Could sauropods have gradually changed their metabolic rate as their growth rates declined in a way not demonstrated in any living animal? How could we test hypotheses about dinosaur’s metabolic rates independent of their growth rates (which is usually assessed through histology)? • Sauropods are structurally unique in many ways. Did their long necks play any role in their unique metabolism? How could we explore this? • Would insulatory covering play a role? What effect might it have if they were feathered when tiny, but lost these as they grew?

18.5.3 When in the Dinosaur Lineage Did Metabolic Rates Start to Increase? And When Did These High Metabolic Rates Become Fixed, as We Know They Did in Birds? In the warm and stable global climates that dominated when the dinosaurs originated, they probably did not need metabolisms greatly elevated above their competitors, and these rates could have risen slightly without a much greater need for food. After all, just a little bit more activity earlier or later in the day than their competitors would have given them a very great advantage. Was this a kind of “arms race” in dinosaurs, where keeping that metabolic advantage required ever-increasing

465

466

CHAPTER 18    Dinosaur Physiology and Metabolism

adaptations to take in more food and oxygen? Or, as some evidence seems to suggest (see Legendre et al. 2016 and Cubo et al., 2019 in Literature), were archosaurian metabolic levels already high before dinosaurs, with living non-avian archosaurs representing a return to lower metabolisms? Questions to consider: • What selective pressures may have contributed to, or driven, the transition to endothermy in the dinosaur lineage or their archosaur ancestors? • Modern birds need an enormous amount of metabolic energy for flight, but clues to their metabolism (presence of LAGs, etc.) are often difficult to find in histological bone sections because their limb bones are thin and hollow (adaptations that make their skeletons suitable for flight), and because most reach full size and stop growing within their first year. How do you think this affects our interpretations when looking at birds and non-avian dinosaurs in the fossil record? How would you try to account for these effects?

18.5.4 What Drives Higher Metabolic Rates at the Cellular and Molecular Levels? Although there is no specific gene for “endothermy”, all changes and adaptations that have occurred in lineages over time must have a genetic basis, or they cannot be passed on to offspring. So, what genes may have been involved in the endothermic transition within the dinosaur lineage or their archosaur ancestors that we know resulted in warm-blooded birds? Questions to consider: • How can we ask genetically based questions about dinosaurs if we will (probably) never have dinosaur DNA sequences?

18.5.5 How Can Dinosaurs Contribute to Our Understanding of Living Animals? To understand anything about dinosaur metabolism we have to study the range of metabolic strategies in living animals, and look for correlates that might survive and be preserved in fossilized remains of extinct animals. But can that apply in the reverse also? All living organisms today are the result of all the “choices” made at turning points in their evolutionary history. By studying how these metabolic changes occurred over time in dinosaurs, can we shed light on, and make predictions for, how living organisms might respond to global climate changes in the future? Questions to consider: • What particular evidence for climate/environmental changes might we see in the fossil record? How do you think these can be correlated to what may be occurring in our planet today? How long would these trends have to last to drive evolution? One generation? Ten? More? • How would you recognize environmental conditions/changes in the fossil record? How might you correlate these to shifts in animal physiology? What sort of specimens would you need to investigate any such correlation? What would you need to know about geology and the distribution of dinosaurs to truly address this?

18.5  What We Don’t Know

467

INSTITUTIONAL RESOURCES Chinsamy-Turan, A. (2005). The Microstructure of Dinosaur Bone: Deciphering Biology with Fine-Scale Techniques. Johns Hopkins University Press, Baltimore, Maryland. Ohio University, Ohio News. https​: //ww ​w.ohi​o.edu​/news ​/ 2019​/10/n​ew-oh​io-st​ udy-s​hows-​huge- ​dinos​aurs- ​evolv​ed-di​f fere​nt-co​oling​- syst​ems-c​ombat​-heat​. Padian, K., and Lamm, E. T. (Eds.) (2013). Bone Histology of Fossil Tetrapods: Advancing Methods, Analysis, and Interpretation. Univ of California Press, Oakland, California.

LITERATURE Brocklehurst, R. J., Schachner, E. R., Codd, J. R., and Sellers, W. I. (2020). Respiratory evolution in archosaurs. Philosophical Transactions of the Royal Society Series B, 375(1793), 20190140.

Huttenlocker, A. K., Woodward, H. N., and Hall, B. K. (2013). The Biology of Bone. University of California Press, Berkeley, CA, pp. 13–34.

Clarke, A. (2013). Dinosaur energetics: Setting the bounds on feasible physiologies and ecologies. The American Naturalist, 182(3), 283–297.

Legendre, L. J., Guénard, G., Botha-Brink, J., and Cubo, J. (2016). Palaeohistological evidence for ancestral high metabolic rate in archosaurs. Systematic Biology, 65(6), 989–996.

Cubo, J., and Jalil, N. E. (2019). Bone histology of Azendohsaurus laaroussii: Implications for the evolution of thermometabolism in Archosauromorpha. Paleobiology, 45(2), 317–330.

Myhrvold, N. P. (2016). Dinosaur metabolism and the allometry of maximum growth rate. PLoS One, 11(11), e0163205.

Hone, D. W., Tischlinger, H., Xu, X., and Zhang, F. (2010). The extent of the preserved feathers on the four-winged dinosaur Microraptor gui under ultraviolet light. PLoS One, 5(2), e9223.

Varricchio, D. J. (1993). Bone microstructure of the Upper Cretaceous theropod dinosaur Troodon formosus. Journal of Vertebrate Paleontology, 13(1), 99–104.

19 HOW DO WE KNOW BIRDS ARE DINOSAURS?

19

THE PHYLOGENY OF MANIRAPTORIFORMES AND THE ORIGIN OF FLIGHT

B

y now, you know that we use the concept of common ancestry, revealed through homologous characters in organisms, to classify organisms scientifically (Chapters 3 and 4). The more homologous features that are shared between organisms, the more recently in time they share an ancestor. By that definition, scientists who study dinosaurs classify birds as a group within Dinosauria, just as primates and canines represent two groups within Mammalia. But can the turkey you eat at Thanksgiving, the pigeon on the street, and the sparrow building a nest in your tree really be a dinosaur? Let’s look a little more closely at the evidence!

19.1 THE TERMINAL BRANCH: GROUPS WITHIN MANIRAPTORIFORMES After reading this section you should be able to… • Name the lineage of dinosaurs that is still alive today. • Describe the five characteristics that are diagnostic of Maniraptora. • Define and explain the importance of a pygostyle. • Draw a cladogram of Maniraptora, showing the branches leading to modern birds.

When we discussed the phylogenetic tree of Saurischia (Chapter 9), we ended with Coelurosauria, a derived group of theropods that includes both Tyrannosaurus rex and the lineage that gave rise to birds—Maniraptoriformes. Now, we will pick up where we left off, and work our way through the phylogeny of Maniraptoriformes. Figure 19.1A shows a basic cladogram of Tetanurae, in which you can see where spinosaurs (Megalosauria) and allosaurs (Allosauria) diverge from Coelurosauria, which itself splits into Tyrannosauroidea and Maniraptoriformes. Figure 19.1B shows an expanded cladogram of Maniraptoriformes, which includes the most recent common ancestor of Ornithomimus and modern birds (Aves), and all of its descendants.

IN THIS CHAPTER . . . 19.1 THE TERMINAL BRANCH: GROUPS WITHIN MANIRAPTORIFORMES 19.2 BIRDS OF A FEATHER: AVIALAE AND AVIAN CHARACTERISTICS 19.3 BUILT FOR FLIGHT: ADAPTATIONS FOR POWERED FLYING 19.4 THE SKY’S THE LIMIT: THE EVOLUTION OF FLIGHT 19.5 WHAT WE DON’T KNOW

470

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.1  (A) Cladogram of Tetanurae, showing the position of the group Maniraptoriformes (highlighted) within the clade. (B) Expanded cladogram of Maniraptoriformes.

Figure 19.2  Cladogram of Maniraptoriformes with the group Ornithomimosauria highlighted within the clade.

Figure 19.3  Skeleton (cast) of the ornithomimid Struthiomimus, or “ostrich mimic”. The head and feet are

very similar to living ostriches, although the arms of this specimen are much longer and more robust than those of ostriches. (Courtesy of M. Beauregard at the Royal Tyrell Museum, https://flic.kr/p/8HHUqG.)

19.1.1 Ornithomimosauria Ornithomimosauria means “bird mimic”, a name that arises from the many bird-like features the members within this group possess, even though they represent a very basal branch within Maniraptoriformes, and are thus not very closely related to modern birds (Figure 19.2). For example, although early ornithomimids had teeth, as did the majority of their theropod ancestors, derived members of the group were toothless, as are living birds—a convergent character between these two groups.

19.1  The Terminal Branch: Groups within Maniraptoriformes

471

Dinosaurs within Ornithomimosauria include Sinornithomimus (bird mimic from China) and Gallimimus (chicken mimic) (Figure 19.3). Gallimimus (galli = chicken, mimus = mimic) is the largest of the ornithomimids, and had a starring role in the original Jurassic Park movie (immortalized by the line, “They’re flocking this way!”). Like other derived ornithomimids, Gallimimus was toothless, but some exceptionally preserved specimens of Gallimimus show something really surprising. The bones at the front part of its jaws are marked with a rugose (ridged and bumpy) texture (Figure 19.4A) that is similar to the texture we see in modern animals that have keratinous structures—like beaks—covering them. The presence of this feature strongly supports the hypothesis that the jaws of this group of dinosaurs may have been covered with a keratinous beak, like those of living birds. Additionally, in some living birds, the cutting edges of their bill (called tomia) have developed ridges, bristles, or sawtooth-like serrations that help them process their food (Figure 19.4C). With such modifications to their tomia, birds without teeth can hold slippery prey better, grind grains for easier digesting, or strain small water insects to use as food. However, unlike teeth, these structures are not made of enamel, but keratin, the same protein that comprises the beak itself. It has been proposed that, within birds, beaks evolved to replace teeth as a selective adaptation for flight, because keratinous beaks are much lighter than a mouthful of enameled teeth. It was surprising, then, when Gallimimus was recovered with similar modifications (Figure 19.4B)!

19.1.2 Maniraptora Even with all their very bird-like traits, the dinosaurs within Ornithomimosauria are not on the lineage that directly leads to birds, but are a side branch that would, like the vast majority of dinosaurs, leave no descendants. The closest relatives of the ornithomimids, the manirapFigure 19.4  Comparison of a Gallimimus skull preserving originally soft tissues (A, B), compared with the keratinous, teeth-like structures on the tomia of a living bird (C). (A and B

courtesy of M. A. Norell et al., 2001, The beaks of ostrich dinosaurs. Nature, 412: 873–874; C courtesy of S. Friedt, https​:// co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=35​34278​3.)

472

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.5  Cladogram of Maniraptoriformes with the group Maniraptora highlighted within the clade.

torans (Figure 19.5), are the focus of the remaining history of the dinosaurs because members of this group are very much alive today! Maniraptorans are diagnosed by: • Elongated arms and hands: The arms and hands become increasingly long relative to leg length. In birds, this will eventually result in a wingspan much greater than the length of their legs. • An ossified sternum: The sternum consists of bony plates that show broadening and in some cases fusion, the beginnings of what is seen in the massive sternums of later birds. This increased surface area will (eventually) be adapted for the attachment of very large flight muscles (Figure 19.6). • A retroverted pubis: Ornithomimids, the closest relatives of the maniraptorans, have the ancestral saurischian condition of a pubis that points forward (forming a tripod pelvis). However, starting in Maniraptora, the pubis begins to retrovert, orienting posteriorly and becoming roughly parallel with the ischium, as in living birds (Figure 19.7). This is convergent with the condition observed in all of Ornithischia and is the reason that that group is confusingly

Figure 19.6  A well-preserved specimen of the dromaeosaurid Zhenyuanlong suni showing an expanded ossified sternum (arrow).

(Courtesy of J. Lü and S.L. Brusatte, 2015.)

19.1  The Terminal Branch: Groups within Maniraptoriformes

473

Figure 19.7  Skeleton of Deinonychus antirrhopus showing the retroverted pubis that is diagnostic for Maniraptora. This is convergent with the

morphology seen in ornithischian dinosaurs (see Chapter 8). (Courtesy of K. Tiffany, photographed at the Field Museum.)

called “bird-hipped” despite the fact that birds evolved from “lizard-hipped” dinosaurs. • A semi-lunate carpal: The semi-lunate (half-moon) carpal is a small bone present in the wrist of all living birds (Figure 19.8) that allows them to retract their wrist efficiently. This bone is structurally crucial in the flight stroke of a bird. However, it first appears long before birds, and is present within maniraptorans. If you remember the scene in the first Jurassic Park movie, where the raptors turn the doorknob to try to attack the children, this bone is what makes that movement possible. • Feathers: Although filamentous coverings are observed in other dinosaur lineages—and even in archosaurs outside of Dinosauria (i.e., pterosaurs), maniraptorans are thought to be the first organisms to possess “true” feathers. One of the most crucial pieces of evidence that supports the evolutionary relationship between birds and dinosaurs—namely that birds are dinosaurs—is the discovery of “true” (i.e., complex) feathers on dinosaurs. Feathers are the most complex epidermal structures in vertebrates (Figure 19.9). They are comprised of a long, stiff, and hollow central rod, or rachis, that gives rise to angled, branching structures called barbs. These barbs themselves give rise to structures called barbules, the ends of which can curl into hooklets. When these hooklets interact with barbules, they form a vane. If you have ever seen a bird preening, they are “combing” these parts of the feather back in place, like Velcro. It was long thought that such feathers were a feature totally unique to birds, and indeed, an early specimen of the first recognized bird, Archaeopteryx, had been identified as a compsognathid dinosaur until further preparation revealed the impression of feathers, allowing its placement within birds. Many of its other features, such as its long bony tail, teeth,

Figure 19.8  The semi-lunate carpal in the wrist of (A) a chicken and (B) a pelican. The semi-lunate carpal allows

birds to fold their wrist, and is crucial in the flight stroke of birds. However, semi-lunate carpals have been found in maniraptorans that did not fly, such as Velociraptor. (Courtesy of K. Tiffany.)

474

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.9  Diagram of the structure of a feather. Feathers are composed

of a hollow central rod called a rachis, from which barbs arise. Barbs give rise to barbules, which have tiny little hooklets that hook onto each other. (Adapted from U. Gille, https://commons.wikimedia.org/wiki/ File:Feather_scheme.png.)

and retention of “fingers”, are decidedly un-birdlike and closer to features observed in more basal maniraptorans. The hypothesis that birds are descended from (and therefore are) dinosaurs allowed scientists to predict that some dinosaurs within the lineage most closely related to birds should also display feathers—a prediction that became reality with the discovery of Sinosauropteryx in 1995. This small, hatchling dinosaur (Figure 19.10), discovered in China, was found with a filamentous body covering, supporting the hypothesis that some dinosaurs had elevated metabolic rates (see Chapter 18), and suggesting that the first feathers were much more simple than the complex, branched, and diversified feathers of today’s birds. Sinosauropteryx was followed by the discovery of many other non-avian dinosaurs with either feathers or filamentous (protofeather?) coverings, not only requiring biologists to re-evaluate what we consider a “bird”, but also to identify evolutionary pressures that led to the origin and diversification of feathers within this lineage. Filamentous structures related to feathers have now been found on many maniraptoran dinosaurs, and even some theropods more distantly related to birds than maniraptorans. Additionally, filamentous structures have been found in a few members of Ornithischia (e.g., Psittacosaurus),

Figure 19.10  Specimen of a hatchling Sinosauropteryx, showing, among other features, a filamentous covering along the midline of its back. This was the first non-avian dinosaur

described with feather-like integumentary structures. (Courtesy of Sam/Olai Ose/ Skjaervoy, https://flic.kr/p/3gT977.)

19.1  The Terminal Branch: Groups within Maniraptoriformes

475

and even pterosaurs. Do these represent an ancestral trait distributed across Avemetatarsalia? Did they eventually give rise to complex feathers? Or do they represent convergence, with independent origins in pterosaurs, ornithischian dinosaurs, and saurischian dinosaurs? How would you test this? We know that feathers originated in the lineage of dinosaurs most closely related to birds for “reasons” other than flight; this is strongly supported because we see feathers in many animals that clearly did not fly. So far, what we do know is that complex feathers with fully developed rachis, barbs, etc., are limited to Maniraptora. If so many theropods have either feathers or filamentous coverings, why did it take us so long to discover it? Specimens bearing feathers or feather-like structures have, so far, come from specific depositional environments. Usually, feather preservation requires very fine-grained sediments, like mud or clay, and is favored by environments low in oxygen such as stagnant lake bottoms. If a feathered dinosaur did not live (or die) in an environment that specifically favors the preservation of feathers, even if we are lucky enough to find its bones, we may never know that feathers were once present. Additionally, fragile remnants of feathers can accidentally be scraped away during excavation or preparation of a fossil if one doesn’t know to look for them. However, there might be bony correlates indicating the presence of feathers, even when the feathers themselves don’t preserve. In most birds that engage in active flight, tiny ligaments attach the root of the feather to the bone. These ligaments in turn are attached to tiny muscles, providing a way for the animal to manipulate their feathers to respond to the stresses of flight (Figure 19.11A). Like all other muscles that act upon bone, these leave small bumps or scars called quill knobs on

Figure 19.11  (A) Quill knobs on the ulna of an extant pelican. These raised knobs provide surface area for the ligament attachment of the muscles that move the flight feathers. (B, C, D) Quill knobs on the ulnae of several fossil (non-avian) maniraptorans: (B) Dakotaraptor, (C) Velociraptor, and (D) Concavenator. (A courtesy of K.

Tiffany; B–D courtesy of R. A. DePalma et al., 2015.)

476

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

the ulna. These very same marks, evenly spaced, have been identified on the ulna of a velociraptor, and on a few other non-flying dinosaurs as well (Figure 19.11B).

19.1.3 Alvarezsauria After ornithomimids diverged from maniraptorans, the next group to branch from this lineage are a group of little dinosaurs called Alvarezsauria (Figure 19.12). Members of this group have been recovered from Argentina, parts of Asia, and in North America. One notable member of Alvarezsauria is a strange little dinosaur called Mononykus olecrans (Figure 19.13). This species is named for its unusual forelimb anatomy. Its rather short arms end in hands comprised of a single, robust digit (mono = one, nykus = claw). A specimen of Shuvuuia deserti, another alvarezsaur from Mongolia, was preserved in articulation, perfectly laid out in the desert sands. But when the American Museum crew began to prepare this little specimen, they noticed the presence of filaments in its cervical (neck) region. Detailed analyses using many different methods revealed that these filaments were hollow, and maintained small regions of the same keratin protein that makes up modern feathers—a specific protein called β-keratin (or corneous β-protein) that mammals do not possess!

Figure 19.12  Cladogram of Maniraptoriformes with the group Alvarezsauria highlighted within the clade.

Figure 19.13  Skeletal mount (cast) of Mononykus olecranus, an alvarezsaurid found in Late Cretaceous sediments from Mongolia.

It is characterized by an enormous claw on its tiny arms. (Courtesy of T. Cowart, photographed at the American Museum of Natural History, https​://co​mmons​.wiki​media​ .org/​w/ind​ex.ph​p?cur​id=74​84985​.)

19.1  The Terminal Branch: Groups within Maniraptoriformes

477

19.1.4 Therizinosauria The next group to branch off on our path to birds is Therizinosauria (Figure 19.14). Although bigger than alvarezaurians, many members of this group are just as weird. The largest representative of this group, Therizinosaurus (Figure 19.15), had massive claws on their hands—up to 1 m in length (Figure 19.16)! If you’ve ever wondered what Edward Scissorhands would look like as a dinosaur, Therizinosaurus is it! Another surprising feature of this group is their diet; although they are theropods, and theropods are all ancestrally carnivorous, some have hypothesized that therizinosaurs may have been herbivorous, or perhaps omnivorous. Traits we observe in some therizinosaurs, including small, spoon-shaped teeth with coarse serrations that are inset from the jawline to form cheeks, and an expanded gut, are features associated with herbivory, and are convergent with some traits that we observe in

Figure 19.14  Cladogram of Maniraptoriformes with the group Therizinosauria highlighted within the clade.

Figure 19.15  Skeletal mount of Therizinosaurus, showing the massive claws for which it is known. (Courtesy

J. Lallensack, photographed at the Natural History Museum of Utah, Salt Lake City, UT, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=64​19008​4.)

478

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.16  Claws from the manus of Therizinosaurus. (Courtesy of

Ghedoghedo Aathal, photographed at the Dinosaur Museum in Zürich, Switzerland, https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=15​17904​3.)

ornithischians. If members of this group were herbivorous/omnivorous, its long hands with clawed fingers may have been useful in digging up leaves and branches and pushing them into its mouth.

19.1.5 Oviraptorosauria After the divergence of Therizinosauria, we are left with a clade called Pennaraptora, or “feather thief”, which includes the most recent common ancestor of oviraptors, extant birds, and all its descendants. The first group of interest that diverges as we move toward birds is Oviraptorosauria (Figure 19.17), the group that contains the much-maligned, incorrectly named Oviraptor or “egg stealer” (Figure 19.18). Figure 19.17  Cladogram of Maniraptoriformes with the group Oviraptorosauria highlighted within the clade.

Figure 19.18  Skull of Oviraptor philoceratops (the “egg-stealing lover of ceratopsians”). This dinosaur’s name

(and much-maligned reputation) arose from a mistaken fossil identification. The eggs the first Oviraptor was accused of stealing were not protceratops eggs, they were its own eggs! (Courtesy of K. Tiffany.)

19.1  The Terminal Branch: Groups within Maniraptoriformes

479

Figure 19.19  Artist sketch comparing tail feather attachment in (A) living birds and (B) Archaeopteryx. Living

birds and at least some dinosaurs close to birds convergently evolved pygostyles (red arrow), or fused tail vertebrae that increased the surface area for feather insertions. Conversely, Archaeopteryx, while considered a bird, does not have a pygostyle. Instead, tail feathers are anchored to individual vertebrae. (Public domain, courtesy of Nordisk Familjebok, http://runeberg.org/nfba/0758.html.)

Throughout Maniraptoriformes, we see a general trend toward an ever-shortening tail, which in birds eventually becomes a short nubbin of fused tail vertebrate called a pygostyle (Figure 19.19A). Whereas the ancestral theropod state is a long, bony tail with many vertebrae (Figure 19.19B), the pygostyle in birds acts as an expanded area to anchor the tail feathers, which provide control during takeoff and landing. The development of the pygostyle is, therefore, a crucial adaptation for flight, and thus such fusion in the distal tail was once thought to be uniquely avian. However, in at least one member of Oviraptorosauria, Nomingia gobiensis, the last five vertebrae of the tail have fused (Figure 19.20). But do these fused vertebrae represent a pygostyle, or a convergent trait? This question brings us back to Archaeopteryx, which retains the long bony tail of its ancestors (e.g., Figure 19.19B). As opposed to a fan-like feathered tail of living birds, the tail feathers of Archaeopteryx are anchored along the individual vertebrae. Could this “first bird” fly without a pygostyle? If so, it was probably was not as efficient a flier as modern birds. Moreover, the lack of a pygostyle in Archaeopteryx, which is much more closely related to birds than Nomingia, supports the hypothesis that these fused tail vertebrae arose convergently in Oviraptorosauria and living birds. Thus, what we see in Nomingia is likely not a “true” pygostyle—though much like feathers, the presence of this feature in an obviously flightless dinosaur requires paleontologists to look beyond flight as a selective pressure for its evolutionary development.

Figure 19.20  This oviraptor specimen (Nomingia gobiensis) shows the beginning of the fusion of the distal tail vertebrae. (A) Shows the distal part of the tail, including the fused vertebrae, and (B) Shows all of the preserved caudal series (caudal vertebrae 2 through 24). In

maniraptorans more closely related to birds, this trend continues, resulting in the pygostyles of living birds. These fused vertebrae provide a large surface area for attachment of tail feathers that aid in flight. Scale bar represents 10 cm. (Adapted from R. Barsbold et al., 2000.)

480

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.21  Cladogram of Maniraptoriformes with the group Paraves highlighted within the clade.

19.1.6 Paraves After the divergence of Oviraptorosauria, our simplified phylogeny is left with a clade called Paraves, which originated in the Jurassic, and which includes the major groups Troodontidae, Dromaeosauridae, and extinct and living birds (Avialae) (Figure 19.21). The relationships among these groups is somewhat unclear. For decades, it was thought that Troodontidae and Dromaeosauridae were sister groups, more closely related to each other than to birds, together forming a clade called Deinonychosauria. However, recent studies have hypothesized that this may not be the case, and that troodontids may be more closely related to birds than they are to dromaeosaurs. Here, we use the earlier grouping of these two clades into Deinonychosauria, but be advised that like with all dinosaur systematics, hypotheses can change with new discoveries!

19.1.7 Deinonychosauria Deinonychosauria is comprised of two groups: Dromaeosauridae, which includes the informally dubbed “raptors” of Jurassic Park fame such as Velociraptor, and Troodontidae (Figure 19.22). These two groups are united by the possession of a highly modified, large “sickle” claw on their foot. In many species, this claw was mounted on a toe with hyperextensible joints—meaning they could retract the claw past a 90° angle relative to the rest of the foot, holding it off the ground (Figure 19.23) so that it didn’t interfere with walking. Although this claw was present in both dromaeosaurids and troodontids, it is more pronounced in dromaeosaurids, and it is thought that some troodontids could not hold the toe very far off the ground, which would limit its size. Dromaeosaurids, or “running lizards” (dromeus = run, sauros = lizard), were a group of carnivorous dinosaurs that we now know were mostly Figure 19.22  (A) Cladogram of Maniraptoriformes with the group Deinonychosauria highlighted within the clade. (B) Inset cladogram of Deinonychosauria, showing the two sister groups that comprise it: Dromaeosauridae and Troodontidae.

19.1  The Terminal Branch: Groups within Maniraptoriformes

481

Figure 19.23  The right foot of Deinonychus antirrhopus, a dromaeosaurid from the Cretaceous period. These medium-sized (~11 ft, or 3.5

m) predators are hypothesized to have been fast runners with excellent vision. (Courtesy of K. Tiffany, photographed at the Field Museum.)

(possibly all) feathered, at least on their legs and feet—despite the outdated appearance of them that persists in Hollywood to this day. Modern birds, of course, have lost these leg feathers, but the genes for this trait still exist, and with some manipulation, feathers can still be induced to form on the legs and feet of living birds. Besides feathers, another interesting feature dromaeosaurs possessed were long tails that were reinforced with ossified tendons (Figure 19.24), a trait convergent with the ossified tendons observed in members of Ornithischia. It is hypothesized that these rod-like bony tendons stiffened their tails, stabilizing them for rapid changes in direction and movement while running, allowing the tail to act as an efficient counterbalance. Troodontids were first diagnosed primarily by their teeth; the dentition of many members of this group bears a serrated edge in which the individual serrations are extremely large relative to the overall size of the tooth, a unique trait within Theropoda (Figure 19.25). However, more recent discoveries of articulated specimens, as well as eggs and juveniles, have greatly expanded our understanding of this group. Among all dinosaurs, troodontids had the largest brain size (in proportion to their overall body size). This has led to hypotheses that they were capable of complex behaviors and finely tuned senses, particularly vision. Similar to the more basal oviraptors, some well-pre-

Figure 19.24  In dromaeosaurids, the vertebrae of the tail are held in tight alignment by surrounding ossified tendons, stiffening the tail and aiding in balance. (Courtesy of K. Tiffany,

photographed at the Field Museum.)

482

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.25  Troodontid teeth showing the greatly enlarged serrations that are typical in many members of this group. An American

dime is shown for scale. (Courtesy of W. Kaveney and The Children’s Museum of Indianapolis, https://commons.wikimedia. org/wiki/File:The_​Child​rens_​Museu​m_of_​ India​napol​is_-_​Trood​on_te​eth.j​pg.)

Figure 19.26  A small theropod dinosaur, Mei Long, with its head tucked under its arm in a bird-like position. Its name means “sleeping dragon”. (B) Shows a diagram of the position of the bones in the specimen, with the skull highlighted. (Courtesy of

X. Xu and M.A. Norell, 2004.)

served troodontid specimens have been preserved in a brooding position, and others have been discovered that display additional bird-like behaviors. One spectacular specimen shows a small troodontid with its head tucked under its arm (Figure 19.26), a roosting behavior also observed in sleeping birds!

19.2 BIRDS OF A FEATHER: AVIALAE AND AVIAN CHARACTERISTICS After reading this section you should be able to… • Describe two diagnostic characteristics of birds.

We come to the last node of our basic Maniraptoriformes tree, Avialae (Figure 19.27), which encompasses all living and extinct birds. Our diagnoses of Avialae has changed somewhat, because many discoveries in the last few decades have changed how we classify members of this group, and have clarified our understanding of the evolutionary relationships within Avialae—as well as Maniraptora, and even more broadly in Theropoda. For many years, the following features were thought to be autapomorphies of Aves: • Toothlessness† • Pneumatic bones* • Pygostyle† • Furcula* • Enlarged sternum • Shortened tail† • Horizontal scapula and lateral glenoid*

19.2  Birds of a Feather: Avialae and Avian Characteristics

• Elongate coracoids* • Elongate arms and hands* • Retroverted pubis* • Feathers* The features listed with an asterisk (*) are now known to be basal features (plesiomorphies) among extant birds—that first appeared earlier in their evolutionary lineage. The features listed with a cross (†) are also found to have convergently evolved in non-avian dinosaur species closely related to birds. Thus, the more we learn about the evolutionary history of this terminal branch of Dinosauria, the more we have to adjust our thinking about what we consider a “bird”. What, then, are the defining features (autapomorphies) for birds?

19.2.1 Avialae Avialae (Figure 19.27B) is defined as “the most recent common ancestor of Archaeopteryx and Passer domesticus (house sparrow) and all its descendants”. Essentially, this clade encompasses the earliest recognized bird, the most derived living bird, and all birds in between. Avialans emerged in the Late Jurassic, and they have been found (and still exist) on all continents. The oldest fossil organism that we define as a bird is Archaeopteryx (Archaeo = old; pteryx =wing), known from the Jurassic, about 150 million years ago. Archaeopteryx is known from about ten specimens, in various states of completeness and preservation. As mentioned earlier, when first found, Archaeopteryx was misidentified as a small, basal compsognathid, many of which had been found in the same quarry. Thus, Archaeopteryx languished in a museum drawer for years, until further preparation of the specimen revealed feathers (Figure 19.28)! These feathers were perfectly aligned, as complex as the feathers of living birds, and they originated from the ulna just as in modern birds. The problem was, Archaeopteryx, for all its strikingly bird-like features, also has many features that aren’t bird-like at all, including the presence of teeth and a long bony tail. If many of the features traditionally considered “bird-like” are found in very basal maniraptorans, then what makes a bird (i.e., a member of Avialae)? The answer to this question, like many questions about dinosaur phylogeny, is still in flux, and will no doubt change somewhat as we discover new specimens within this lineage. However, one feature that appears to be autapomorphic for Avialae is arm length equal to or longer than leg length (Figure 19.29). Already within Maniraptora we start to

Figure 19.27:  (A) Cladogram of Maniraptoriformes, showing the position of the group Avialae (highlighted) within the clade. (B)

Expanded cladogram of Avialae.

483

484

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.28  Skeleton of Archaeopteryx lithographica, complete with preserved feathers, recovered from Jurassic sediments near Solnhofen, Germany. Because it

retains many ancestral features compared with modern birds (e.g., teeth, a long bony tail) there is still much debate whether to consider Archaeopteryx a bird. (Courtesy of W. Sauber, photographed at the Natural History Museum Vienna, Austria, https:// commons.wikimedia.org/wiki/File:NHM_​ -_Arc​haeop​teryx​_lith​ograp​hica_​Fossi​l.jpg​.)

Figure 19.29  comparison of the foreand hindlimb proportions in theropod dinosaurs, including (A) Allosaurus, (B) Tyrannosaurus, (C) Struthiomimus (an ornithomimosaur), (D) Deinonychus, and (E) Archaeopteryx, the first recognized bird. (Adapted from

K. M. Middleton and S. M. Gatesy, 2000.)

see an elongation of arm length, and this trend continues, until in Avialans, the arms are (in some cases) much longer than the legs. Another bird-defining feature is anisodactyly (an = not; iso = same; dactyl = digit). This is a condition in which, of four toes, one toe (the first) faces a different direction than the other three (Figure 19.30). In perching birds, this is taken to the extreme—the first toe is oriented fully backward, in opposition to the other three, allowing them to grasp branches securely. However, in some lineages of birds that do not perch, this trait has been modified; birds like ostriches have lost two of their toes, so their feet are limited to only two toes, both forward-facing. Avialae represents those theropod dinosaurs more closely related to living birds than to Deinonychus. But, the group Avialae includes more than just birds (Aves). Within Avialae we see evidence of continued evolutionary advancements that are shared with Aves, but the earliest birds differed in many significant ways from living birds. So “birds”, when the fossil record is included, contain many groups that can be differentiated by evolutionary landmarks, but which, for the most part, do not have direct descendants today. Many dinosaurs that appear very bird-like exist within this branch but are not considered “birds” quite yet. These include the Jurassic Anchiornis and many other spectacular Chinese feathered specimens.

19.2  Birds of a Feather: Avialae and Avian Characteristics

485

Figure 19.30  Anisodactyly in the feet of both (A) Archaeopteryx and (B) a living tui bird (Prosthemadera novaeseelandiae). Anisodactyly is a

condition in which one or more toes is rotated to a different plane of grasping that the others, which greatly aided birds in perching. (A courtesy of E. Willoughby, https://commons.wikimedia.org/wiki/ File:Berl​in_Ar​chaeo​ptery​x_-_d​etail​_of_f​eet.j​ pg; B courtesy of T. Willis, https​://co​mmons​ .wiki​media​.org/​wiki/​Bird_​feet#​/media/ File:Tui_foot_02.jpg.)

19.2.2 Ornithothoraces Nested within Avialae is a more derived clade, called Ornithothoraces (ornitho = bird, thoraces = thorax) (Figure 19.31). This group includes birds united in specific adaptations to their thorax, including a greatly enlarged sternum that possesses a keel or ridge in the center, and modifications to their shoulder girdle. Ornithothoraces include two important groups: Enantiornithes (opposite birds) and Euornithes (true birds). All living birds descended from the latter group. Almost all of the Enantiornithes that have been found still possess teeth—with a striking diversity of placement in their jaws—as well as clawed fingers on each wing. However, aside from these traits, if you saw an enantiornithine nesting in a tree outside your window (Figure 19.32), you probably wouldn’t look twice, as there wouldn’t be much to distinguish them from your friendly neighborhood robin. Enantiornithes and Euornithes (eu = “true”, ornithes = bird) are distinguished primarily by the anatomy of their shoulder joint. In Euornithes (which include modern birds), the joint is comprised of a knob-like boss on the shoulder blade (scapula) and a dish-shaped facet on the coracoid. In Enantiornithes, this condition is exactly reversed; the scapula has a dish-shaped facet and the coracoid has a knob-like boss, hence the name “opposite birds”. Additionally, parts of the ankle in “opposite” birds fuse in a reverse manner to that of living birds.

Figure 19.31  Cladogram of Avialae with the group Ornithothoraces highlighted within the clade.

486

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.32  (A) Well-preserved skeleton of Zhouornis hani, an enantiornithine from China. (B) Flesh reconstruction of the enantiornithine Iberomesornis. (A courtesy of Y. Zhang et

al., 2014, https://doi.org/10.7717/peerj.407/ fig-3; B courtesy of J.-M. B. Álvarez, photographed at the National Museum of Natural Sciences in Madrid, Spain, https​:// co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=19​32499​.)

There are additional differences between Enantiornithes and Euornithes that aren’t so obvious from outward morphology. In particular, the microstructure of enantiornithine birds reveals that these birds grew much more slowly than modern birds—even slower than some dinosaurs! It took them several years to reach sexual maturity, whereas all modern birds (except the very basal, large paleognaths) reach sexual maturity within a year. This seems to indicate a very different metabolism than living birds. This is significant because during the Mesozoic, Enantiornithes were far more successful than their living counterparts! They were more widespread and far more diverse, while Euornithes, from all indications, lived in their shadow.

19.2.3 Ornithurae Continuing our journey toward extant birds, within Euornithes is a more exclusive clade, Ornithurae (ornith = bird, oura = tail) (Figure 19.33). The birds of this group are characterized by a shortened tail (less than the length of the femur) where the vertebrae at the end are fused to form a true pygostyle. Basal birds within this group, such as the Cretaceous Hesperornis (a large diving bird) (Figure 19.34) and Ichthyornis (a seabird) still possessed teeth, but later forms all lack them, and some may have possessed keratinous beaks instead. It has been proposed that the first beak was a small, keratin-covered region on the tip of the premaxilla and predentary, and that it coexisted with teeth in Ichthyornis. However, to date, the evidence to support this hypothesis is inconclusive.

Figure 19.33  Cladogram of Avialae with the group Ornithurae highlighted within the clade.

19.2  Birds of a Feather: Avialae and Avian Characteristics

487

Figure 19.34  Skeletal reconstruction of the diving bird Hesperornis.

(Courtesy of T. Jorstad and the Smithsonian Institution.)

19.2.4 Aves At last we arrive at Aves, a group that encompasses all modern birds (Figure 19.35). Although, by this point, you should well know that phylogenetic definitions can change over time, one widely accepted definition for the clade Aves is “the last common ancestor of all living birds, and all its descendants”. Thus, any bird you’ve seen outside your window is a member of Aves. Aves is also referred to as Neornithes (neo = new, ornith = bird). Within Aves, the most basal group of living birds is a group called Palaeognathae (palaeo = ancient, gnath = jaw), a group primarily differentiated from the more derived Neognathae (neo = new, gnath = jaw) by the anatomy of their bony secondary palates (i.e., the roof of their mouths). As a group, palaeognathans are (mostly) secondarily flightless—meaning that while their ancestors could fly, they have lost that ability. Some palaeognathans with which you are probably familiar include ostriches, emus, kiwis, and cassowaries (Figure 19.36). The more derived Neognathae is comprised of two groups (Figure 19.37): Galloanserae and Neoaves. Galloanserae, the more basal of the two groups, includes Galliformes, which are landfowl/gamefowl such as chicken, turkey, pheasants, and partridges (Figure 19.38A), and Anseriformes, which are waterfowl such as ducks, geese, and swans (Figure 19.38B). If you eat a bird, it is most likely (but not always) a member of Galloanserae. All other, more derived birds diverge from neognathans into Neoaves, a group which contains ~95% of the diversity

Figure 19.35  Cladogram of Avialae, with the group Aves highlighted within the clade. Aves is a group that

exclusively encompasses modern birds.

488

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.36  (A) Flesh and (B) skeleton of an ostrich (Struthio camelus), an extant paleognath.

(A courtesy of A. Tschentscher, https:// commons.wikimedia.org/wiki/File:Ostrich_ Left_2019-07-24.jpg; B courtesy of Wagner Souza e Silva and Museum of Veterinary Anatomy FMVZ USP, https://commons. wikimedia.org/wiki/File:Avestruz_alta.jpg.)

Figure 19.37  Cladogram of Aves showing the relationship between Palaeognathae and groups within Neognathae.

Figure 19.38  (A) A chicken, an example of a living galliform. (B) A duck, an example of a living anseriform. (A courtesy of T. Lucas,

https://commons.wikimedia.org/wiki/File:A_ Very_Fancy_Chicken_(206902057).jpeg; B courtesy of K. Tiffany.)

within Aves, and includes the highly derived members such as parrots, hawks, vultures, owls, penguins, flamingos, and many, many other species. The clade Aves is much more diverse and successful than our own clade of mammals, because Aves contains almost twice the number of species as are in Mammalia! Dinosaurs, then, are doing pretty well today!

19.3  Built for Flight: Adaptations for Powered Flying

489

19.3 BUILT FOR FLIGHT: ADAPTATIONS FOR POWERED FLYING After reading this section you should be able to… • Describe the difference between powered flight and gliding. • Name the four animal groups that have independently evolved flight. • Discuss the benefits of powered flight.

An important part of the success and diversification of birds is, of course, their ability to fly. But what counts as “flying”? When we discuss flight as a behavior, we’re referring to powered flight, which is very different from gliding and has different biomechanical constraints. Powered flight has two required components: (1) The ability to get off the ground and into the air (2) The ability to stay there Both of these are tall orders, and require an enormous input of metabolic energy. Getting off the ground requires the musculature, skeletal adaptations, and power to generate enough upward force (or lift) to overcome the downward pull of gravity, and enough forward force (or thrust) to overcome the frictional force exerted by the air itself (or drag) (Figure 19.39). Staying in the air requires the muscle power to continuously maintain lift and thrust for the duration of the flight. The biomechanical and physiological demands of the actual launch from the ground are very different from that required to maintain flight in-air, and as we shall see, they are important considerations in deciphering how flight may have evolved in the bird lineage. Conversely, gliding is a passive process. It relies on external forces to provide lift, and does not require thrust. In powered flight, the organism’s muscles generate the forces required to attain upward lift and forward thrust (Figure 19.40). Typically, terrestrial animals that glide climb trees or make their way up to other high places and jump, employing expanded surfaces of skin (usually) like an airfoil to generate lift as they fall.

Figure 19.39  Diagram of the forces at work during powered flight. The flier

must generate enough forward thrust and upward lift to overcome the downward pull of gravity and the friction of drag. (Courtesy of K. Tiffany.)

490

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.40  Diagram of the forces at work during gliding. Gliders typically

use expanded skin surfaces as an airfoil to generate enough lift jumping from high places to overcome the downward force of gravity. However, gliders don’t generate forward thrust (see Figure 19. 38), so the frictional force of drag eventually causes them to lose the speed needed to maintain lift, and they fall to the ground. (Courtesy of M. Hays, https://commons.wikimedia. org/wiki/File:Jill_Flying_1.jpg.)

However, because these animals can’t generate thrust, the drag against their bodies eventually causes them to lose speed, and so they cannot maintain the lift that keeps them in the air, and they fall to the ground. This is why no hang-glider, paper airplane, or Frisbee can stay in the air as long as a sparrow can. As a passive process, the energy input for gliding is only what it takes to climb to a high point. Powered flight, on the other hand, requires a massive amount of metabolic energy, and this energy requirement, in turn, drives unique adaptations in the metabolism, physiology, and certainly, the morphology of fliers. Although the capability for true, powered flight is rather rare in vertebrates, it is not unique to birds. Flight evolved four times within animals (three of those times within Vertebrata), and in all organisms that have evolved this ability, the generation of forces to provide lift and thrust is accomplished by flapping wings. Despite this commonality, flight in each of these groups had an independent origin, and is therefore convergent. In fact, most of these groups are not even closely related to one another. Let’s take a look at where this behavior has cropped up in the phylogenetic tree of animals: Flight evolved, (Figure 19.41):

independently,

in

four

groups

within

Animalia

• Insecta (insects): As a subgroup of arthropods, insects include most familiar “bugs” and as a group, have members that exhibit incredible diversity, from commonly observed bees and flies to the rather intimidating flying praying mantis (Figure 19.42). All of these, however, are dwarfed by the flying insects of the Carboniferous. In

Figure 19.41  Cladogram of Animalia.

Stars mark the four groups in which powered flight has evolved.

19.3  Built for Flight: Adaptations for Powered Flying

491

Figure 19.42  Eastern Black Swallowtail butterfly (Papilio polyxenes). Insecta was the first group

of animals to evolve powered flight, and it remains an incredibly diverse group of fliers. (Courtesy of K. Tiffany.)

this era, insects flourished and tested the limits of powered flight in invertebrates, the first organisms to take to the air. • Pterosauria (pterosaurs): As discussed in Chapter 10, these archosaurian “cousins” to dinosaurs were extremely well-suited for flight. • Dinosauria (birds): Birds represent the fliers within the dinosaurian lineage. Although both pterosaurs and birds are within the group Avemetatarsalia, it is important to note that they lacked a common ancestor with the ability to fly, and thus evolved this trait convergently. • Mammalia (Bats): Bats are the only mammals to have achieved powered flight (Figure 19.43). Other mammals, such as so-called “flying squirrels” are actually gliders, not fliers! Given that flight is metabolically extremely expensive, why would an organism invest so much in this behavior? As with virtually all other evolutionary novelties we have studied, it comes with a trade-off. In exchange for being the most energy-expensive behavior a vertebrate can undertake, it also provides some great advantages. Flight has advantages for the following behaviors: • Escaping predators: The ability to launch into the air and out of reach of earth-bound predators gives flying animals an advantage in survival. Figure 19.43  Mexican long-tongued bat (Choeronycteris mexicana) in flight. Bats are the only mammals to have

attained fully powered flight. (Courtesy of US Fish and Wildlife Service.)

492

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

• Catching prey: On the other hand, the ability to attack from the air gives a great advantage to predators targeting their prey from above. • Traveling: Flight allows animals to cover more territory in less time, and do so more directly and with less physical obstacles, thus greatly expanding their range over earth-bound competitors. We use the expression “as the crow flies” to describe the most direct route to a location (which is usually not accessible by car or by foot); this takes on new evolutionary meaning in this context. This ability to efficiently cover more ground allows flying organisms to migrate to areas where food is more plentiful or the weather is more tolerable, making them less vulnerable to local environmental changes. • Accessing food sources: Flying allows animals to utilize new sources of food inaccessible by ground travel (such as fruit or seeds in trees or fish in open water), which in turn reduces competition. • Using their legs: Although birds do not have “hands” as such, their ability to take to the air frees their feet for use as weapons in food capture or manipulation or grasping/perching. Although considerable, are these advantages significant enough to offset the incredible expense of powered flight? This energy-intensive flying lifestyle drives some very specialized skeletal and physiological adaptations in vertebrates. Below, we discuss some of the features observed in birds that have been adapted to this novel lifestyle, and which include some highly adapted, particularly unique morphologies.

19.3.1 Wings The forelimbs of birds are highly modified to form the structure of their wings. As mentioned above, they are greatly elongated relative to the length of their hindlimbs. Additionally, modern birds have reduced their number of digits and fused various bones in their manus; for example, their metacarpals and a distal carpal are fused into a single carpometacarpus. This results in stronger compound bones with fewer joints, which serve to stabilize the wing during flight (Figure 19.44) and also reduces drag on the forelimb.

19.3.2 A Stabilized Skeleton In addition to the fusion observed in the wing, the skeletons of living birds show bony fusion in various elements. As we saw in Chapter 13, fusion and/or loss of bony elements contributes to stability, as the less

Figure 19.44  Diagram of the bones in a bird forearm (wing). In the manus,

multiple bones are either lost or fused together, resulting in a reduced number of bones. This provides stability to the wing during flight. (Public domain.)

19.3  Built for Flight: Adaptations for Powered Flying

493

Figure 19.45  The ribcage of a pelican (Pelicanus onocrotalus). Arrows indicate

the uncinate processes, which stabilize and stiffen the ribcage. (Courtesy of K. Tiffany.)

individual elements a structure or joint has, the fewer possibilities there are for these elements to become twisted, dislocated, or sprained. For example, while many animals have a sacrum—fused sacral vertebrae to which the pelvic girdle is anchored--members of Aves as well as some more basal birds incorporate more vertebrae from the thoracic (back) and caudal (tail) regions into the fusion, forming a specialized synsacrum. Further, although bird bones are light in weight, their bone tissue is also extremely dense—more so than other vertebrates. As bone density increases, so does its stiffness and strength. Another important feature of the avian skeleton that greatly aids in flight is the presence of small bony projections on their ribs, called uncinate processes (Figure 19.45). These bony processes from the ribs overlap to increase the structural stability and rigidity of the chest, and play a small role in muscle attachment. The additional stability these processes confer to the ribcage makes respiration more efficient. These small projections are also found in some other, non-avian dinosaur fossils, and similar processes are found in some living crocodiles, though these are made of cartilage and not bony. Interestingly, uncincate processes are not observed in Archaeopteryx, another feature that calls into question the ability of this “first bird” to actively fly. However, if they were made of cartilage as in some crocodiles, the likelihood of their preservation is low. These many fusions and adaptations make birds extremely efficient fliers, but the stability of their skeleton comes at the cost of reduced flexibility.

19.3.3 Feathers As discussed above, feathers are complex, branching structures (Figure 19.8), and the Velcro-like interactions between the hooklets and barbules that form the vane of the feather create an excellent airfoil for flight. Feathers are comprised of the protein keratin, but feather keratin is very different from the keratin that makes up the hair, skin, or nails of mammals. Feather keratin is stiff, yet flexible, and very strong. In addition, the hollow rachises of feathers contribute to weight reduction and efficient insulation. Although the presence of feathers on animals that certainly weren’t flying indicates that feathers did not originally develop under selective pressures of flight, they were certainly secondarily adapted for this locomotor mode.

19.3.4 Powerful Flight Muscles Because birds use muscle power to generate lift, they have very large and powerful pectoral and shoulder muscles to flap their wings. The sternum, already showing expanded bony plates within Maniraptora, becomes huge in modern birds (Figure 19.46) and even develops a sharp

494

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.46  The expanded sternum of a Velociraptor mongoliensis (A), compared with the keeled and even more expanded sternum of an extant Pondicherry vulture (Sarcogyps calvus) (B). The greatly expanded sternum

preceded flight and is a synapomorphy within Maniraptora. (A courtesy of B. Townsend, photographed at the Wyoming Dinosaur Center, https://commons. wikimedia.org/wiki/File:Velo​cirap​tor_W​ yomin​g_Din​osaur​_Cent​er.jp​g; B courtesy of K. Tiffany, taken at the Field Museum.)

ridge (or keel) in the center. This expansion of bone provides more space for muscles to insert, which allows the muscles to enlarge as well (this results in your favorite turkey breast!), and thus produce more power. However, they also need to maintain a relatively lightweight body, so the balance between strength, muscle mass, and importantly, the position of those muscles is key. A single flap of a wing during flight includes both an upstroke and a downstroke. To visualize this, extend your arms out to your side, bring them forward to clap your hands (downstroke), and then swing them toward your back as far as you can (upstroke). As a human, the muscles that bring your arms together in front of you are located on your chest (e.g., the pectoralis), and the muscles that pull your arms toward your back are located on your back, or the back of your shoulders (e.g., deltoids, triceps). Because the only thing any muscle can do is contract— only pull, never push—this placement makes sense; muscles on your chest pull your arms forward when they contract, muscles on your back/ shoulders pull them back. When you look at a bird, however, you can see that although they have enlarged chests, they have very little muscle mass on their backs to pull up their wings (Figure 19.47), a movement critical to flight. How is this possible? Birds have evolved a unique pulley system in their shoulders, in which the bodies of both the muscle to pull their wings down (the pectoralis), and the muscle that pulls their wings up (the supracoracoideus), are located on their chests (Figure 19.48). In fact, if you’ve ever eaten a chicken breast, you’ve eaten both of these muscles. Instead of being placed on the back, the majority of the muscle mass (or body) of the supracoracoideus (supra = above, coracoideus = coracoid) is on the chest, where it is anchored to the sternum. A tendon arises from this muscle body, looping up over the coracoid and inserting on to the top of the humerus. It operates similar to a rope thrown over a sturdy tree branch and attached to load. Just as pulling down on the rope drags it over the branch and lifts the load into the air, contracting the supracoracoideus pulls

Figure 19.47  Despite the need for strong muscles to contract and pull their wings up, birds have very little muscle mass on their back (arrow).

How is this possible? (Courtesy of K. Tiffany.)

19.3  Built for Flight: Adaptations for Powered Flying

495

Figure 19.48  Diagram depicting the position of the flight muscles in birds.

Both the muscles that pull the wing up (the supracoracoideus) and the muscles that pull the wing down (the pectoralis) are located on the chest, with virtually no muscle mass on the back. This redistribution of muscle mass is an adaptation for flight. (Courtesy of L. Shyamal, https://commons.wikimedia. org/wiki/File:Wing_Muscles,_color.svg.)

the muscle down toward the chest, dragging it over the coracoid and lifting the humerus up. And just like our simple rope-branch pulley, the pulley-like musculature of the avian shoulder expends much less energy to move the wing than we expend to lift weights or bench press. It also allows the bulk of the muscle to be oriented in an aerodynamic-friendly manner, where it will not obstruct the airflow necessary to maintain lift. It is a true engineering marvel! Intriguingly, Archaeopteryx lacked any bony evidence for this complex, derived state. It is hard to picture a bird being able to fly without this highly adapted shoulder, although most scientists agree that Archaeopteryx was capable of some kind of powered flight. Just how they attained this is still unresolved.

19.3.5 An Extremely Efficient Respiratory System Trying breathing in, then breathing out once, and pay attention to how the air in your body seems to move. When most vertebrates breathe, the air flows in as the lungs inflate, oxygen is exchanged for carbon dioxide, then air flows out as the lungs deflate. This creates a respiration cycle in which air is flowing over lung tissues first one way, then the other (bidirectionally). Since your lungs never fully deflate (no matter how hard or long you try to breath out), a certain volume of deoxygenated (“stale”) air stays in your lungs, and mixes with the new, fresh air when you breathe in. In fact, humans only exchange about 15% of the air in their lungs when they breathe. While this is sufficient for the oxygen exchange required for our metabolic needs, from an engineering standpoint, it’s hardly efficient! Conversely, in birds, the process of respiration is totally different. Rather than having inflatable lungs, birds have rigid lungs and a series of air sacs that inflate and deflate to move the air around the respiratory system in a unidirectional pattern (Figure 19.49). During inhalation, the oxygenated

Figure 19.49  A schematic drawing of the inhalation and exhalation cycles of respiration in living birds. Birds

are unique among living vertebrates in that they lack a diaphragm and have rigid lungs. Air is moved through the lungs in an unidirectional air flow by numerous air sacs anterior and posterior to the lungs that work like bellows. (Adapted from L. Shyamal, public domain.)

496

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

air moves down the trachea and flows either through the lungs for oxygen exchange, or to inflate the posterior air sacs. Air moving across the lungs during inhalation, having expended its oxygen, then flows into the anterior air sacs, inflating them. During exhalation, the used air in the anterior air sacs flows out of the trachea, and the stored, still-fresh air in the posterior air sacs now flows across the lungs, exchanging oxygen. Thus, bird lungs are constantly exchanging oxygen, during both inhalation and exhalation. Further, the unidirectional nature of the air flow around the air sac system means that “fresh” and “stale” air are never mixing, thus providing continual access of air with the highest concentration of oxygen possible to the blood. Because oxygen is required to maintain both elevated metabolisms and long-term muscle power—these modified airways are an adaptation vital to avian flight. In addition to the adaptations of their lungs, a suite of adaptations to the avian heart also contribute to the efficiency of breathing in extant birds. Relative to their body size, avian hearts are larger than those of mammals, and they beat faster than other vertebrates.

19.3.6 A Lightweight Skeleton The heavier a body, the greater the force that must be generated to overcome gravity and achieve lift. In animals, that force is generated by muscle power, so more weight translates to a need for even greater muscle mass—which itself adds more weight! Thus, the simplest biological path to achieving the necessary body weight to muscle ratio is to reduce the weight of the rest of the body relative to similar-sized non-flying animals. In birds, a lightweight skeleton is one of the key features that contribute to weight reduction. If you’ve ever cracked open a limb bone of a chicken, you will find that it is very thin and hollow in cross-section (Figure 19.50). This is the result of a process called post-cranial skeletal pneumatization. Above, we discussed how birds have air sacs connected to their lungs that function like bellows to move air around their respiratory system. During embryonic development, out-pockets of these air sacs called diverticula invade developing bones to create a hollowed (pneumatic) skeleton. This process reduces the weight of the bone without compromising its structural integrity, which is crucial; flying puts the skeleton under extreme stress, so it is not enough that bones be light, they must also be sufficiently strong to withstand the forces of takeoff and landing. To add to fracture resistance, the thinnest sections of bird (and pterosaur) bones are also reinforced with internal bony struts (Figure 19.50). Although post-cranial skeletal pneumaticity is unique to birds among living animals, the origin of this trait is deeply rooted in the dinosaur tree. In fact, it is a feature that was convergently attained in Pterosauria

Figure 19.50  Cross-section through a bird femur, showing the very thin bony wall and a hollow interior filled with thin bony struts for added support. (Courtesy of E. Schroeter.)

19.3  Built for Flight: Adaptations for Powered Flying

and birds, and accounts for the lightweight skeleton that allowed efficient powered flight in both lineages (Figure 19.51). The excavation of bones by diverticula is recorded in dinosaur fossils and early birds because they leave behind bowl-shaped depressions ( fossae), entry holes ( foraminae), and internal bone tissue that looks a little like Swiss cheese. Differing degrees of pneumaticity are observed throughout Saurischia. Nearly all sauropods possess pneumatic vertebrae, and some display pneumaticity in other bones as well. This character is hypothesized to have lightened the weight of their incredibly long necks, and reduced the strength and muscular energy required to hold them upright (see chapter 9). This trend continues within theropods, which show even greater pneumaticity that extends to their limb elements—if we find a hollow leg bone in the field (Figure 19.52), we know it’s from a theropod!

497

Figure 19.51  Cladogram of Archosauria. Stars mark the lineages in

which post-cranial skeletal pneumaticity (PSP) is observed. Although PSP is present broadly throughout the groups Pterosauria and Saurischia, it is absent in all members of Ornithischia. Did similar respiratory systems that result in PSP develop twice through convergence, once in Pterosauria and once in Saurischia? Or did it evolve once in Avemetatarsalia, but only cause PSP in pterosaurs and saurischians?

Figure 19.52  This theropod bone, seen in cross-section in its entombing sediments, was found in Judith River sediments from the Mid-Late Cretaceous. (Courtesy of M. Schweitzer.)

498

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Interestingly, although we readily observe pneumaticity in all of Saurischia, to date, it has not been observed in any ornithischian (Figure 19.51). However, it is clearly present in pterosaurs. Was this a convergent feature between pterosaurs and saurischians? Or was it present in the common ancestor of these two groups, suggesting that pneumaticity—and the highly efficient respiratory system that produces it—was present in the ancestor of Avemetatarsalia (Figure 19.51), and was lost or modified in ornithischians?

19.4 THE SKY’S THE LIMIT: THE EVOLUTION OF FLIGHT After reading this section you should be able to… • Define exaptation. • Describe the two hypotheses for the origin of light, and outline the evidence supporting each. • Explain the temporal paradox for the evolution of birds.

As we have seen, birds are very well adapted to flight, but many of these adaptations already existed in dinosaurs that we are certain were physically incapable of flight. Thus, these features must have conferred benefits that gave their bearers a selective advantage other than those associated with flight, and were exapted for flight later. Exaptation is the term for a trait that originally evolved under a given set of selective pressures, but which subsequently becomes useful for something completely different. For example, sauropod dinosaurs have pneumatic vertebrae that lighten their extremely long necks. Pneumaticity, therefore, is not a feature that arose and spread in the dinosaur lineage because of its utility for flight. After all, we can say with certainty that sauropods did not fly (fortunately). But the presence of hollow, lightweight pneumatic bones already in place within this lineage could be co-opted for flight later. Another example of exaptation is feathers. During development and throughout the body of a bird, feathers take on different forms. Embryonic feathers are simpler and more flexible than the stiffened, branched flight feathers of adults. Similarly, flight feathers on the wings are structurally and functionally very different than down feathers or bristles, yet at the molecular level, they are all very similar, pointing to a common origin for all feathers. We find feathers of all different morphologies, from simple bristle-like structures to full flight feathers, in dinosaurs that clearly could not fly. Thus, feathers clearly evolved for different reasons than flight—perhaps insulation, display, or species recognition—and were exapted for flight late in the lineage. How, then, did powered flight first evolve in theropods? And when? Because adaptations initially thought to be associated with flight (e.g., feathers, a furcula, and pneumatic skeletons) are already observed in more basal, non-flying theropods, this is an open question. There are two primary, often quoted, and hotly debated hypotheses as to how flight originated, and both are supported by data! These hypotheses are known in shorthand as “Trees Down” and “Ground Up” hypotheses.

19.4.1 “Trees Down” Hypothesis The “Trees Down” hypothesis rests on the assumption that the feathered, dinosaurian ancestor of flying birds was small, possessing clawed fingers and grasping, anisodactyl feet, adaptations that fit them for climbing;

19.4  The Sky’s the Limit: The Evolution of Flight

499

Figure 19.53  This spectacular fossil is the type specimen of Microraptor gui, recovered from ~120 millionyear-old sediments of the Jiufotang Formation of China. Microraptor has true

flight feathers on both its forelimbs and its hindlimbs. (Courtesy of D. W. E. Hone et al., 2010.)

thus, flying evolved from gliding behavior. These early tree-dwelling dinosaurs, it is proposed, could glide in short spurts from branch to branch. Over generations, these small dinosaurs became more efficient gliders, covering more ground with each effort. Eventually, these features, combined with other acquired modifications such as a fused furcula, increasing pneumatization, and increasingly elongated arms and shortened tails, resulted in the first dinosaurs to attain powered flight. However, this hypothesis is problematic, because animals today with gliding ancestors show no evidence of transitioning to true powered flight, and a gliding phase is not, apparently, required for flight. Furthermore, until recently, there was little evidence that highly derived dinosaurs (or early birds) could have climbed trees. However, spectacular finds from China in the last three decades not only support the idea that dinosaurs may have climbed trees, but suggest that some little dinosaurs may have been uniquely suited to glide. The discovery of Microraptor gui lends support to the Trees Down hypothesis. Like Archaeopteryx, this little dinosaur had many bird-like features, including wings with feathers. But it had many ancestral dinosaurian features as well, including fully functional hands with little of the fusion observed in modern bird wings, and a long, bony tail reinforced with thin ossified tendons (Figure 19.53). This little dinosaur, exquisitely preserved, possessed something else that was utterly unexpected—true flight feathers on its hindlimbs! Who could have predicted a four-winged dinosaur? Because the long flight feathers on its “hindwing” would probably have hindered its movement on the ground, it seems likely it wasn’t doing much running, and was more likely leaping and gliding as the “Trees Down” hypothesis suggests. A modification of the “Trees Down” hypothesis contends that flight evolved from ambush hunting behaviors by predatory bird ancestors. It states that these predators climbed trees or small embankments to give them the advantage of elevation to ambush their prey, freeing their legs to disembowel their unsuspecting victims. Finally, evidence in support of the “Trees Down” hypothesis is found in living birds. There is a very strange, colorful, and smelly bird living in the Amazon rainforests that retains tiny claws on its wings until it reaches adulthood. It climbs more than it flies when it is young and uses these claws very efficiently (Figure 19.54). Although the hoatzin is an extant bird far more derived than dinosaurs like Microraptor, could it be a model for behavior that might have resulted in the development of flight? Other birds retain claws on their wings as well, including the basal paleognath, the ostrich.

500

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.54  (A) An adult hoatzin (Opisthocomus hoazin), or “stink bird” from Peru. (B) Illustration of a hoatzin chick. Hatchling hoatzins have claws on two of their fingers that they use to climb before they are capable of flight. (A courtesy of Kate,

https​://co​mmons​.wiki​media​.org/​w/ind​ex.ph​ p?cur​id=14​03955​2; B courtesy of J. A. Thomson, public domain.)

19.4.2 “Ground up” Hypothesis The other hypothesis addressing the origin of flight states that small, agile, and feathered terrestrial dinosaurs were the first to develop powered flight, and they did it by flapping their feathered arms, using them in a manner similar to the flight stroke to aid in running. The “Ground Up” hypothesis was first proposed in the late 1800s by Samuel Williston, and was modified in the 1970s by John Ostrom, who proposed the first wings were used to gather flying insects during running. Several lines of evidence support this theory. We know that the dinosaurs most closely related to birds, the small deinonychids, were fast, ground-dwelling runners. These small, ground-dwelling predators used their forelimbs for balance, and in the process, selective pressure favored arm/wing structures that provided a bit of lift, thereby allowing the predator to leap further. These behaviors would ultimately result in limbs that could generate enough lift for powered flight. Alternatively (or perhaps concurrently), it has been suggested that feathers and flying hops may have first originated for display, either for attracting mates or for intraspecific competition, and therefore would have already been available for exaptation for flight. In the 1990s, experimental evidence lent support to the “Ground Up” hypothesis. Dr. Ken Dial and colleagues hypothesized that “wing assisted inclined running” was a model for the origin of flight, and tested this idea in a series of experiments on living birds. Birds today flap their wings to provide enough lift to help them run up steep slopes or inclines (Figure 19.55). Newly hatched baby birds cannot fly, but they can run up remarkably steep slopes by flapping their tiny wings. Adult birds have also been observed to use their wings to aid in running, and many will choose to run with wing assistance rather than fly, because this behavior is less energetically expensive. In experiments, it was found that muscles that do the work during WAIR are the same pectoral muscles utilized for flight, and that stronger muscles in these areas allow birds to run up more steeply angled inclines. Thus, the “Ground Up” hypothesis posits that the forelimb development necessary for flight was driven by

Figure 19.55  Illustration of the behavior in living birds that lend support to the Wing Assisted Inclined Running (WAIR) hypothesis for the origin of flight. Living birds can walk/run up very steep inclines, vertical walls, and

even slopes tilted past vertical when they use their flapping wings to assist them. (Courtesy of J. Hutchinson, 2003.)

19.4  The Sky’s the Limit: The Evolution of Flight

selective pressures favoring the ability to run up increasingly steep inclines. This would have enabled small protobirds to run up steep slopes, rocky cliffs, or even tree trunks or embankments to pursue prey or avoid predators. The answer to how flight evolved is probably not an “either/or” scenario. Both of these hypotheses, or some combination of them, could have led to flight; WAIR could have been employed to scale tree trunks, but a gliding locomotion would be a more efficient way to leave the treetops than trying to climb back down. Thus, both of these selective forces—and perhaps some additional ones—probably contributed to the ultimate attainment of true powered flight in avians.

19.4.3 The Temporal Paradox of Bird Evolution Our understanding of the origins and evolution of flight in birds was hampered by a seeming incongruity in the timing of the development of bird-like features within Dinosauria, which among dinosaur paleontologists is referred to as “The Temporal Paradox”. The Temporal Paradox refers to the fact that members of the theropod groups most closely related to birds (i.e., Troodontidae and Dromaeosauridae)—those possessing the most bird-like features—are all found in the Cretaceous, the latest period of time in the reign of dinosaurs and long after the fossils of the first bird. Deinonychus, for example, is found in sediments dating to about 115 Mya. Conversely, Archaeopteryx, which is recognized as the earliest-known bird, comes from sediments dating to the Late Jurassic (~150 Mya)—tens of millions of years before bird-like troodons and Dromaeosaurus appeared. Simply put, the most bird-like dinosaurs were only known from a geologic time when birds had already evolved and diversified. If birds evolved from bird-like dinosaurs, shouldn’t it be the other way around? This problematic time gap provoked many questions. Could it be an artifact of preservation? That is, did avian ancestors in the Jurassic that gave rise to Archaeopteryx and other birds live in areas that were not favorable for preservation? Were they just not recognized because their bones preserved, but no evidence for feathers could be seen? To account for this, one scientist even proposed that all the very bird-like, Late Cretaceous theropods were actually true birds that were secondarily flightless, like the ostrich. So how do we resolve this paradox? In 2009, paleontologists found a fossil skeleton in China that went a long way to resolving the Temporal Paradox. Deposits in China have produced many exceptionally preserved fossils—in fact, they have provided most of the feathered dinosaur species that have been described. Jurassic deposits in China have been crucial in changing and improving our understanding of many aspects of the evolution and divergence of dinosaurs and birds. In 2009, paleontologists working in Jurassic deposits in China announced the discovery of a small troodontid dinosaur, Anchiornis huxleyi (Figure 19.56) that was found preserved with long feathers—on both its arms and legs. This was similar to the four-winged condition observed in Microraptor, but whereas Microraptor came from the Cretaceous (~120 Mya), Anchiornis was from the Jurassic (~160 Mya), much, much older than Microraptor, and indeed, older than Archaeopteryx itself (~150 Mya). The exquisitely preserved Anchiornis specimen—and others that have been described since this initial find—showed that the temporal paradox was an artifact of an incomplete fossil record, missing crucial specimens that documented key evolutionary transitions on the road to Aves—a picture that is still far from complete. It also suggests that the four-winged condition, which was one imagined prior to its discovery in the fossil record, was probably an ancestral condition for flight. This idea is supported by developmental and genetic evidence in living birds

501

502

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Figure 19.56  (A) Exceptionally preserved specimen of the Jurassic dinosaur Anchiornis huxleyi. (B) Magnified view of the arm of a (different) specimen of Anchiornis, showing attached feathers. This little feathered dinosaur is much older than the first recognized bird, Archaeopteryx. (A courtesy of J. Lindgren

et al., 2015; B courtesy of X. Wang, M et al, 2017.)

as well. It doesn’t, however, resolve the question whether flight evolved from the trees down, or the ground up!

19.5 WHAT WE DON’T KNOW 19.5.1 What Selective Pressures Led to the Evolution of Feathers? Feathers express a form of keratin, called β-keratin, or corneous β-protein, that mammals do not possess. Feather-like features or protofeathers arose in dinosaurs long before they flew and may even have been present in pterosaurs (see Chapter 14.5 and Yang et al., 2019), possibly making these features ancestral in Avemetatarsalia and to all dinosaurs. These findings raise a lot of interesting, and, as yet, unanswered questions concerning feathers. Questions to consider: • What factor favored the expression of β-keratin in integumentary structures derived from skin? Were all of these filamentous structures observed in fossils comprised of the same β-keratin as are feathers? • Did feathers arise in tandem with an elevated metabolic rate, to prevent heat loss in young dinosaurs, and were they lost as the dinosaurs reached full size? • Were feathers selected together with brooding behavior as aids in protecting and sheltering young animals? • If feathers and their precursors were for insulation, why not simple filaments like hair? • Experiments with modern birds have shown that we can induce long leg feathers on birds through genetic manipulation, so the capacity for feathered hindlimbs remains in modern birds. When, and why, did they lose these structures?

19.5.2 What Allowed the Euornithes to Survive the End Cretaceous Extinction, Paving the Way for the Ascendance of Modern Birds? It is still a mystery as to what contributed to the success of the Enantiornithine (opposite birds) and why they dominated the Mesozoic skies, while today, they are completely extinct and the Euornithes rule. Why did this very diverse and widespread group go extinct at the end of the Cretaceous Period, yet the Euornithes, minor players during the whole of the Mesozoic, were able to survive and give rise to modern birds. One explanation that has been proposed is that survivors within Euornithes were ground-dwellers, while the Enantiornithes were tree-dwellers. The worldwide devastation of forests (as evidenced by the lack of pollen in the fossil record after the asteroid impact, Chapter 20) at the Cretaceous–Paleogene boundary would have favored survival of the ground-dwelling Euornithes.

19.5  What We Don’t Know

503

Questions to consider: • If forests didn’t disappear globally as some argue, what other factors could have allowed Euornithes to survive the Cretaceous– Paleogene extinction? A diet of seeds, the ability to fly far, larger brains, or predominantly altricial young? • If Euornithes hadn’t survived, how would modern ecosystems be different in the absence of birds?

CHAPTER ACKNOWLEDGMENTS We thank Dr. Alyssa Bell and Dr. N. Adam Smith for their generous reviews and suggested improvements to this chapter. Dr. Bell is a Lecturer in the Geological Sciences Department at Cal State Polytechnic University in Pomona. Dr. Smith is Curator at the Bob Campbell Geology Museum at Clemson University.

INSTITUTIONAL RESOURCES Chiappe, L. M. (2007). Glorified Dinosaurs: The Origin and Early Evolution of Birds. John Wiley, Hoboken, New Jersey. Chiappe, L. M., and Qingjin, M. (2016). Birds of Stone: Chinese Avian Fossils from the Age of Dinosaurs. JHU Press, Baltimore, Maryland. Howard Hughes Medical Institute. BioInteractive, the origin of flight—what use is half a wing. https://youtu.be/JMuzlEQz3uo. Paul, G. S. (2002). Dinosaurs of the Air: The Evolution and Loss of Flight in Dinosaurs and Birds. JHU Press. University of Montana, Development of wing-assisted incline running. https:// youtu.be/b1dekSaGhlc and https://youtu.be/k94EDd8aKng.

LITERATURE Barsbold, R., Osmólska, H., Watabe, M., Currie, P. J., and Tsogtbaatar, K. (2000). A new oviraptorosaur [Dinosauria, Theropoda] from Mongolia: The first dinosaur with a pygostyle. Acta Palaeontologica Polonica, 45(2), 97–106. DePalma, R. A., Burnham, D. A., Martin, L. D., Larson, P. L., and Bakker, R. T. (2015). The first giant raptor (Theropoda: Dromaeosauridae) from the hell creek formation. Paleontological Contributions, 2015(14), 1–16. Field, D. J., Bercovici, A., Berv, J. S., Dunn, R., Fastovsky, D. E., Lyson, T. R., Vajda, V., and Gauthier, J. A. (2018). Early evolution of modern birds structured by global forest collapse at the end-Cretaceous mass extinction. Current Biology: CB, 28(11), 1825–1831. Greenwold, M. J., and Sawyer, R. H. (2011). Linking the molecular evolution of avian beta (β) keratins to the evolution of feathers. Journal of Experimental Zoology Part B: Molecular & Developmental Evolution, 316(8), 609–616. Hone, D. W., Tischlinger, H., Xu, X., and Zhang, F. (2010). The extent of the preserved feathers on the four-winged dinosaur Microraptor gui under ultraviolet light. PLoS One, 5(2), e9223.

Hutchinson, J. R. (2003). Biomechanics: Early birds surmount steep slopes. Nature, 426(6968), 777–778. Lindgren, J., Sjövall, P., Carney, R. M., Cincotta, A., Uvdal, P., Hutcheson, S. W., Gustafsson, O., Lefèvre, U., Escuillié, F., Heimdal, J., Engdahl, A., Gren, J. A., Kear, B. P., Wakamatsu, K., Yans, J., and Engdahl, A. (2015). Molecular composition and ultrastructure of Jurassic paravian feathers. Scientific Reports, 5(1), 1–13. Lü, J., and Brusatte, S. L. (2015). A large, short-armed, winged dromaeosaurid (Dinosauria: Theropoda) from the Early Cretaceous of China and its implications for feather evolution. Scientific Reports, 5, 11775. Middleton, K. M., and Gatesy, S. M. (2000). Theropod forelimb design and evolution. Zoological Journal of the Linnean Society, 128(2), 149–187. Wang, X., Pittman, M., Zheng, X., Kaye, T. G., Falk, A. R., Hartman, S. A., and Xu, X. (2017). Basal paravian functional anatomy illuminated by high-detail body outline. Nature Communications, 8, 14576.

504

CHAPTER 19    How Do We Know Birds Are Dinosaurs?

Xu, X., and Norell, M. A. (2004). A new troodontid dinosaur from China with avian-like sleeping posture. Nature, 431(7010), 838–841. Yang, Z., Jiang, B., McNamara, M. E., Kearns, S. L., Pittman, M., Kaye, T. G., Orr, P. J., Xu, X., and Benton, M. J. (2019). Pterosaur integumentary structures with complex feather-like branching. Nature Ecology & Evolution, 3(1), 24–30.

Zhang, Y., O’Connor, J., Di, L., Qingjin, M., Sigurdsen, T., and Chiappe, L. M. (2014). New information on the anatomy of the Chinese Early Cretaceous Bohaiornithidae (Aves: Enantiornithes) from a subadult specimen of Zhouornis hani. PeerJ, 2, e407.

20 HOW DO WE KNOW ABOUT EXTINCTIONS?

20

THE END OF THE DINOSAUR REIGN AND OTHER MASS EXTINCTIONS

E

xtinction.

The very word seems more or less synonymous with dinosaurs. But extinctions have occurred often throughout the history of life. Since life began almost 4 billion years ago, organisms have come and gone. In fact, over 99% of all organisms that have ever lived, from the outlandish soft-bodied Ediacaran creatures, to the trilobites and marine organisms of the Burgess Shale, to the dinosaurs (Figure 20.1), and—perhaps more familiar—woolly mammoths and saber-tooth cats, are all now extinct. The life we see around us that is so familiar represents less than 1% of all the organisms that have ever occupied our planet! Extinction is the ultimate fate of all species, including ours—and it is happening today. Although in the mind of humans, the concept of extinction is associated with only negative things, extinctions throughout the history of our planet are generally accompanied by the origins of new things. Extinctions are more than death and destruction—they are also life and diversity. The definition of extinction is when the last member of a species (or genus, or family) dies. All members of a species may disappear, but if there are other, still-living species within that genus, then the genus has not gone extinct (only the species). Thus, defining extinction depends upon what level you choose. Given what you now know about them, have “dinosaurs” truly gone extinct?

20.1 TYPES OF EXTINCTIONS After reading this section you should be able to… • Differentiate between the four types of extinctions. • Explain what a Lazarus taxon is.

Not all extinctions are equal. In fact, there are multiple types of extinction to consider.

IN THIS CHAPTER . . . 20.1 TYPES OF EXTINCTIONS 20.2 VULNERABILITY TO EXTINCTION 20.3 MASS EXTINCTIONS 20.4 THE END-PERMIAN EXTINCTION: THE GREAT DYING 20.5 DINOSAURS GET THEIR CHANCE: THE END-TRIASSIC EXTINCTION 20.6 THE DINOSAUR REIGN ENDS: THE CRETACEOUS–PALEOGENE MASS EXTINCTION 20.7 THE POST-CRETACEOUS WORLD 20.8 WHAT WE DON’T KNOW

506

CHAPTER 20    How Do We Know about Extinctions?

Figure 20.1  Artistic interpretation of the End-Cretaceous extinction event.

Tyrannosaurus rex met the same fate that >99% of all life on this planet has met. (Courtesy of K. Carr.)

Types of extinctions include: • Background extinctions are those that happen “in the background”, so to speak. Over geologic time, species have been continuously evolving (i.e., speciation) and going extinct at a fairly steady pace. The balance between this steady, background extinction and speciation results in the diversity of life we see today. Background extinctions are measured, or quantified, by the number of species that go extinct over a given time period. It is estimated that the normal background extinction rate is ≤1 species a year for every million that exist. Individual species, regardless of the size of populations, diversity, or distribution, typically exist for about 500,000 to 1–2 million years before going extinct. So, to put this in context, it is estimated that, although the human lineage extends back to about 4 million years, humans in their present form (e.g., Homo sapiens sapiens) originated between 200,000 and 300,000 years ago! As if you didn’t have enough to worry about, we may have lived over half our allotted species lifetime already! • Mass extinctions get all the attention because they are dramatic. During a mass extinction, a large portion of species go extinct over a short period of time (geologically speaking), and the overall rate of extinction greatly outpaces the rate of speciation. Mass extinctions are defined as events where more than 75% of species go extinct, and usually, these mass extinctions result from extraordinary events that are both sudden and temporary, but which affect large numbers of species indiscriminately. When mass extinctions occur, we see a sharp decrease in both diversity and abundance of life. In fact, it is so apparent that most of the divisions on our geological time scale are defined by extinctions of major groups in mass extinction events. • Local extinctions occur when a species has a reduction or change in its range, so in regions where the organism was once common, it is now never seen. Examples include the American grizzly bear (Figure 20.2A). When Lewis and Clark first traveled the interior of North America, the grizzly was frequently sighted by these explorers on the plains and prairies of the Midwest, but today it is never seen there, and its range is restricted primarily to Canada and Alaska—and Yellowstone Park, of course (Figure 20.2B). Another term for a local extinction is extirpation, which is more fitting because a local extinction is not a true extinction, in that the species does still exist, just somewhere else.

20.1  Types of Extinctions Figure 20.2  (A) The North American Grizzly bear, Ursus arctos horribilis, is one of the largest predators alive today. (B) The grizzlies had a much

• Global extinctions, on the other hand, are just that—global. Species that once enjoyed a wide distribution and great success, as measured by diversity, are no longer found anywhere on the planet. Examples of global extinction in recent times include the dodo, the passenger pigeon, and some of the great Australian marsupials, like the thylacine or Tasmanian tiger (Figure 20.3), all of which have gone extinct during recorded human history. Then, of course, there are “mistaken” extinctions—this is when a species long thought to be extinct is then rediscovered. An example is the coelacanth, a large fish with fleshy, lobed fins. The lobe-finned fish, or crossopterygians, are thought to be the ancestors of all tetrapods, from frogs to crocodiles and elephants. The coelacanth was known only from fossils (Figure 20.4A) in ancient sea sediments, and was thought to have gone extinct at the end of the Cretaceous, along with the dinosaurs. Then, one turned up, quite alive, in the net of a South African fishing captain (Figure 20.4B). It wasn’t extinct after all, just very well hidden! Those species identified in mistaken extinctions are also called “Lazarus taxa” (named after the biblical character Lazarus, who was raised from the dead by Jesus), because the discovery of small pockets of living members (or refugia) essentially raises these taxa “from the dead”. Mistaken extinctions are clearly observational artifacts, because these species obviously did not actually go extinct globally (although they may have locally).

Figure 20.3  Images of animals that were once plentiful, and which co-existed with modern humans, but which have since gone globally extinct. (A) The dodo was a giant flightless bird that survived well in

the isolated island environment of Mauritius, east of Madagascar. B is a passenger pigeon, once existing in flocks so huge as to block the sunlight. Right, the last thylacine, or Tasmanian tiger, was a carnivorous marsupial endemic to Tasmania, New Guinea, and mainland Australia before being completely hunted to extinction by humans early in the 1900s. These animals are the subject of intense research into “de-extinction”, an attempt to re-create these lineages using ancient DNA recovered from the tissues of the animals. (A courtesy of J. Hoefnagel, public domain; B courtesy of S. St. John, https://flic.kr/p/ pEZ6Jq; C, public domain.)

wider range before the arrival of humans, extending from what is now Alaska to Mexico, and from California to the Midwest. This successful predator experienced a local extinction event, and now is much more limited in its range. (A courtesy of Jean Beaufort, https://commons.wikimedia. org/wiki/File:GrizzlyBearJeanBeaufort. jpg; B courtesy of CNX OpenStax, https:// commons.wikimedia.org/wiki/File:Figure_ B47_03_06.jpg.)

507

508

CHAPTER 20    How Do We Know about Extinctions?

Figure 20.4  The lobe-finned coelacanth, a fish on the lineage leading to tetrapods, was only known from fossils like this one in (A), and was thought to have gone extinct in the Paleozoic. However, in 1938,

fishermen off the coast of South Africa caught one in their net (B), and brought it to a local museum, where it was identified. This fish is more closely related to tetrapods (and therefore you) than it is to the much more common and diverse ray-finned fishes. (A courtesy of Reinhold Möller, https://commons. wikimedia.org/wiki/File:Bamb​erg_N​aturk​ undem​useum​_Foss​il_Qu​asten​floss​e_17R​ M1927​.jpg;​B adapted from Yinan Chen, in Public Domain.)

Coelacanths weren’t only mistaken as extinct because we hadn’t seen one alive until 1938; they were assumed extinct because there was no fossil record of coelacanths after the Cretaceous. However, since we now know they’re still around today, we also know they were around for the 65 million years for which we don’t have their fossils. We call this gap in the fossil record a ghost lineage. Ghost lineages, or ghost taxa, refer to any taxon for which we can infer existence during a time period in which they did not leave a fossil record (or for which we simply haven’t discovered one yet). The extinction of the dinosaurs is sometimes referred to as a “mistaken extinction” because a remnant group still exists, and is widely distributed and highly successful. That is why scientists distinguish between “non-avian dinosaurs”, which are completely extinct, and have been for at least 65 million years, and “avian” dinosaurs which are thriving. Lazarus taxa demonstrate how big the gap in our knowledge is, even today, with respect to creatures with whom we share our planet. We have named and described about 1.5 to 2 million living species, the vast majority of which are land-dwelling animals. But, based upon distribution patterns and other factors, it is estimated that there are probably around 9 million species that currently exist, but that are not recognized, described, or characterized—including over 80% of terrestrial species, and over 90% of marine organisms! If we do not even know the living groups with which we share the planet, how far off will our estimates be of ones who once lived, but are now no more? Today, when you read about or discuss extinctions, most often these refer to mass extinctions, because they are both monumental and unpredictable with respect to the groups affected. Past mass extinctions radically changed the planet and the trajectory of life—repeatedly. Although the sudden and spectacular loss of life makes mass extinctions stand out, in reality, background extinctions represent a far greater loss in terms of overall number of taxa affected. It is estimated that, from the origin of life in the Archaean (3.5–4 billion years ago) to today, this planet has been home to somewhere between 5 and 14 billion species, more than one species for every year of Earth’s existence!. Because only 9 million are estimated to exist today, that represents a lot of extinctions.

20.2  Vulnerability to Extinction

20.2 VULNERABILITY TO EXTINCTION After reading this section you should be able to… • List and explain factors that can put a species at risk of extinction.

Why do species go extinct? What characteristics make a species vulnerable to extinction? Many factors combine to make some species more susceptible to background extinctions than others. Factors that increase vulnerability to background extinction include: • Small population sizes: This makes a group more likely to succumb to species-specific diseases or environmental challenges. Small populations are particularly sensitive to habitat change. • Limited geographic range: If that range is restricted, compromised, or invaded, these organisms have nowhere else to go to recover. For example, the Iriomote cat only lives on the Iriomote island of Japan; any habitat destruction could spell its end. • Dependence on single food sources/highly specialized diet: 99% of the giant panda’s diet comes from only one source: bamboo. Because of its dependence on bamboo forests in the mountains of China, habitat invasion through deforestation and farming put this animal at particular risk. Beyond human interference, if a blight or virus affects their sole food source, pandas will be at an even greater risk for extinction. • Low reproductive rates: Particularly when coupled with very longlived organisms, a low birth rate can endanger a species because if disease or disaster strikes, these groups take a very long time to recover. When animals do not breed until they are older, and do not have many young when they do, they decline rapidly when habitats are threatened. They are not as resilient as those species that reproduce often, with numerous young. For example, elephants gestate for nearly two years (645 days) prior to giving birth, and can only produce one baby at a time. Conversely, a female cat can have up to ten kittens at a time and can give birth every 64 days. In the same time it takes for one elephant to be born, a single cat may produce 100 young. Which do you think is more in danger of extinction? • Low fitness/non-competitive: Animals that are slow-moving, have low mobility, poor defensive strategies, or that have evolved without the pressure of predators (such as animals that have been relatively protected on an island environment until new predators are introduced) are particularly at risk. Some flightless birds are an example (e.g., the dodo, great auk, or elephant bird) as are many species found on islands like Australia or Madagascar. • Large size: Large animals tend to grow slower and have lower reproductive rates. Large animals also tend to require greater habitats, ranges, and food supplies, all of which put them at risk. These are just a few factors that make a species more prone to extinction, and they probably applied equally to the non-avian dinosaurs as to today’s animals. Additionally, habitat changes were particularly problematic over the course of dinosaur existence. When the giant inland sea

509

510

CHAPTER 20    How Do We Know about Extinctions?

that had divided North America for millions of years finally receded for the last time, there was no longer a barrier between dinosaurs from what is now the east coast of North America and the west coast; dinosaurs were free to intermingle. It could be, then, that diseases that had coevolved with one group of dinosaurs were free to spread to other, closely related species that hadn’t co-evolved with the disease, decimating populations. At present, there are no hard data to support this hypothesis, but it is not unreasonable that such intermingling had a deleterious effect on some populations, given what has been observed in our own and other living species. When the Europeans invaded North America after thousands of years of separation, they brought with them diseases to which they had become accustomed (e.g., smallpox, measles, influenza), but to which the native populations had never been exposed. Possessing no natural immunity to European diseases, indigenous populations suffered catastrophic losses from sickness—tens of millions of individuals. Even if a species has none of the vulnerabilities listed above, they are not immune from extinction. Mass extinction events, as mentioned above, are not selective, so all species are equally vulnerable. They are driven by rapid and dramatic changes in Earth systems, whether caused by internal (e.g., volcanism) or external (e.g., impact) events. These disruptions can have profound effects on the biosphere, leading to the extinction of many species, including those that were widespread and highly successful.

20.3 MASS EXTINCTIONS After reading this section you should be able to… • List the five largest mass extinction events in Earth’s history. • Differentiate the mass extinctions influencing dinosaur evolution from others.

The fossil record of our planet records five major mass extinction events in the Phanerozoic (the time since the appearance of multicellular organisms, or about the last 500–600 million years, TABLE 20.1), marked by a precipitous drop in species numbers relative to those prior to the event (Figure 20.5). We see certain groups of organisms (e.g., trilobites) that were plentiful, diverse, and widely distributed in the rocks leading up

TABLE 20.1 EARTH’S FIVE LARGEST* EXTINCTION EVENTS IN CHRONOLOGICAL ORDER Extinction

Age

% Extinct

Relative Size (based on species loss)

End Ordovician

444 Ma

86% of species 57% of genera

Second largest

Late Devonian

374-359 Ma

75% of species 35% of genera

Fifth largest

End Permian

252 Ma

96% of species 56% of genera

Largest

End Triassic

201 Ma

80% of species 47% of genera

Third largest

End Cretaceous

66 Ma

76% of species 40% of genera

Fourth largest

*These ranking vary on the methods, data, and counts (e.g., marine vs. total genera) used, see Bond and Grasby, 2017, for a comparison of different rankings. The End Permian always ranks at the top, however.

20.3  Mass Extinctions

511

Figure 20.5  This graph shows the relative extent and significance of extinctions over time. The Y-axis is

the percentage of marine animal genera becoming extinct. What sets mass extinctions apart from the others recorded here is the sheer magnitude of the species lost in a short period. (Courtesy of CNX OpenStax, https://commons.wikimedia.org/ wiki/File:Figure_47_01_04.jpg.)

to a certain point—then we do not see them again, but instead see very different animals in the younger rocks deposited later. When many different types of animals show this pattern, and they all disappear in the same rock layers, that is how we identify a past mass extinction. These are referred to as boundary events, and at these boundaries, species can disappear completely, or they can give rise to new, related forms. Of the five largest extinction events recorded in Earth’s history, three of them affected the dinosaurian evolution directly, and we will look at those in detail in the sections below. The other two occurred earlier, during the Paleozoic Era—one at the end of the Ordovician Period 444 million years ago, and the other during the Late Devonian Period, about 374 million years ago. Although these two extinction events didn’t directly affect the dinosaurs, like all mass extinction events, they resulted in a dramatic redirection of the course of life on Earth, determining which organisms would move forward on Earth’s stage, and which organisms would vanish forever. Without extinctions, life’s history on Earth would have been entirely different, and dinosaurs may never have evolved. We too, owe our existence to the conditions influencing who survived and flourished following large extinction events. Without the End-Cretaceous mass extinction that eliminated the non-avian dinosaurs, they might still dominate terrestrial environments today, as do their avian relatives. Although mammals co-existed with dinosaurs throughout their entire reign, mammals were only inconsequential background players until the non-avian dinosaurs were removed. Did the success and diversity of the dinosaurs delay or hinder the eventual rise and diversification of mammals, including those we care most about—Homo sapiens—us?

20.3.1 The End-Ordovician Mass Extinction The mass extinction event (which was actually two separate, but closely spaced, events) that occurred at the end of the Ordovician Period is the second largest in the history of Earth, wiping out roughly 86% of all species. All the major groups suffered during the event, with many species of brachiopods, bryozoans, and corals becoming extinct. Imagine how different our planet would be without the extensive coral reefs that provide habitat for so many life forms, and which redirect ocean currents, directly affecting life on land! The most probable cause of the End-Ordovician extinction event, after millennia of warm global temperatures, is widespread planetary cooling, which was eventually accompanied by extreme glaciation. These were

512

CHAPTER 20    How Do We Know about Extinctions?

Figure 20.6  This paleomap shows the location of all the landmasses in the world with exposed surfaces, centered around the south pole. The

continents merged through tectonic action to form the supercontinent of Gondwana, and this began to drift poleward. As CO2 outgassing from volcanic activity decreased, it could no longer counteract this global cooling and huge ice sheets formed. (Reprinted with permission from Chris Scotese.)

the result of the poleward movement of the supercontinent Gondwana, and reduced atmospheric CO2 because of decreased volcanic activity. The lethality of this cooling event was the result of the paleogeography of the Late Ordovician (Figure 20.6). Let’s look at the chain of events that set off this mass extinction: 1. Weathering begins reducing atmospheric CO2: Prior to the extinction event, a large number of igneous rocks were produced in a pulse of volcanic activity from island arcs located at the equator (Figure 20.6). These rocks were continually weathered by acidic rain (atmospheric CO2 combines with rainwater to form carbonic acid) of the equatorial climate. The weathering and erosion of these igneous rocks deliver calcium and other minerals to the ocean, where they are incorporated into the shells of marine organisms. When these shelled organisms die, they are buried, sequestering the CO2 that was once in the atmosphere. 2. The climate cools: As a greenhouse gas, CO2 traps infrared radiation from the Earth (keeping it warm) so its reduction as the major continents continued to drift poleward contributed to a cooling climate. 3. Glaciers began to form: As the climate cooled, glaciers began to form on the southern supercontinent of Gondwana. Evidence of this glaciation is seen in the rocks of Africa and the Sahara Desert, areas that were part of Gondwana during the Ordovician (Figure 20.7).

Figure 20.7  Parallel striations, like the ones pictured here, have been found on Ordovician rocks in Africa and the Sahara Desert. These striations are made

as glaciers carry large-sized sediment over the bedrock, carving striations and polishing the surfaces. These features are one piece of evidence for past glaciations. (Courtesy of D. Czajka.)

20.3  Mass Extinctions

4. Sea levels drop: As glaciers incorporated water in the form of ice on the continents, sea levels dropped. This had devastating consequences for life living on the shallow, warm continental shelves. 5. Oxygen mixing: Changing ocean temperatures and chemistry modified ocean water circulation causing oxygen levels in the deeper oceans to dramatically fluctuate, fatally affecting life in the deep sea as well. This is evidenced by changes in the rock record from gray, bioturbated shale indicative of higher oxygen levels, to black shales, indicative of low oxygen. These shales were also devoid of bioturbation; the tracks and traces of small organisms living in or traveling across the ocean bottom sediments. During the Ordovician (~488–444 Ma), except for very early plants (i.e., moss), most multicellular life existed in the world’s oceans. Sea levels were high and continental shelves, where most marine life lives, were plentiful. When global cooling occurred in the middle to end of this period, it caused a dramatic drop in sea level, and this in turn had dire consequences for ocean life during this period; many underwater habitats were exposed to air and lost to marine life. Eventually, the Earth once again began to warm, and during the Silurian Period, the glaciers melted. With this reprieve, life began to diversify into new habitats that opened up, both in the expanding seas and on land. In the wake of the End-Ordovician extinction, the Earth saw the rapid expansion and diversification of vertebrates, especially jawed and bony fish. These were important precursors on the path to dinosaurs because they were the first organisms to possess “true” bone.

20.3.2 The Late Devonian Mass Extinction The Late Devonian extinction was actually a series of extinction “pulses”, occurring over about 20 million years. The first major pulse (at 374 Ma) and the last (at 359 Ma), marked the end of the “Age of Fishes”. By the end of the Devonian Period, there was a much greater diversity of living organisms, thus many more types of organisms were affected. Insects and plants had begun to colonize the land, and bony fish were rapidly diversifying in the oceans. The fossil record shows that the vast majority of lifeforms wiped out in this event were marine, and the few terrestrial species in existence weren’t greatly affected. Many causes have been suggested for this extinction, some similar to those triggering the previous event; similar changes in sea level have been recorded in the rock record, and there is evidence for increasing anoxia. It has also been proposed that perhaps this event was triggered by an impact event, and a large formation in Sweden, known as the Siljan Ring, can be correlated to this approximate time. But one very likely contributing factor to this massive die-off may have been…trees! At the beginning of The Silurian, as life staged a comeback from the End-Ordovician extinction, plant life on land was small, not widely distributed, and low to the ground. In addition, strong root systems, seeds, and vascular systems had not yet evolved, so plants were limited to regions of wet or damp soils, similar to environments where today’s mosses are found. The middle Devonian saw very low levels of atmospheric oxygen (about 10%, relative to today’s 21%) and high levels of CO2. But by the Late Devonian, the advanced plant structures—intricate vascular systems and complex roots—had developed, allowing plants of all kinds to invade vast areas of the exposed continents. Plants also expanded upward, reaching a height of up to 30 meters! The early trees of the Devonian, called lycopsids, were not like present-day trees; fossils show that they were more like giant, woody ferns (Figure 20.8).

513

514

CHAPTER 20    How Do We Know about Extinctions?

Figure 20.8  (A) The fossil remains of one of the first vascular plants, with a single root (arrow) exposed.

These plants were fern-like in structure, but grew as tall as ~30 m. (B) The development of roots and a complex vascular system provided these plants with a great evolutionary advantage, and made possible the great forests of the Carboniferous. As they spread throughout the continent, they sequestered CO2 in their biomass, and produced oxygen as a byproduct of photosynthesis, greatly altering the chemistry of the atmosphere— and the progression of life. (A courtesy of M.C. Rygel, https://commons.wikimedia. org/wiki/File:Lycopsid_joggins_mcr1.JPG; B courtesy of Retallack, https​://co​mmons​.wiki​ media​.org/​w/ind​ex.ph​p?cur​id=49​01112​7)

These complex plants brought about two significant changes that forever shifted the balance of life on the planet. First, their deep roots contributed to breaking up the bedrock, greatly increasing the rate of weathering. Second, they took in much greater amounts of CO2 than smaller plants could, contributing to the rapid decrease of this greenhouse gas (and thereby to global cooling). It is estimated that atmospheric CO2 dropped by up to 90% in the Late Devonian, and the breakdown of this CO2 “blanket” led to a dramatic cooling of the climate and glaciation. This had devastating impacts on life during this time period, for many of the same reasons that prior cooling devastated life in the Ordovician. The episodic nature (i.e., the pulses) of this extinction may have been associated with plants evolving these novel features of roots, spores, and precursors of true seeds—innovations that allowed them to spread and flourish, resulting in continents that became densely forested. In addition, weathering added nutrients to the waters, contributing to algal blooms and anoxia. Thus, although the Late Devonian extinction shared some features with the End-Ordovician extinction that preceded it, because life had increased greatly in complexity and occupied more niches by the end of the Devonian, the devastation to life was more widespread than the preceding glaciation. Reef-building organisms like corals were especially hard hit during the Late Devonian mass extinction, as were groups like the trilobites, brachiopods, and ammonites. Many of the bony fish and sharks were also hard hit, especially the armored, apex predator placoderms. The Devonian was also when the first tetrapods evolved, beginning the transition of vertebrates to land. This may have been fueled in part by low oxygen levels early in the Devonian. As animals became more active, the need for oxygen to fuel their muscle activity grew as well. When oxygen is low in the atmosphere, it is even lower in the water, so the first tetrapods (Figure 20.9) may have needed to move onto land to survive. Alternatively, their greater activity levels required more food, and as oxygen levels increased throughout the Devonian (because of increased distribution of plants, including trees) the move to land may have been favored by access to the abundant insects that thrived as oxygen levels increased in the Devonian with the expansion of forests. The only tetrapods to survive the Late Devonian extinction were a lineage of freshwater, five-fingered tetrapods—to which your own hands testify. It would take millions of years for the groups impacted by the extinction to recover, but they eventually did, with the dawning of the “Age of Amphibians” in the Carboniferous Period. The critically important amniote egg would also arise during this time, in the wake of the Late Devonian extinction. Although the End Ordovician and Late Devonian mass extinctions didn’t directly affect the dinosaurs, they help illustrate some of the ways in which the Earth system can be thrown out of balance and pushed to

20.4  The End-Permian Extinction: The Great Dying Figure 20.9  This cladogram shows the transition from the lobe-finned fish (sarcopterygians, of which the coelacanth and living lungfish are examples) to tetrapods fully adapted to life on land. Fossil evidence for this

transition is abundant, represented here by (from bottom to top): Eusthenopteron, a well-known late Devonian sarcopterygian; Panderichthys; Tiktaalik; Acanthostega; Ichthyostega; and Pederpes. Evolutionary patterns include increasing robustness of the forelimb, the reduction and simplification of the tail, and the appearance of digits, first on the forelimbs and then the hindlimbs. (Courtesy of M. Karala, https://commons.wikimedia.org/ wiki/File:Fishapod_evolution.jpg.)

extremes, which can have dire consequences for life on the planet. But what about the extinction events that shaped dinosaur evolution? Were they similar to these two earlier mass extinctions, or were they completely unique in cause and effect?

20.4 THE END-PERMIAN EXTINCTION: THE GREAT DYING After reading this section you should be able to… • State the most likely cause of the End-Permian Extinction. • Discuss factors that made the Siberian Traps volcanism so lethal for life on the planet. • Identify organisms that went extinct and groups that diminished at the End Permian. • List key survivors of the End-Permian extinction.

As discussed in Chapter 5, life in the Permian was represented by large, diverse, widespread, and very successful amphibians that included carnivores, herbivores, and omnivores, which filled many of the niches later occupied by reptiles. Although amphibians were a large part of the Permian landscape, amniotes were also present, and the distant ancestors of all living mammals and all archosaurs first arose in the Permian. Some of these—the ancestors of pseudosuchians (crurotarsans) were becoming dominant. The dicynodonts, on the line leading to mammals, were also diversifying. The Archosaurian ancestors of dinosaurs, however, remained in the background.

515

516

CHAPTER 20    How Do We Know about Extinctions?

The Permian ended with the greatest extinction our world has ever experienced, so much so that it is sometimes referred to as the “Great Dying”. It is estimated that 96% of species went extinct with this event, and it would take over 10 million years to begin to recover from this extinction event because of the massive loss of life and the lingering effects.

20.4.1 Proposed Causes of the End-Permian Mass Extinction Many hypotheses have been put forth to try to explain the cause or causes of this greatest of extinctions, but like the previously discussed events, no single cause has yet been identified. One hypothesis states that, like other extinctions, this one may have been triggered by an extraterrestrial object. But if our planet was hit by an extraterrestrial body of sufficient size to do such damage, there should be hard evidence—a crater, perhaps, or shocked quartz, or a layer of iridium (see Section 20.6 below); but no such evidence has yet been uncovered that can be directly linked to the End-Permian event. Excessive volcanism has been suggested as a cause, and indeed, massive volcanic activity is recorded in the rock record at the time of this extinction. The Siberian Traps mark the largest volcanic event in Earth’s history, in both geographic extent and duration. This volcanic activity resulted in a series of eruptions that flooded the landscape, covering much of what is now Siberia in igneous basalts. Some estimate that the original area covered by this volcanic rock was about 7 million square kilometers! Even after 200 million years of weathering, these basalts still extend over an area covering about 1 million square kilometers— roughly the area of the entirety of western Europe (Figure 20.10). The volcanism that produced these Siberian Traps is hypothesized to have continued for over a million years uninterrupted, expelling thousands of tons of CO2 and SO2 into the atmosphere. As we have seen previously, such increases cause acid rain and extreme ocean acidification. The drop in oceanic pH resulted in the dissolution of coral reefs, as well as the shells of mollusks. Losing these groups of organisms would greatly affect marine food webs. Other sedimentary data show strong evidence for a trio of co-occurring conditions that would devastate marine life—anoxia (greatly reduced oxygen levels), euxinia (lots of dissolved hydrogen sulfide), and very high levels of CO2. We know that the oceans became anoxic and euxinic because we observe black marine shales

Figure 20.10  This map marks the extent of the Siberian Traps, the massive expanse of volcanic basalts resulting from the long duration of volcanic activity that corresponds to the end of the Permian. (Derivative work

by Jo, original by Kaidor, https://commons. wikimedia.org/wiki/File:Extent_of_Siberian_ traps_german.png.)

20.4  The End-Permian Extinction: The Great Dying

from this time period with sedimentary structures that do not form in the presence of oxygen, such as tiny, raspberry-like pyrite framboids. Flood basalts like the Siberian traps are the result of “hot spots”, or large plumes of superheated material that extend from the Earth’s mantle toward the surface. What may have made the Siberian flood basalts so deadly at the End-Permian was not only their size and extent, but also their location. These flood basalt eruptions were occurring in the Tunguska Basin, a sedimentary basin that was host to petroleum-bearing salt deposits and coal beds. The heat from these hot spot eruptions would have caused the hydrocarbon materials to ignite like a giant coalfired furnace, greatly increasing the input of greenhouse gases into the atmosphere and raising global temperatures. In fact, ocean surface temperatures were estimated to have reached 40°C (104°F) based on oxygen isotope data! Another factor that is associated with the end of the Permian, and which may have contributed to this extinction is high levels of atmospheric methane, a far more potent greenhouse gas than CO2. Today, large deposits of methane hydrates (essentially methane ice) are stored in the deepest parts of the ocean. The low temperatures and high pressure keep these relatively stable. Enormous amounts of methane are tied up in these deposits. It is hypothesized that similar methane deposits in the Permian may have been released into the atmosphere by the eruption of the flood basalts onto continental shelves. As long as they remained frozen, these methane deposits were inert, but the warming resulting from the eruptions may have changed that. If the Earth’s current deposits were to be released as rapidly as they were in the Permian, both terrestrial and marine life today would be greatly affected. All of these cascading factors would have created conditions inhospitable (to say the least) for life in the seas. This is consistent with the disproportionately greater effect the End-Permian extinction had on marine vs. terrestrial life. Although some evidence has been presented for extraterrestrial impacts as a cause of the End-Permian extinction, no craters can be directly linked to this extinction. Some potential craters have been identified, but these do not correlate to the same time as the extinction, are too small to have caused the extent of extinction observed, or turn out to not even be impact craters at all. While the exact causes of the End-Permian extinction event are still debated, the rock record shows inarguably that the Earth experienced dramatic volcanism that had devastating effects on atmospheric and oceanic chemistries. More work is needed to elucidate the exact chain of events responsible for the most massive extinction event our planet has ever seen.

20.4.2 Which Organisms Went Extinct? Remember that mass extinctions affect successful and vulnerable species equally. Who went extinct in the Great Dying? Marine organisms: Life in the oceans was hit hard by the End-Permian extinction. Trilobites, successful and very diverse arthropods that originated at the Cambrian Explosion (Figure 20.11A), disappeared entirely at the end of the Permian. Corals, and the coiled ammonites that looked like nautiloids, but which were more closely related to squid and octopus, were both hugely successful and widespread ancient marine invertebrates that were present throughout all of the Paleozoic oceans. But these decreased dramatically after the extinction, and the few species that survived the event were very different than those that came before (Figure 20.11B). Other marine casualties included most eurypterids (sea

517

518

CHAPTER 20    How Do We Know about Extinctions?

Figure 20.11  These are examples of the type of life that flourished in the Permian seas, but which either vanished completely or changed drastically after the End-Permian extinction event. (A) Trilobites (in

ventral and dorsal views) did not survive this event, even though they were present since the beginning of the Cambrian. (B) This pyritized ammonite has very different sutures patterns than those that followed. (C) These beautiful flower-like crinoids, which belong to the same group as today’s sea stars, were greatly reduced from their wide Paleozoic distribution. (A courtesy of Moussa Direct Ltd., https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=44​61171​; B courtesy of J. St. John, https://flic.kr/p/ppiJ3R; C courtesy of Vassil, https://commons. wikimedia.org/wiki/File:Agar​icocr​inus_​ameri​ canus​_Carb​onife​rous_​India​na.jp​g)

scorpions), brachiopods, crinoids (Figure 20.11C), and echinoderms (like starfish). Gastropods (snails and slugs) were also hard hit, losing over 95% of their genera. Insects: The vast majority of Paleozoic insect groups disappeared entirely at the end of the Permian. Insects had diversified far beyond what we see today, and by the end of this era, many were larger and more diverse than today’s forms. Imagine being dive-bombed by a dragonfly with a wingspan of over a foot (Figure 20.12) or meeting a centipede larger than you on your morning run! But the Permian extinction saw the end of those groups as well as many others. Interestingly, in addition to being different from other mass extinctions in showing a greater loss of marine than terrestrial groups, the end-Permian extinction is the only record we have of mass extinctions of insects. Plants: Many land plants declined or went extinct. We know this because pollen grains are preserved in the sediments from this time period, but these differ greatly from the pollen found in later rocks. We also see a sharp decline, or total lack of evidence of many plants, even though these were abundant in Permian deposits. In fact, one of the ways the P–T event is recognized is by the existence of the so-called “coal gap”, a period of about 10 million years when coal deposits were not formed at all, anywhere on the planet. Because coal forms from plant remains, no coal means that there were simply no plants to become a source of coal. The great Permian forests were gone. No plant material meant that herbivores were devastated by these conditions.

Figure 20.12  Examples of Permian insects that vanished with the rest of the Permian life forms. (A) The

Permian flying insect Dunbaria fasciipennis, preserved with original color patterns in its wings. (B) Meganeuridae, one of the largest insects ever to have lived, with a wingspan of over a foot! (A courtesy of Wellcome Images, https:// commons.wikimedia.org/wiki/File:Dunb​aria_​ fasci​ipenn​is_Ti​llyar​d_192​4.jpg​; B courtesy of Ghedoghedo, https://commons.wikimedia. org/wiki/File:Meganeuridae_indetermined. jpg.)

20.4  The End-Permian Extinction: The Great Dying

519

Figure 20.13  The articulated skeleton of Sclerocephalus haeuseri, a Permian labyrinthodont amphibian. (Adapted

from Dr. G. Bechly, https://commons. wikimedia.org/wiki/File:Meganeuridae_ indetermined.jpg.)

Figure 20.14  This Permian Gorgonopsid, Sauroctonus parringtoni, is a non-mammalian synapsid, one of many synapsids that went extinct in the Permian–Triassic extinction. (Courtesy of H. Zell, https​://

co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=12​42607​3.)

Figure 20.15  (A) Cynodonts such as this Exaeretodon, form the group ancestral to all mammals, including humans. Cynodonts

Vertebrates: Among vertebrates, the giant amphibians that had dominated the landscape completely disappeared (Figure 20.13). Many therapsids, those organisms belonging to the group that would eventually give rise to mammals (Figure 20.14), also went extinct. Only two lineages of the once-abundant “mammal-like reptiles” survived; the widely dispersed dicynodonts (Figure 20.15B) like Lystrosaurus, and the cynodonts (Figure 20.15A), which, although less widespread, were ultimately more successful, because they left living descendants—the mammals. Diapsids: Many diapsid reptiles also went extinct, but at least two groups remained: the pseudosuchians (crurotarsans), and the Avemetatarsalia (ornithodirans). The number of species within these groups were greatly reduced, but enough remained to ensure that dinosaurs would eventually rise to become dominant. The extinction was devastating. The world was almost sterilized, and took 10 million years to repopulate. When ecosystems were re-established, the taxa that diversified into the empty ecological space were very, very different from their Permian predecessors.

passed through the P–T extinction, and went on to diversify, giving rise to the first true mammals in the Triassic. (B) This dicynodont, Placerias hesternus, also survived the P–T extinction and went on to dominate the herbivore niche in the Early Triassic. (A courtesy of CT Snow, https://commons.wikimedia.org/ wiki/File:Cynodont.jpg; B adapted from F. Kovalcheck, https://commons.wikimedia. org/wiki/File:Plac​erias​_at_t​he_Ra​inbow​_Fore​ st_Mu​seum.​jpg.)​

520

CHAPTER 20    How Do We Know about Extinctions?

Figure 20.16  Prestosuchus is a rauisuchid, an archosaur related more closely to modern crocodiles than to dinosaurs (a pseudosuchian). This

group was successful and widely distributed after the P–T extinction event, and only with its extinction did dinosaurs rise to ascendency. (Adapted from V. Smith, https​ ://co​mmons​.wiki​media​.org/​w/ind​ex.ph​p?cur​ id=29​36268​7.)

20.4.3 Extinction Recovery The gradual return of complex systems to terrestrial environments saw one major change over life in the Permian. Although the Permian landscapes were dominated by the large and diverse amphibians, the climate and continents of the Triassic were much drier than before. Amniotes, those animals with an egg surrounded by protective membranes (and often a hard shell) were favored in the harsh, dry conditions that existed in the interior of Pangea. The dinosaurs were among the groups that emerged in the Late Triassic, after the recovery began, but they remained bit players, moving in the shadows of the pseudosuchians that rose to dominance. Pseudosuchians divided into many groups that varied greatly in lifestyle and habitat—some were even herbivorous! Some evolved into fast-moving, bipedal animals, and many were larger than their early dinosaur competitors. The successful rauisuchians (Figure 20.16), a group of pseudosuchians with an upright gait, filled the terrestrial predator niche that would later be occupied by theropod dinosaurs. Many different groups of pseudosuchians are found in Triassic deposits of eastern North America. Relatives of modern lizards also appear here, although their forms were varied and, in some cases, quite bizarre. The first pterosaurs took to the skies after the P–T event and were the first vertebrates to do so. Similarly, the giant reptiles that would fill the barren seas—the ichthyosaurs, plesiosaurs, and mosasaurs, first appeared during the slow recovery from the great extinction. The cynodonts of the Permian gave rise to the lineages that would become mammals. But for millions of years, these new fur-bearing creatures would, like the dinosaurs, remain in the background; small and nocturnal, but accruing adaptations that would greatly favor their kind later in time.

20.4.4 The Emergence of the Dinosaurs The dinosaurs, although much smaller than they would eventually become, had already developed key innovations that marked them as dinosaurs, but they did not yet outcompete the much more successful crocodiles! Although low in abundance, by the Late Triassic, dinosaurs had already divided into the two main lineages—ornithischians and saurischians, both of which appeared at roughly the same time. Almost simultaneously with the appearance of the ornithischians and saurischians, we see that herbivory had evolved—not just once, but twice, independently (see Chapter 15), from a carnivorous ancestor. The first recognized dinosaurs, Herrerasaurus and Eoraptor were both carnivores, but the most basal ornithischian, and all of its descendants—the whole lineage—were herbivorous. On the saurischian line, the earliest sauropodomorph was also herbivorous.

20.5  Dinosaurs Get their Chance: The End-Triassic Extinction

Triassic saurischians included the earlier forms, Herrerasaurus and Eoraptor; the tiny coelophysids, and the larger, herbivorous Plateosaurus. Triassic ornithischians like Lesothosaurus were also small and bipedal, but already showed a hint of ornithopod traits. If the dinosaurs were just background players in the Triassic, what enabled them to finally take center stage and rule for the rest of the Mesozoic? The answer to that is: yet another mass extinction event.

20.5 DINOSAURS GET THEIR CHANCE: THE ENDTRIASSIC EXTINCTION After reading this section you should be able to… • State the most likely cause of the End-Triassic extinction. • Discuss how the rifting of Pangea caused the End-Triassic mass extinction. • Identify organisms that went extinct and groups that diminished at the End Triassic. • List key survivors of the End-Triassic extinction.

It took about 10 million years for organisms to emerge after the End-Permian extinction, and to diversify to levels approximating those of the Permian, filling the many niches that were left vacant by that catastrophic event. But then, after about 50 million years (about 200 Ma), the world underwent another mass extinction that would eliminate 80% of species on the planet. This one separated the Triassic and Jurassic, and marked a major change for dinosaurs in particular.

20.5.1 What Caused the End-Triassic Extinction? The end of the Triassic Period saw the return of a familiar killer—flood basalts. Remember that at the end of the Paleozoic Era, the continents had all joined to form the supercontinent Pangea. During the Triassic Period, changing dynamics in the Earth’s mantle sent plumes of superheated rock toward the surface that would begin to tear the supercontinent apart. As rifts began to appear, the hot mantle released widespread flood basalts across the surface of the giant landmass. This process has repeated many times in earth’s history, and can even be observed today in the East African Rift Valley (Figure 20.17), where eastern Africa is tearing away from the rest of the African continent. These Triassic flood basalts would eventually cover 4 million square miles, and the resulting rocks can be found today in the northeastern United States, Brazil, Europe, and northwestern Africa. The presence of these rocks, from the same source and time period, is one of the strongest pieces of evidence that all of these continents were once joined together, before Pangea split and they became separated by the Atlantic Ocean. Today, you can see remnants of these basalts if you take a trip to New York. They form the Palisades, across the Hudson River from New York City (Figure 20.17C). Although not as extensive as the earlier flood basalts of the End-Permian Siberian Traps, those of the End-Triassic had similar devastating effects. Volcanic outgassing resulted in at least double, and possibly triple the concentrations of atmospheric CO2 from previous levels. As we’ve seen before, this led to atmospheric and ocean warming, a decrease in oxygen in the oceans, ocean water acidification, and widely fluctuating sea levels. These effects alone can be devastating for life, but it is also

521

522

CHAPTER 20    How Do We Know about Extinctions?

Figure 20.17  (A) Map showing the occurrence and extent of a modern rift valley, as East Africa begins to separate from the rest of the continent. This is accompanied

by deep depressions, surrounded by steep walls of rock (B) as in today’s Middle East, as the continent stretches apart. (C) A similar feature, the Palisades of the Hudson River Valley, a remnant of the rifting of North America and Europe. (A courtesy of Redgeographics, https://commons.wikimedia.org/wiki/ File:MapGreatRiftValley.png; B courtesy of Zairon, https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=39​19619​9; C courtesy of CrankyScorpion, https://commons. wikimedia.org/wiki/File:Pali​sades​_Sill​_from​ _Pali​sades​_Park​way.j​pg.)

thought that aerosols (in the form of volcanic ash) released during these eruptions would have blocked the sun’s heat from reaching the Earth’s surface. This would have led to geologically brief periods (hundreds of years) of cooling, followed by thousands of years of intense heating. These periodic cooling events would have made surviving the rapidly changing climate even harder. As with most extinctions, some have suggested an extraterrestrial event, but a crater both large enough and of the right timing to cause such an extinction has not been identified.

20.5.2 Which Organisms Went Extinct? Although not quite as devastating as the End-Permian event, this one took a greater toll on terrestrial animals than on marine animals. Those marine organisms hit hardest again included the corals, which almost perished completely, and bivalves, which lost about 50% of their diversity. Conodonts (eel-like organisms that arose in the Cambrian) were wiped out after more than 300 million years of success. Giant ichthyosaurs were also hit hard, never again achieving the diversity and success that they saw in the Triassic. Most groups of fish, however, made it through relatively unscathed. What might have caused this disparity in the survival of these marine groups? It is the End-Triassic event that cleared the way for the true ascendency of the dinosaurs, because the group that suffered major losses were their competitors—the pseudosuchians. The three major lineages of crocodiles that survived the End-Permian extinction were reduced to one lineage by the End Triassic, and that one group was greatly reduced in diversity and distribution. Today, Crocodylia—the alligators, crocodiles, caiman, and gharial—are all that remain of this large, successful, and diverse group that once kept dinosaurs in the shadows. The remaining giant amphibians that survived into the Triassic did not survive this event, nor did most of the synapsids. Almost all of the successful dicynodonts disappeared forever in the End-Triassic event, although fragmentary evidence may hint at the possible survival of one lineage as a Lazarus taxon in Australia. All that remained of the once widespread synapsids were tiny and primitive (but true) mammals (Figure 20.18). We don’t know why the dinosaurs were able to survive the End-Triassic mass extinction with few casualties whereas the pseudosuchians lost great

20.5  Dinosaurs Get their Chance: The End-Triassic Extinction

523

Figure 20.18  A life reconstruction of one of the oldest known “true” mammals, Juramaia sinensis, from China. This shrew-sized animal probably

didn’t provide much competition for the emerging dinosaurs. (Courtesy of N. Tamura, https://commons.wikimedia.org/ wiki/File:Juramaia_NT.png.)

numbers, but one proposal is that the unique metabolic strategy of the dinosaurs may have allowed them to cope with the drastic temperature fluctuations of the End Triassic.

20.5.3 Extinction Recovery What we see in the dinosaurs after the End-Triassic mass extinction is the true “Jurassic Park”. Almost all lineages of dinosaurs show a rapid increase in body size—all were bigger than their Triassic precursors. Was this strictly the opening of new habitats and reduction of competition that accompanied the loss of major groups of pseudosuchians? Regardless of the ultimate causes, we finally see the dinosaurs rise to ascendency. They are now the dominant land vertebrates, with more species and greater abundance than any other group. Further, throughout the remainder of their reign, there were really no other significant competitors. It is here, after we move into the Jurassic, that we finally see the origin of many dinosaur groups that should now be familiar to you (Figure 20.19). There is no Tyrannosaurus rex, and no Triceratops, but it is during the Jurassic that the giant sauropods reach their full size and distribution. Carnivorous dinosaurs, including Dilophosaurus and allosaurs like Carcharodontosaurus, and, of course, Allosaurus in North America, rise to dominance. These carnivores were (mostly) smaller than T. rex, and some data suggest that many of these theropods may have hunted in packs—that level of cooperation would be needed for feasting on herds of giant sauropods! Ornithischians also diversified greatly in the Jurassic. Here we see the first appearance of the stegosaurs and other thyreophorans. Maniraptoran dinosaurs also first appeared in the Jurassic, and included the densely feathered and very bird-like Anchiornis (Figure 20.20, see also Chapter 19). The Jurassic is also when the first avialan appears (the first one we have fossil evidence for, anyway)—Archaeopteryx, the fossil that changed our perceptions about birds, and about dinosaur evolution.

Figure 20.19  Two Allosaurus individuals eat from the carcass of a Diplodocus. These are species that rose to

prominence during the Jurassic, long before T. rex or Triceratops evolved. (Courtesy of M. Hallett.)

524

CHAPTER 20    How Do We Know about Extinctions?

Figure 20.20  The Jurassic saw the origin of many evolutionary innovations including the earliest complex feathers in multiple specimens of Anchiornis huxleyi (A) and other maniraptorans, and the probable origin of archosaurian flight in the earliest bird, Archaeopteryx lithographica (B). (A adapted from Bjoertvedt, https://commons.wikimedia.org/

wiki/File:Anch​iorni​s_hux​leyi_​-_mid​dle_j​urass​ic_Li​aonin​g_IMG​_5202​_Beij​ing_M​useum​ _of_N​atura​l_His​tory.​jpg; B courtesy of J.L. Amos, public domain.)

20.6 THE DINOSAUR REIGN ENDS: THE CRETACEOUS–PALEOGENE MASS EXTINCTION After reading this section you should be able to… • State three possible causes for the Cretaceous–Paleogene extinction. • Outline the evidence for an impactor at the Cretaceous–Paleogene boundary • Identify organisms that went extinct at the end of the Cretaceous.

The Jurassic ended with a whimper, compared with the End-Permian and End-Triassic mass extinctions, but many important dinosaur groups mysteriously disappeared, only to be replaced yet again by others that occupied similar niches. Like all the other divisions on the geological time scale, this one too is marked by the loss of many groups of organisms, but particularly noticeable were the non-avian dinosaur groups that vanished forever at this point in time. And, like other extinction events, this one also does not have a definite cause. But it ushered in the true dinosaur renaissance. The Cretaceous Period (145–66 Ma), saw the peak diversity of the Dinosauria. Although the largest of the theropods, including T. rex, lived during the Cretaceous, the giant sauropods were replaced (at least in North America) by smaller but more diverse hadrosaurs and ceratopsians as the dominant herbivores, and in many lineages, there was a trend toward decreasing size. What changed, so that the Earth could no longer support these most massive land animals of the Jurassic? Or was it the dinosaurs that changed? The Cretaceous, like the Triassic and Jurassic, continued the trend of faunal turnover, and we see some distinct patterns emerge within Dinosauria. It is important and timely to remember that although the occupants may change, the niches remain the same, and this is clearly reflected in the Jurassic–Cretaceous transition. The big carnivore role, filled by Ceratosaurus, Allosaurus, and others in the Jurassic, was occupied in the Cretaceous by the much larger Spinosaurus, Giganotosaurus, Tyrannosaurus rex, and others. In the northern continents (i.e., North American and Eurasia), the dominant herbivore role changed from prosauropods in the Triassic, to sauropods in the Jurassic, to the hadrosaurs and ceratop-

20.6  The Dinosaur Reign Ends: The Cretaceous–Paleogene Mass Extinction

sians in the Cretaceous. These dinosaurs had advanced dental batteries, massive bony protrusions for the insertion of jaw muscles, and complex chewing mechanisms facilitated by moveable joints in their skulls. Gone were the simple, peg-like teeth, weak jaws, and relatively tiny heads of the sauropods—at least from North America and Eurasia. Sauropods were reduced in diversity but lasted throughout the Cretaceous across South America, Africa, Australia, and Antarctica. It appears that the emerging herbivorous dinosaur adaptations followed changes to plant textures and diversity. It was, after all, in the Cretaceous that we saw a major innovation in flora: the onset of the angiosperms, or seed-bearing, flowering plants. Then, it happened again. The Cretaceous Period ended with a bang—literally.

20.6.1 What Caused the Cretaceous–Paleogene Mass Extinction? The End-Cretaceous extinction goes by a variety of names, and you may have heard it referred to as the K–T extinction event. The “K” stands for Kreide, the German word for Cretaceous, and “T” refers to the Tertiary, the period that marks the beginning of the Cenozoic Era. However, more recently, the Tertiary (from ~66 Ma to 2.5 Ma) has been replaced by the Paleogene (66 Ma to 23 Ma) and Neogene periods (23 Ma to 2.5 Ma). Thus, the End-Cretaceous extinction is now more accurately referred to as the Cretaceous–Paleogene, or K–Pg, extinction. It will probably take a while for the “K–T extinction” term to be replaced in popular culture and even scientific literature, but you should know that K–T and K–Pg are two names for the same event. So, what caused this mass extinction? Like the other events, many ideas have been put forward since we realized the depth and extent of this event. Some of the early ideas were (in retrospect) quite amusing. For example, it was proposed that dinosaurs got so big they could no longer support themselves under their own weight. What are the obvious problems with this hypothesis? Another popular idea was that the mammals were faster and smarter (because we are mammals so they had to be better suited to take over the world, right?) and simply out-competed the slow, sluggish, and stupid dinosaurs. A corollary to this was that mammals, as they diversified, simply ate the dinosaurs out of existence with a diet focused on dinosaur eggs! The problem with these ideas is that mammals and dinosaurs co-existed for the entire 150-million-year reign of the dinosaurs. Thus, the idea that mammals caused the sudden demise of all non-avian dinosaurs everywhere on the planet just doesn’t fit the evidence. The question of what killed the non-avian dinosaurs is one that has fascinated researchers (and cartoonists) for a long time (Figure 20.21). There must have been a reason that, except for birds, this very successful, diverse, and widespread group isn’t around any longer. Probably the most famous and well-known explanation for the End-Cretaceous extinction is an extraterrestrial impact—i.e., an asteroid that collided with the Earth. Although extraterrestrial events have been proposed for each of the extinctions affecting dinosaurs, the End-Cretaceous event is the only one to have multiple lines of direct and compelling evidence for such an impact, linking it to the ultimate demise of the non-avian dinosaurs. One of the most compelling pieces of evidence is the abundance of the element iridium in clay layers dated to the K–Pg boundary (Figure 20.22), which was first noted by Luis and Walter Alvarez. Iridium is extremely rare in the Earth’s crust, but it is common in

525

526

CHAPTER 20    How Do We Know about Extinctions?

Figure 20.21  One idea (not supported by data!) put forth to explain the disappearance of the dinosaurs.

(Courtesy of Dan Regan.)

Figure 20.22  This thin white band (arrows) represents a layer of clay that contains high concentrations of the element iridium (Ir), which is very rare on Earth but occurs at high levels in asteroids. Iridium has been detected in

rocks worldwide of the same age, dating to approximately 66 million years ago. (Courtesy of E. Zimbres, https://commons. wikimedia.org/wiki/File:K-T-boundary.JPG.)

comets, meteors, and asteroids. As recently as the 1980s, the discovery of abnormally high levels of iridium in the clay layers separating Cretaceous and Paleogene sediments—not just in some places, but everywhere on the planet—led to the first well-supported hypothesis of an extraterrestrial cause for this mass extinction. In rocks of the same age as the iridium layer, we see another feature that is also associated with an impact. Many rocks that date to this layer show quartz crystals that have had their crystal structure rearranged along planes, which appear as sharp lines under microscopic examination (Figure 20.23). This type of crystal rearrangement can only occur in quartz when very intense heat and pressure are applied; it is called “shock metamorphism”. Like the iridium, this “shocked quartz” appears worldwide at the K–Pg boundary. The planet-wide iridium anomaly and shocked quartz at the K–Pg boundary was strong evidence for an extraterrestrial impact. However, if an extinction-inducing asteroid impact had occurred, then we would expect a very large crater to exist somewhere on the planet. When the

20.6  The Dinosaur Reign Ends: The Cretaceous–Paleogene Mass Extinction

527

Figure 20.23  (A) Photomicrograph of a grain of shocked quartz, showing the planar rearrangement of crystals that appear as regular lines in normal light. Under polarized light (B),

iridium and shocked quartz were first discovered and the asteroid hypothesis proposed, such a crater had not been discovered. For ten years, debate raged in the paleontology and geology communities—surely a body large enough to cause worldwide destruction, and the vanquishing of an entire group of successful vertebrates, would leave a crater. But despite active attempts around the world to do so, none had been found.

this pattern becomes even more apparent. This pattern only occurs under elevated temperatures and extremely high pressures, such as would occur at the site of an asteroid impact. (A courtesy of M. Schmieder, https​://co​mmons​.wiki​media​.org/​ w/ind​ex.ph​p?cur​id=74​25503​; B courtesy of G.A. Izett (https://commons.wikimedia.org/ wiki/File:820qtz.jpg.)

Unbeknownst to the K–Pg extinction scientists at the time, two geophysicists working in the oil industry had presented evidence in 1981 for an impact crater on the edge of the Yucatan Peninsula in Mexico. They had discovered the buried structure through magnetic and gravity anomaly maps (which show deviations in magnetism or gravity from expected values) used for oil exploration (Figure 20.24). It took until 1990, however, when a reporter who had covered the crater story nine years earlier got the geophysicists talking to the geologists. When the two groups compared notes and data, the K–Pg event could be directly linked to an impact from space. At last, a mass extinction had a “smoking gun”—direct evidence of an impact! The size was right (over 90 miles in diameter, big enough to accomplish the level of destruction observed), the age was right (isotope dating placed it at 66 million years ago), and its rim contained shocked quartz. The crater, known as the Chicxulub impact crater, is named for the Mexican town now located at its center. Proponents of the impact-extinction hypothesis lay out several effects of the impact that, combined, would have led to global extinctions on a scale large enough to bring the ~150 million-year reign of the non-avian dinosaurs to an end. Immediately following impact, they proposed that massive tsunamis and shockwaves would spread at supersonic speeds across the earth. The impact to predicted to have hit with the force of over a billion atomic bombs, inducing massive volcanic eruptions, earthquakes, and landslides, all contributing to the collapse of the continental shelves that contain most marine diversity. Superheated chunks of rock particles, called ejecta, would be launched high into the atmosphere, Figure 20.24  (A) Gravitational anomaly map created using soundwaves, which confirms that an extraterrestrial body hit our planet.

(B) Rendering of the location and size of the crater revealed by map in A. The iridium layer and this anomaly coincide in the rock record at precisely in time, and together with shocked quartz, provide strong support for an impact event. They provide a cause, and a location, for the K–Pg mass extinction. (A courtesy of the United States Geological Survey, public domain; B courtesy of Dementia (https​ ://ww​w.fli​ckr.c​om/ph​otos/​45617​735@N​ 07/4420307678.)

528

CHAPTER 20    How Do We Know about Extinctions?

and when these fell back to earth, would cause global wildfires fueled by the higher oxygen levels in the atmosphere over today. At this boundary layer, we see large deposits of soot that may be the remnants of these wildfires. Following the impact, smaller particles of soot and debris are hypothesized to have remained suspended in the atmosphere for years, blocking sunlight enough to shut down photosynthesis, putting an end to the many plant groups and the large herbivorous dinosaurs that depended on them, and cooling the planet enough to cause catastrophic ecological change. This scenario seemed sufficient to explain the demise of the non-avian dinosaurs and the mass extinction at the end of the Cretaceous. But was this single event really enough to completely eliminate such a widespread and successful group? This is a question that is still hotly debated. Geological evidence shows that another extraterrestrial body, about two-thirds the size of Chicxulub, hit Earth during the Triassic, but there is no evidence of an extinction event in the fossil record. So was the body that formed the Chicxulub crater just enough larger to induce a global extinction? And if not the impact, then what other evidence is there to explain the K–Pg mass extinction? Like the End-Permian and End-Triassic events, the End-Cretaceous is also correlated to extreme volcanism, again evidenced by flood basalts. The Siberian Traps can be dated to the end of the Permian, but the Deccan Traps, a smaller, yet still massive volcanic formation that covers a large portion of India, has been dated to the K–Pg boundary. As previously discussed, massive and prolonged volcanism would have devastated habitats, spewing particles and aerosols that block the sun. The global cooling (“nuclear winter”) that accompanied this atmospheric disaster was followed by rapid greenhouse effects as CO2 levels rose in response to expanding volcanism. This would be accompanied by increasing acid rain, which would result again in a significant lowering of the pH in terrestrial and marine waters, as it had after the End-Permian event, making these environments increasingly hostile to life. And, if the plant life was harmed, animals would soon follow. But, as if an impact from a large space body and massive volcanism were not enough, at the end of the Cretaceous we see another event that might have provided the third in this “triple whammy” that greatly affected life on the planet. If you remember from Chapter 2, the continents and oceans are dynamic, and for much of the age of dinosaurs, a massive shallow sea covered much of these continents, at least in North America. An ocean covering what is now Kansas, Minnesota, and the heartland of the United States began to recede as sea levels dropped due to uplift of the continent caused by convergence along the western edge of the continent. As a result, the dinosaurs living near the coasts of these interior shallow seas would have experienced harsher winters and hotter summers than when the seas moderated the climate. A rapid regression of sea levels would also have drastic consequences for marine organisms living on the relatively shallow continental shelves. But rapidly regressing sea levels would not explain the extinction of groups like the ammonites who could survive out in the deep ocean, and these also went extinct with the dinosaurs. How can we know for sure what killed the non-avian dinosaurs? There is irrefutable evidence for global climate change—the entire Mesozoic, when the dinosaurs ruled, had elevated CO2 levels in the atmosphere that contributed to a warm and humid world. But geological evidence in the form of oxygen isotope data shows that the Cenozoic, immediately after the event, was cooler, drier, and much more variable, encompassing extremes of heat and cold, aridity and humidity. Because the K–PG,

20.6  The Dinosaur Reign Ends: The Cretaceous–Paleogene Mass Extinction

like the other mass extinctions described here, did not single out one particular group or organism—marine organisms and terrestrial ones were equally affected, both vertebrate and invertebrate animals went extinct, and plants were likewise affected—more than one single cause was probably to blame. The evidence for an extraterrestrial event at this K–Pg boundary is robust, but so is evidence for massive flood basalt volcanism and declining sea levels at the end of the Cretaceous. Perhaps it was bad luck (for the dinosaurs) that all of these events occurred at the same time. Maybe they could have survived one, but there is no doubt that these events, in combination, would have had devastating impacts on life. Perhaps many communities were already weakened by the lowering sea levels and climate change resulting from increasing volcanism; the impact then served as the final death blow. Furthermore, it has been shown that impacts can induce volcanism, and some evidence suggests that the Chicxulub impact may have greatly increased the degree and rate of volcanism that resulted in the Deccan traps, making the two a deadly combination.

20.6.2 Which Organisms Went Extinct? The End-Cretaceous event, like the others before it, was not selective. There were no obvious characteristics one could assign to the groups that would predict their extinction or survival. Although the end of the Cretaceous is synonymous with the end of all of the non-avian dinosaurs, dinosaurs were not the only creatures affected. About 76% of all species were driven to extinction. There is still some mystery about this End-Cretaceous event. Dinosaurs were present, successful, diverse, and widespread, occupying every niche and every continent, until the very end of the period, although some evidence suggests dinosaur diversity was decreasing the last 5–10 million years of the period. Their extinction was simultaneous (geologically speaking), and worldwide. Not a single non-avian dinosaur survived, even though other organisms that had long co-existed with them did. We have no dinosaur fossils that can be reliably dated to time periods later than the Cretaceous, even though we have many of their fossils from the latest Cretaceous and the preceding ~150 million years. The end of this long-lived lineage was abrupt and sudden. Besides the dinosaurs, several major vertebrate groups went extinct, including the last of the pterosaurs, the giant mosasaurs that rose to dominance in the oceans, and one entire group of birds, the widespread, speciose, and diverse enantiornithines. These disappeared without a trace, leaving no descendants. Despite the sudden and complete disappearance of many long-lived lineages, many groups of animals that co-existed with dinosaurs emerged from this event virtually unscathed, and seemed almost completely unaffected by the events that brought the dinosaurs to their abrupt end. Members of Crocodylia, as well as many groups of sharks and rays survived, while others disappeared. Some amphibians, known today as indicator species for environmental collapse, went extinct, but many survived. Many groups of lizards and snakes survived and radiated. The champsosaurs—crocodile-like diapsids that lived in the Cretaceous— survived the K–PG event only to go extinct at a later time. Turtles, of course, survived and flourished. All major groups of mammals (monotremes, marsupials, and placentals) survived this event, though each group lost some species and saw changes in distribution. What patterns do we see in which groups survived and which went extinct? Land animals that were relatively big—somewhere around 50–100 lbs. (~25 kg) and larger—went extinct, but smaller lineages also disap-

529

530

CHAPTER 20    How Do We Know about Extinctions?

peared, as well as every single species of enantiornithine bird (Chapter 19). Why? Why did the ornithurine birds, background players throughout their entire history until this point, survive, but not the more successful enantiornithines? One pattern we can detect seems to indicate that both size and physiology may have played a role. Relatively big, cold-blooded animals like the modern crocodiles survived. Small and warm-blooded animals (mammals and ornithurines) also survived. But, big animals with an intermediate or endothermic physiology (like the non-avian dinosaurs) did not survive, nor did the smaller animals like enantiornithines, that perhaps were elevated in metabolic rates, but not quite to the same level as modern endotherms. Organisms that photosynthesized were also severely impacted, including plants and algae. This had a direct effect on organisms that relied on photosynthesizers as their food source. Surviving mammals were predominantly omnivorous or insectivorous, with many herbivorous and carnivorous mammals going extinct. The omnivorous mammals could survive by incorporating variety into their diets, eating insects and seeds. A similar trend is seen in surviving birds. It also seems that freshwater communities were less impacted than marine, perhaps because freshwater environments expanded as the sea levels receded, and continental surface waters had longer paths to the oceans, creating larger drainage basins.

20.6.3 Extinction Recovery For about the first 5–10 million years of the Cenozoic (during the Paleogene), life struggled to regain diversity. The fossil record from this time period is poor, and the sediments show a lack of evidence for diverse plants, invertebrates, or freshwater species, as in other events. But, just as was seen after the End-Permian event, as it recovered, life on this planet looked very, very different than it had in the Cretaceous. Mammals and avian dinosaurs gradually moved to fill the empty niches left by the dinosaurs and marine reptiles.

20.7 THE POST-CRETACEOUS WORLD After reading this section you should be able to… • Argue for the importance of studying mass extinctions.

No extinction event we have discussed in this chapter left the planet completely lifeless. Thus, after each of them, life went on. Life changed dramatically at the end of the Cretaceous, just as we saw with each of the previous extinctions. After the Cretaceous, there were no more dinosaurs, plesiosaurs, or pterosaurs. Instead, we see the rise of mammals and the dominance of birds. Interestingly, beyond the astonishing absence of these major groups, the rocks indicate that Earth’s climate was not much different after the K–Pg extinction than before. The climate after the initial cataclysm was much as it had been in the Cretaceous. Similar to other global mass extinctions, many niches remained unfilled for significant periods of time. Slowly, though, the rocks record a radiation of new mammals and birds. From tiny, nocturnal players relegated to the background, mammals spread to occupy the niches once held by the mighty dinosaurs—and more. Never again will we see the giant sauropods. The largest herbivores after the Cretaceous were mammoths and then elephants; familiar, but not quite as awe-inspir-

20.7  The Post-Cretaceous World Figure 20.25  After the extinction event, many niches once held by the dinosaurs were filled by other organisms—usually mammals, but in this case, the dinosaur niche was filled by—a dinosaur! These large, fast, predator birds were the terror of the Cenozoic; hence their nickname, “terror birds”. (A courtesy

of M. Schweitzer, photographed at the Smithsonian Institution; B courtesy of N. Tamura, https://commons.wikimedia.org/ wiki/File:Paraphysornis_BW-2r.jpg.)

ing! Instead of giant predatory theropods, today we have lions…and tigers…and bears! Smaller and four-legged, but perhaps equally effective. Where there once were hadrosaurs and ceratopsians, gomphotheres and giant sloths filled the Cenozoic herbivorous niche, followed by horses, elk, deer, and zebras. Sharks preceded and outlasted the dinosaurs and are still thriving today. But in the oceans, instead of mosasaurs, ichthyosaurs, and plesiosaurs, sharks are preying on whales and dolphins. Life has found a way. One point of interest in the post-Cretaceous world is the appearance of giant, predatory, flightless birds known as Phorusrhacidae, or terror birds. These birds were bigger than a human, and probably preyed on the small horses and other herbivores just appearing on the scene—filling the empty theropod niche. Some terror birds reached almost 10 feet in height and were the apex predators of South America (Figure 20.25). In a way, dinosaurs would continue their reign through the Cenozoic Era. These large carnivorous birds would rule South America until the closing of the isthmus of Panama some 2.6 Mya. This land bridge would allow the introduction of mammalian competitors, which would eventually drive the terror birds to extinction around 1.8 Mya. Today, believe it or not, dinosaurs still reign supreme. Although smaller than comparable mammals, they are twice as speciose, and equally widespread. By any measure of success, the avian dinosaurs are still the dominant terrestrial vertebrates! What are the implications of all these extinctions? What do these data tell us about our world today? One thing we can say with certainty as we walk through the history of our dynamic, tectonically active planet, is that global change is the norm, not the exception. The planet has warmed and cooled. Landmasses have emerged and become submerged; come together and rifted apart. Polar ice has formed, expanded, retracted, and disappeared, and mountains have risen and weathered away. The atmosphere has changed drastically in the amount of both CO2 and oxygen many times, and ocean water chemistry has changed radically over time. But unlike the dinosaurs, we can see and measure and predict these changes, and so perhaps prepare for them. But are we? Some scientists think that we are entering a sixth mass extinction, and this one has a cause unlike all of the others. In just a few centuries, humans have left their mark on the planet, ushering in unprecedented changes—unprecedented in the rapidity of their occurrence, at least as far as we can tell with the limited resolution of the geological record. Because geological eras are marked in the fossil record by the turnover of species, perhaps we have earned the right to our own epoch—the Anthropocene.

531

532

CHAPTER 20    How Do We Know about Extinctions?

Figure 20.26  A scene from your window (if there was one) from 70 million years ago might look very much like the image in (A); dinosaur communities interacting in their world, surrounded by brightly colored, toothed enantiornithines that made their home in the tall cycads and sequoias. But a scene from

50,000 years ago (B) would look totally different! Tall mountains where there hadn’t been any, true conifers, and the true birds that look so familiar would visit the lumbering wooly mammoth and tease the saber-tooth cats hunkered down in tall grasses, ready to ambush unsuspecting prey. What might you see out that same window, a million years from now? (A courtesy of ABelov2014, https://commons. wikimedia.org/wiki/File:Kaiparowits_fauna. jpg; B courtesy of the National Park Service, nps.g​ov/wh​sa/le​arn/n​ature​/foss​ilize​d-foo​ tprin​ts.ht​m.)

Life has changed. Life is changing. Life will continue to change. Extinctions—local or global, background or mass extinctions, all are part of life, part of this planet, and a critical part of shaping our future as surely as it has shaped our past. However, current research is revealing that the human overprint on natural patterns is far outpacing anything we have seen in the rock record of Earth’s past. Humans move more Earth material and cause more erosion than natural processes, and we are increasing atmospheric CO2 level at a rate not seen in Earth’s past, including the Paleocene–Eocene Thermal Maximum, an intense period of warming some 55.5 million years ago. As we have seen, rapid adjustments to Earth’s thermostat can have dire consequences for much of the biosphere. Will human influence be the tipping point toward another mass extinction? It is imperative to tease apart the changes brought about by natural cycling from those induced by humans, and to compensate only for the damage we have done without, in the effort, pushing the planet over the other edge. This earth represents 4.6 billion years of experiments. The data to evaluate our role and plan our future resides in the rocks. They simply need to be interpreted. Our future course must be informed by the past. We cannot, nor should we, arrest those changes that have been part of our planet forever. But we can, and should, compensate for our own influence. Hence, we should not try to resurrect extinct dinosaurs (a la Jurassic Park) even if it were possible, but if we are able to prevent the demise of species that have been brought to near extinction by human activities, that is an effort worth perusing. If you looked out your window 70 million years ago, you might have seen a scene like Figure 20.26A. If you looked out your window 40,000 years ago, your world might have looked like Figure 20.26B. Who knows what you might see, when you look out the window a million years from now? Life is change. It always has been, and it always will be. Extinction—even our own inevitable (but hopefully very, very distant) extinction—is part of that change.

20.8 WHAT WE DON’T KNOW There is still a mountain of work that is needed to fully understand not only mass extinction events, but also other smaller extinctions in Earth’s past. This is an area where the “what we don’t know” about mass extinctions could fill an entire book. Below are just a few general questions related to the unknowns behind mass extinctions.

20.8.1 What Were the Exact Causal Mechanisms for the K– Pg Mass Extinction (and All the Mass Extinctions)? While we have learned quite a bit about Earth’s major mass extinctions from studying the fossil record, no consensus on the cause has been reached for any of them. For the K–Pg, we know that a large impact from an extraterrestrial body was certainly a contributing factor, but there is still much contention as to what role the Deccan Traps volcanism may have played in the mass extinction that ended the reign of the dinosaurs.

20.8  What We Don’t Know

The K–Pg mass extinction is the only extinction event with confirmed evidence of an impactor, and is also the only mass extinction to occur after Pangea’s breakup. Questions to consider: • What role does the position of the continents play in mass extinctions? • Was the Chicxulub impactor alone capable of causing a planetary-wide mass extinction event? • Are there other impactors that we haven’t found evidence for that are related to the other mass extinctions or the many smaller extinction events in Earth’s history? • What allows an extinction event to impact both marine and terrestrial organisms? This likely involves some atmospheric connection, but what are the exact linking mechanisms?

20.8.2 What Makes Certain Species Likely to Survive a Mass Extinction Event? As we’ve seen, mass extinctions tend to affect species indiscriminately, killing off both marine and terrestrial species from a wide variety of habitats and niches. The history of life on Earth has been greatly shaped by those organisms that were able to survive extinction events. It was extinction events that allowed dinosaurs to rise to prominence and reign for 150 million years, and also led to their demise and the eventual rise of mammals and evolution of our own lineage. Questions to consider: • Do stressors associated with mass extinctions (e.g., climate change) affect organisms of different trophic levels differently? • How do communities (see Chapter 12) respond to extinction stressors like climate change? • Will understanding how organisms become extinct allow us to predict future extinctions accurately?

20.8.3 How Can Mass Extinctions and Other Extinction Events in Earth’s Past Inform the Present and Allow Us to Predict and Mitigate Anthropogenic Impacts on the Biosphere? Events like volcanism and impactors have been linked to mass extinctions, but they are the drivers of the actual stressors (or kill mechanisms) that include anoxia, global warming, and ocean acidification, all of which are linked to changes in atmospheric greenhouse gas concentrations. Anthropogenic factors are currently altering the geosphere and atmosphere, causing extant marine and terrestrial organisms to face some of these stressors, and driving discussions of a sixth mass extinction. Questions to consider: • Why have these stressors led to mass extinction in Earth’s history, while at other times they have not? • How can insight into the above question be used to guide human decisions and conservation efforts? • Are we in the midst of a sixth mass extinction, and if so, can we do anything to slow or stop it?

533

534

CHAPTER 20    How Do We Know about Extinctions?

CHAPTER ACKNOWLEDGMENTS We thank Dr. Greg Wilson for his generous review and suggested improvements to this chapter. Dr. Wilson is a Professor in the Department of Biology at the University of Washington.

INSTITUTIONAL RESOURCES Benton, M. J. (2003). When Life Nearly Died: The Greatest Mass Extinction of All Time. Thames & Hudson, London, UK. Brannen, P. (2017). The Ends of the World: Volcanic Apocalypses, Lethal Oceans and Our Quest to Understand Earth's Past Mass Extinctions. Harper Collins, New York, NY. Kolbert, E. (2014). The Sixth Extinction: An Unnatural History. Henry Hold & Company, New York, NY. University of California Museum of Paleontology. (2020, April 19), “Mass Extinction”. Understanding evolution https​: //ev​oluti​on.be​rkele​y.edu ​/evol​ibrar ​y/ art​icle/​0 _0_0​/mass​extin​c t_01​. Shubin, N. (2008). Your Inner Fish: A Journey into the 3.5-Billion-Year History of the Human Body. Vintage, New York, NY.

LITERATURE Barnosky, A. D., Matzke, N., Tomiya, S., Wogan, G. O., Swartz, B., Quental, T. B., Marshall, C., McGuire, J. L., Lindsey, E. L., Maguire, K. C., Mersey, B., and Mersey, B. (2011). Has the Earth’s sixth mass extinction already arrived? Nature, 471(7336), 51–57. Bond, D. P., and Grasby, S. E. (2017). On the causes of mass extinctions. Palaeogeography, Palaeoclimatology, Palaeoecology, 478, 3–29. Ceballos, G., Ehrlich, P. R., Barnosky, A. D., García, A., Pringle, R. M., and Palmer, T. M. (2015). Accelerated modern human–induced species losses: Entering the sixth mass extinction. Science Advances, 1(5), e1400253. Deenen, M. H., Ruhl, M., Bonis, N. R., Krijgsman, W., Kuerschner, W. M., Reitsma, M., and Van Bergen, M. J. (2010). A new chronology for the end-Triassic mass extinction. Earth and Planetary Science Letters, 291(1–4), 113–125. DePalma, R. A., Smit, J., Burnham, D. A., Kuiper, K., Manning, P. L., Oleinik, A., Larson, P., Maurrasse, F. J., Vellekoop, J., Richards, M. A., Gurche, L., and Gurche, L. (2019). A seismically in-

duced onshore surge deposit at the KPg boundary, North Dakota. Proceedings of the National Academy of Sciences of the United States of America, 116(17), 8190–8199. Harper, D. A., Hammarlund, E. U., and Rasmussen, C. M. (2014). End Ordovician extinctions: A coincidence of causes. Gondwana Research, 25(4), 1294–1307. McGhee Jr, G. R., Clapham, M. E., Sheehan, P. M., Bottjer, D. J., and Droser, M. L. (2013). A new ecological-severity ranking of major Phanerozoic biodiversity crises. Palaeogeography, Palaeoclimatology, Palaeoecology, 370, 260–270. Stanley, S. M. (2016). Estimates of the magnitudes of major marine mass extinctions in earth history. Proceedings of the National Academy of Sciences, 113(42), E6325–E6334. Thulborn, T., and Turner, S. (2003). The last dicynodont: An Australian Cretaceous relict. Proceedings of the Royal Society of London. Series B: Biological Sciences, 270(1518), 985–993. Wilkinson, B. H. (2005). Humans as geologic agents: A deeptime perspective. Geology, 33(3), 161–164.

INDEX Note: Page numbers followed by “f” refer to figures. Absolute dating, 46, 47, 49, 50

Absolute geochronology, 46 Accretion, 19 Acetabulum, 148, 148f, 149, 234 Acrocanthosaurus, 386f, 388f skeletal mount (cast) of, 217f Actinopterygians, 112 Active metabolic rate (AMR), 443 Aetosaur, 118, 118f, 232f African Rock Python (Python sebae), partial skeleton of, 142f Afrovenator, 15 Age of Conifers, 116 Age of Dinosaurs, 116 Cretaceous Period (145–65 Ma), 121–122 Jurassic Period (201–145 Ma), 120–121 Triassic Period (252–201 Ma), 116, 117–120, 117f Age of Mammals, 122 Age of Reptiles, 116 Alamosaurus sanjuanensis, 206 Alligator, 92; see also American alligator; Crocodile with arms and legs splayed, 449f femur, with fourth trochanter, 146f fleshed head, 330f with a hatchling, 434f homodont dentition in, 353f skull, 330f Alligator mississippiensis, skull of, 146f Allopatric speciation, 67 Allosauria, 216–217, 217f, 469 Allosaur tail vertebra, neural process of, 163f Allosaurus sp., 134f, 163, 212, 395, 397, 398, 523, 523f A. fragilis, 40, 400f articulated foot of, 400f vertebrae, ribs, and ilium of, 397f flesh reconstruction of, 230f, 330f fore- and hindlimb proportions in, 484f skeleton of juvenile Allosaurus, 397f skull (cast) of, 217f, 230f, 330f vertebrae, 401f Alpha (α) decay, 47–48 Alvarezsauria, 476, 476f Alveoli, 462, 462f Amargasaurus sp. A. cazaui, 202 skeletal mount of, 202f

American alligator (Alligator mississippiensis) compared with a hatchling, 434f skull of, 146f American antelope, 73 American black bear (Ursus americanus), heterodont dentition in, 353f American Museum of Natural History (AMNH) in New York, 13, 15 Ammonite cast, 270f Ammonite mold, 270f Ammonite shells, comparison of, 271f AMNH, see American Museum of Natural History in New York Amniote egg, 113, 142f, 514 Amniotes, 83, 84f, 113–115, 141–143, 515, 520 AMR, see Active metabolic rate Amur leopard, 308 hindlimbs of, 309f skeleton, 308f Anabolism, 440 Analogous trait, 83, 86 Anapsida, 143 Anatomical directional terms, 133–134 Ancestor 1, 82, 83, 83f, 84f Ancestor 2, 82, 82f Ancestral (basal) trait, 85 Ancestral characters, 82, 85 Anchiceratops, 181, 182f Anchiornis sp., 15, 315, 338, 484 A. huxleyi, 186, 454f, 501, 502f, 524f Andrews, Roy Chapman, 14, 421–422, 430 Angular unconformity, 43, 44f, 428f Animalia, 140, 490f Anisodactyly, 315, 315f, 484 in Archaeopteryx, 315f, 485f in tui bird (Prosthemadera novaeseelandiae), 315f, 485f Ankylosauria, 159, 160f, 164–165, 164f Ankylosaurid. 165 tail club of, 165f Ankylosauridae, 165 Ankylosaurs, 159, 161, 164–165, 336, 373, 455 Anning, Mary, 10, 11f Anomalocaris, 109, 110f Anoxia, 513, 514, 516 Antibiotics, 64 Antorbital fenestrae, 145, 238 Apatosaurus sp. A. ajax, 202

limb posture of, 205f pelvis, 190f Appalachian Mountains, 28, 111, 114 Appearance, of dinosaur, 325 colors and color patterns, 339 camouflage, 340–346 feathers/feather-likes structures in, 346 ornamentation, 333 ceratopsians, 334–335 ornithopods, 334 sauropods, 335–336 theropods, 337–339 thyreophorans, 336–337 reconstruction, 325–330 skin, 330–333 Appendicular skeleton, 132, 133f Aquilops americanus, 180 Arboreal locomotion, adaptations for, 314–316 Archaeodontosaurus, teeth from, 357f Archaeopteryx, 70, 70f, 243, 315, 473, 479, 483, 495, 501, 523 A. lithographica, 524f skeleton of, 484f anisodactyly in, 315f, 485f fore- and hindlimb proportions in, 484f tail feather attachment in, 479f Archelon, 230 shell of, 230f Archosauria, 144–146, 460, 497f simplified family tree of, 116f Archosaurs, 116, 118, 120, 146, 230–231, 321, 354, 463 lungs of, 463 skull of, 362f teeth of, 145 Argentinosaurus huinculensis, 206 Armored ornithischians, 159 Ankylosauria, 164–165 Stegosauria, 161–164 Arms of Citipati, 456f of Tyrannosaurus rex, 219f, 295–296, 297f, 321, 328–329, 329f Arthropleura, 113 Artificial selection, 61 Artiodactyls, 69 Aspidorhynchus, 243f Asteroids in the solar system, 20 Atomic mass, 47 Atomic number, 46–48

536

INDEX

Autapomorphy, 86, 91, 148, 482, 483 Autotrophs, 288–290 Avemetatarsalia, 116, 146–147, 208, 231, 234, 338, 346, 454, 491, 502 Aves, 92, 149, 487–488 Avialae, 482–485 defined, 483 Avialae and avian characteristics, 482 Aves, 487–488 Ornithothoraces, 485–486 Ornithurae, 486–487 Axial skeleton, 132 skeleton of a bat with, 133f Axis of symmetry, 132, 134 Background extinctions, 506, 508–509 Bacteria, drug-resistant, 64 Badger, 311 forelimbs of, 312f Bakker, Bob, 14 Bakker, Robert, 411 Banded iron formations (BIFs), 51, 106, 106f Barbs, 473, 474f Barbules, 473, 474f Barosaurus sp. B. lentus, neck of, 198f skeletal mounts of, 204f Barringer crater in Arizona, 4f Baryonyx, 216, 372 Basset hound, 304f skeletal forelimbs of, 305f Bat Mexican long-tongued bat, 491f skeleton of with axial skeleton, 133f with cranial skeleton, 133f wings of, 83–84, 85f, 235f Bay breasted warbler, 412f Behavior, of dinosaur, 375 footprint formation and preservation, 378–379, 378f, 379f footprint taphonomy, 379–381 hunting, 404 ichnotaxonomy, 390–394 individual tracks, 381–384 mass death assemblages, 394–395 paleopathologies, 396 disease, 402–404 injuries, 396–404 pathogens of dinosaur, 404 substrate, effects of, 379 trackways, 383–389, 384f, 390f Behrensmeyer, Kay, 15 Bergmann’s Rule, 279 Beta (β) decay, 47 β-keratin, 476, 502 Beta plus decay, 47 BIFs, see Banded iron formations Bighorn sheep, 175, 177–178 skull of, 179f Binomial nomenclature, 80 Biochemical sedimentary rocks, 37 Biofilm, 344–345 Biological environment, 278, 282 Biomechanics, of dinosaur, 301, 321 climbing, 314–316, 315f digging, 316–319 form and function, 302–305 giant claws, herbivorous Therizinosaurs with, 322 jumping, 319–321

running stability and efficiency, 311–314 stride length, adaptations that increase, 305–308 stride rate, increasing, 308–311 tiny arms, T. rex with, 321–322 Biopigments, 343 Biosphere, 285–292 Biostratigraphy, 44, 49 Biostratinomy, 257, 258 bloat, 260–261 rigor, 259–260 scavenging and predation, 261–262 trampling and weathering, 264–265 transport, 262–264 Bipedalism, 315 Bird, R. T., 380 Bird foot ornithischians, 166 Hadrosauridae, 171–173 Saurolophidae, 173–174 Styracosterna, 167–171 Bird-like Archaeopteryx, 70 Bird-like dinosaur, 70 Birds, 5, 149, 414–415, 441; see also Flight, origin of; Wings bones in forearm of, 492f evolutionary relationship with dinosaurs, 5 expressing a range of colors, 340f femur, 496f flight muscles in, 495f hummingbird eggs, 424f inhalation and exhalation cycles of respiration in, 463f, 495f legs of, 449f lung and respiratory system, 463 mummified bird foot, 383f pulley system in, 494 sexual dimorphism in, 410f temporal paradox of evolution of, 501–502 terror birds, 531, 531f and Wing Assisted Inclined Running (WAIR) hypothesis, 500f wings of, 83–84, 85f Bivalves, 285 Black-throated green warbler, 412f Bloat, 258, 259f, 260–261 “Bloat and float” biostratinomic process, 261, 261f Blood cold-blooded animals, 440, 530 red blood cells, producing, 132 temperature of animal’s blood, 440 warm-blooded animals, 440, 530 Body fossils, 268 Bombardment, 20, 21, 103 Bones, 125; see also Skeleton articulation, 258 in bird forearm, 492f cortical bone, 129 defining and classifying, 127–131 of dinosaur, 11, 325 disarticulation, 258, 262f endochondral bones, 129 first bone tissue, origination of, 135 flat bones, 128 intramembranous bones, 128–129 irregular bones, 128 long bones, 128 medullary bone

in fossils of Tyrannosaurus rex, 416f trabecular network of, 415f muscles, providing attachment sites for, 131 organic phase of, 127 phases of bone remodeling, 459f predentary bone, of ornithischian dinosaurs, 156 red blood cells, producing, 132 rib bone, 129, 129f rostral bone, 179 short bones, 128 skeletal map, navigating, 132–135 tetrapod bone, 457 tissue, types of, 125–127 trabecular (spongy) bone, 129 of Troodon formosus, 459f vitamins and minerals, storing, 132 woven bone, 416 Bone tissue, 126, 127, 210, 298, 403, 416, 456, 493 Bony correlates of cheeks, 362–364 Borealopelta sp., 166f, 336f, 342 B. markmitchelli, 161f Boundary events, 511 Boyle’s law, 7 Brachiosaurus, 135f, 204f B. altithorax, 203 forelimb (cast) of, 199f skeleton (cast) of, 204f Brachylophosaurus, 133, 383f Breathing, 259, 448, 462, 495 Breeding of dogs and cats, 63 Brooding, 422, 429, 431, 455 Brown, Barnum, 13, 13f, 14 Browsers, 71, 350 Bucket brigade, 130 Buckland, William, 10 Burgess Shale, 109, 505 Burial after death, 265 of eggs, 242 environment and conditions, 267 C4 plants, 57 Cacops aspidephorus, skeletal cast of, 142f Calcium needed to make eggshells, 414, 415f Callus, 398, 398f Camarasaurus, 363–364 lower jaws of, 358f, 365f skull (cast) of, 203f, 361f three-dimensional reconstruction of skull of, 366f Cambrian Explosion, 51, 109, 517 Cambrian Period (541–485 Ma), 109 Camouflage, 340–346, 341f, 343f Canada goose, 433, 434f Canadian Rocky Mountains, 109 Carbohydrates, 98 Carbon, isotope of, 47 Carbon-14, 48 Carbon cycling, 105, 111 Carbonemys, 230, 231f Carbon films/compression fossils, 269–270, 269f Carboniferous Period (359–299 Ma), 113–114, 514 Carboniferous Rainforest Collapse, 114 Carcharodontosaurus sp., 523 C. saharicus, 217, 220f

INDEX teeth of, 358, 359f Cardiac muscle, 126 Carnivores, 207, 349, 481, 523 Allosauria, 216–217 Ceratosauria, 211–213 Coelophysoidea, 210–211 Coelurosauria, 218–220 Megalosauria, 215–216 Tetanurae, 213–215 Carnivory, 350–353 advantages, 350 disadvantages, 351 Carnotaurus sp., 332 C. sastrei, 212 forelimb of, 214f skeletal diagram of, 213f Carpal, semi-lunate, 473, 473f Cat, 56, 89f, 90, 432f chewing muscles in, 364f Catabolism, 440 Caudipteryx, 368f, 454f Caudofemoralis longus, 326 Caudofemoralis muscle, 326f Cellulose, 98, 351, 366 Centrosaur, 335f Centrosaurinae, 182 Centrosaurines, 183–184, 411 Centrosaurus, skull of, 183f Ceratopsians, 33, 178–181, 180f, 334– 335, 434f Ceratopsidae, 182–184, 183f Ceratosauria, 211–213 Ceratosaurus sp., 121, 337f C. nasicornis, skeletal mount (cast) of, 213f fossilized skull elements from, 337 skeletal mount (cast) of, 213f Champsosaurs, 529 Character matrix, 88, 90 Characters, identifying, 87–91 Chasmosaur, 182–183, 335f Chasmosaurinae, 182, 183f Chasmosaurines, 182–183, 411 Chasmosaurus belli, 335f Cheeks, 363 bony correlates of, 362–364 Cheetah, 73 forelimbs of, 312f Chemical evidence for early life, 105 Chemical sedimentary rock, 37 Chevron, 413–414, 413f Chewing muscles, 363 in horse, cat, and theropod, 364f Chiappe, Luis, 15 Chicken, 433, 488f eggs, 424f semi-lunate carpal in the wrist of, 473f Chicxulub impact crater, 527, 528 Chin, Karen, 15 Chitin, 85, 285 Choeronycteris mexicana, 491f Chordata, 79, 140 Citipati, 375, 422 arms of, 456f embryo of, 423f Clade, 82, 85 and cladistics, 86 cladogram, reading, 86–87 identifying characters, 88–91 defined, 151 Cladistics, 82, 83

Cladogram, 86–87, 87f, 88, 90f, 91f of Animalia, 490f of Archosauria, 497f of Aves, 488f of Avialae with the group Aves, 487f with the group Ornithothoraces, 485f with the group Ornithurae, 486f of Dinosauria, 152f, 159f, 185f, 192f, 221f of Maniraptoriformes, 470f, 472f, 476f, 477f, 478f, 480f, 483f of Marginocephalia, 175f depicting the placement of Pachycephalosauria, 175f showing the placement of Ceratopsia, 179f showing the placement of Ceratopsidae, 183f showing the placement of Coronosauria, 182f of Ornithopoda, 168f depicting the placement of Saurolophidae, 173f indicating the members of Hadrosauridae, 171f indicating the members of Styracosterna, 168f of Sauropodomorpha, 192f depicting the placement of Diplodocoidea, 201f depicting the placement of Titanosauria, 205f indicating the members of Sauropoda, 198f indicating the placement of Macronaria, 203f showing the transition from the lobefinned fish tetrapods, 515f of Tetanurae, 470f depicting the placement of Coelurosauria, 218f depicting the placement of Megalosauria, 215f showing the placement of Allosauria, 217f of Tetrapoda, 226f depicting the placement of Ankylosauria, 164f depicting the placement of Ceratosauria, 212f depicting the placement of Coelophysoidea, 211f depicting the placement of ichthyosaurs, 247f depicting the placement of plesiosaurs, 249f depicting the placement of Tetanurae, 215f with the position of pterosaurs, 234f showing the placement of mosasaurs, 251f showing the placement of Stegosauria, 161f with the various groups of marine reptiles, 245f of Theropoda, 207f of Thyreophora, 160f of Tyrannosauroidea, 219f of vertebrates, 461f Clastic sedimentary rocks, 36–37

537

Claws from the manus of Therizinosaurus, 478f Clay grains, 102, 266 Climbing, 314–316, 315f Coastline matching, 29–30 Coelacanth, 507, 508 Coelophysis, 120, 120f, 395f skull (cast) of, 212f Coelophysoidea, 210–211 Coelurosauria, 218–220 Co-evolution, 73 Cold-blooded animals, 440, 530 Cold-bloodedness, 440 Collagen I, 127 Colors, birds expressing a range of, 340f Colors and color patterns, of dinosaur, 339 camouflage, 340–346 Compression fossils, 269–270 Compsognathus, 372 Computer modeling, 17, 22 Confuciusornis, 15 C. sanctus, 417 short-tailed and long-tailed specimens of, 418f Conglomerates, 38 Connective tissues, 126 Consumers primary, 289 secondary, 289 tertiary, 290 Continental–Continental convergence, 26, 28, 28f Continental crust, 25, 28 Continental drift, 29, 32 Continental–Oceanic convergence, 26, 28, 28f Continental rifting, 27, 27f Continental rocks, 21 Convection, 24 Convection current, 24, 25 Convergent boundary, 25 Cope, Edward Drinker, 11, 12f, 13 Coprolite, 368–369, 369f, 370f Coprophagy, 370 Coronosauria, 181–182 Cortical bone, 129 Corythosaurus, 174, 334 Countershading, 341 Cow, 89f, 90 Cranial-caudal, 134 Cranial skeleton, 132 Crestless hadrosaurids, 174 Cretaceous crocodyliform, skull (cast) of, 145f Cretaceous–Paleogene extinction, 524 causes of, 525–529 extinction recovery, 530 organisms which went extinct, 529–530 Cretaceous Period (145–65 Ma), 33, 33f, 121–122 Crocodile, 92, 230–233, 326, 361–362, 413–414; see also Alligator fossil skeleton of, 441 genitalia, 408f Crocodylian, skull of, 362f Crurotarsal ankle, 147f Crurotarsi, 147 Crust, 23 Cryptic coloration, 340, 341f Currie, Philip, 15

538

INDEX

Cursorial animals, 307f, 312 critical factor for, 311 feet of, 313f Cursorial locomotion adaptations stability and efficiency, 311–314 stride length, adaptations that increase, 305–308 stride rate, increasing, 308–311 Cursorial skeletal features, dinosaurs with, 310 Cursorial theropod, hindlimb of, 311f Cuticle, 283–284, 284f, 426 Cynodonts, 119, 519f Dakota, 269f Darwin, Charles, 53–55, 68 tenets of evolution, 54–57 theory of evolution, 7, 11 Daspletosaurus, 372 skeleton (cast) of, 157f Data, defined, 2 Dating, absolute, 46, 47, 49, 50 Deep time, 51 Definition of Dinosauria, 137–139, 150–151 Deinonychosauria, 480–482 Deinonychus, 14, 189, 484 D. antirrhopus, 473f foot of, 481f fore- and hindlimb proportions in, 484f pelvis of, 151f, 191f skull of, 362f Deinosuchus, 362 Deltaic deposits, 39 Deltopectoral crest, 148 Dentary, 156 Depositional environments, 281 De Ricqlès, Armand, 14 Derived trait, 85 “Descendant” dinosaur, 49 Desmatochelys padillai, 230 Desmatosuchus spurensis, 118f Detritivores, 291 Deuterium, 47 Devonian Period (419–359 Ma), 112–113 Diagenesis, 257, 265 burial, speed of, 265 burial environment and conditions, 267 ground and pore waters, 265 microbial activity, 266 organismal factors, 267 oxygen, amount of, 266 sediment, type of, 265–266 Diapsids, 143, 251, 519 Dicraeosaurid, 202, 202f Dicraeosauridae, 202 Dicraeosaurus hansemanni, 202 Dicynodonts, 118 Diets of dinosaur, 349 carnivory vs. herbivory, 350–353 direct evidence, 371 stomach contents, 371–373 teeth and tooth marks, 371 herbivorous dinosaurs’ diet, 373–374 indirect evidence bony correlates of cheeks, 362–364 feces (coprolites), 368–370 jaw shape, musculature, and articulation, 360–362 skeletal anatomy, 364–368 tooth morphology, 353–359 toothless dinosaurs, 374

Digging, 316–319 Digitigrade Amur leopard, hindlimbs of, 309f Digitigrade foot posture, 91, 308 Dilong paradoxus, 218, 453 Dilophosaurus, 213, 214f, 215f, 337, 377, 523 Dimetrodon, 114, 115f skeleton of, 144f skull of, 144f Dimorphodon, skeletal mounts of, 239f Dino-nots, 149, 151 dinosaurs vs., 137–139 Dinosauria, 11, 80, 92, 491 Dinosaur Park Formation, 289f, 370 ecosystem preserved in, 278f Dinosaur Ridge, 385f Diplodocidae, 202 Diplodocids, 363 Diplodocoidea, 201–202 Diplodocoids, 388 skeletal reconstructions of hips and hindlimbs of, 389f Diplodocus, 13, 194f, 199f, 363–364, 523f lower jaws of, 365f skull of, 361f three-dimensional reconstruction of skull of, 366f Directional selection, 57–58 Disappearance of dinosaurs, 526f Disconformity, 43, 44f Disease, 64, 402–404 Disruptive coloration, 341 Disruptive selection, 58–59 Distant past, study of, 16 Divergent boundary, 26, 26f Diversifying selection (or disruptive selection), 58–59 Diving bird, 487f DNA, 98 DNA coding, 55 DNA sequences, 88 Dobzhansky, Theodosius, 75 Dog, 89f, 90 foot postures in, 309f, 384f Dolphin, 81, 81f Donax variabilis, 54f Dorsal-ventral, 134 Dracorex hogwartsia, 178f Dragonfly, wings of, 83–84, 85f Dreadnoughtus schrani, 206 Drip tip, 283, 284f Dromaeosauridae, 480 Dromaeosaurids, 472f, 480–481, 481f Drug resistance, 64 Dryptosaurus, 218f, 447f D. aquilunguis, 218 Duck, 488f Dunkleosteus, 112f Dust cloud, interstellar, 22 Early Jurassic and Late Jurassic, arrangement of continents during, 68f Early life, evidence for, 104 chemical evidence, 105 fossil evidence, 106–108 mineral evidence, 105–106 Earth age of, 22 core, 23

earthquake waves travelling through, 24f first evidence for water on, 51 five largest extinction events, 510 internal layers of, 23 magnetic field of, 24, 31 Earth, history of, 19 building blocks of the Earth, 34–38 first evidence for water on Earth, 51 formation of the Earth, 20–23 geologic timescale, 49–51, 50f Hadean Period, Earth in, 21, 21f Pangea, formation of, 52 planetary structure and plate tectonics, 23 coastline matching, 29–30 distribution of rock types and ancient life recorded in the fossil record, 30 Global Positioning System (GPS), 32–33 mid-ocean ridges, 30, 31f paleomagnetism, 31 seismic and volcanic activity, 31–32 rocks, age of radiometric dating, 46–49 stratigraphic dating, 40–46 sedimentary environments, 38–40 solar system and Earth, 21–23 Earthquake, 31 epicenters from 1963–1998, 32f in Wadati–Benioff zone, 32f waves, 24f East African Rift Valley, 521 Eastern Black Swallowtail butterfly, 491f Ecological hierarchy, levels of, 286 Ecological relationships, 287f hierarchy applied to dinosaurs, 288f Ecology, defined, 277–278 Ecology of dinosaurs, 277 biosphere, 285–292 Earth’s atmospheric composition, changes in, 298–299 ecological case study, 292–298 environments of Jurassic and Cretaceous, 299 geosphere, 279 ancient environments, proxies for physical parameters of, 281–285 light, 280 oxygen, 279 precipitation/water, 280–281 substrate, 280 temperature, 279 Ectothermic animal, 440 Ectothermic heterotherms, 447 Ectothermic homeotherm, 443 Ectothermic organisms, 441f, 442 Ectothermy, 443 advantages to, 444 disadvantages to, 444–445 Ediacaran fauna, 108 Ediacaran Period (635–541 Ma), 108– 109, 109f Edmontosaurus, 133, 296, 297f, 298, 327f, 361, 371, 371f, 402f skull of, 361f Eggs, 420 challenge of identifying the egg-layer, 421–423 chicken, 424f

INDEX dinosaur, 424f and egg-laying, 436 eggshell structure and classification, 423–426 elephant bird, 420f hummingbird, 424f ostrich, 424f physical constraints of, 420 production and shelling, 421 Eggshells microstructure, 425f ootaxonomy features to classify mineral structure, 425–426 morphology, 423 pore structure, 424–425 surface ornamentation, 424 Egg stealer, 478 Elasmosaurus, 250f Eldredge, Niles, 72 Electrons, 46 Elephant, 389f foot of, 313f hindlimbs of, 310f skeleton, 308f Elephant bird, egg of, 420f Ellesmere Island in Canada, 9 Elongate melanosomes, 344, 345f Embryo of Citipati, 423f Enantiornithes, 485 End-Cretaceous extinction, 506f, 525 Endocast of T. rex brain, 294 Endochondral bones, 129 End-Ordovician mass extinction, 511–513 Endothermic animal, 440 Endothermic organisms, 441f Endotherms, 441, 444–445 turbinates in the skulls of, 461f Endothermy, 442, 443 advantages to, 445 disadvantages to, 445–446 Endothermy gene, 447 End-Permian extinction, 515 emergence of dinosaurs, 520–521 extinction recovery, 520 organisms which went extinct, 517–519 proposed causes of, 516–517 End-Triassic extinction, 521 causes of, 521–522 extinction recovery, 523–524 organisms which went extinct, 522–523 Energy pyramid, trophic levels of, 288 English bulldog, 304f skeletal forelimbs of, 305f Environment, 66, 278; see also Biosphere; Geosphere biological, 278, 282 depositional, 281 physical, 278 sedimentary, 38–40 terrestrial depositional, 39 Eohippus, 71f, 72 Eolian rocks, 39 Eons, 50 Eoraptor, 15, 119, 120, 190f, 520 skeletal reconstructions of, 450f EPB approach, see Extant phylogenetic bracket approach Epithelial tissues, 126 Epochs, 50

Equus, 71 Eras, 50 Erickson, Greg, 15 Erosion rooms, 130 Estuarine, 39 Eudimorphodon, 235, 237f Eukaryota, 140 Eukaryotic cells, 123 Eunotosaurus, 228 flesh reconstruction of, 229f Euornithes, 485 Europasaurus, 193f Euxinia, 516 Evolution, 53; see also Life, origin of Darwin’s tenets of, 54–57 of Dinosauria, 139 Amniotes, 141–143 Archosauria, 144–146 Avemetatarsalia, 146–147 Chordata, 140 Diapsida, 143 Eukaryota and Animalia, 140 Tetrapoda, 141 Vertebrata, 141 evidence for, 74–75 as fact, 73–74 gradualism vs. punctuated equilibrium, 72–73 natural selection, 57, 66–67 directional selection, 57–58 diversifying selection, 58–59 sexual selection, 59–61 stabilizing selection, 59 pace of evolutionary change, 75 populations, change in, 61 drug resistance, 64 human diversity, 64–65 peppered moths, 63–64, 64f selective breeding of dogs and cats, 63 wild corn, 61–63 speciation, microevolution, and macroevolution, 67–71 as theory, 74–75 variation, sources of, 65 genetic mutation, 65–66 sexual recombination, 65 Evolutionary transitions in fossil record, 70 Exaptation, 498 Excessive volcanism, 516 Experiment, 6 Experimental science, 3 Experimentation, 6 Extant phylogenetic bracket (EPB) approach, 91, 92, 432–433 Extinction, patterns of, 16 Extinctions of dinosaur, 505 causal mechanisms for the K–Pg mass extinction, 532–533 Cretaceous–Paleogene mass extinction, 524 causes of, 525–529 extinction recovery, 530 organisms which went extinct, 529–530 End-Permian extinction, 515 emergence of dinosaurs, 520–521 extinction recovery, 520 organisms which went extinct, 517–519 proposed causes of, 516–517

539

End-Triassic extinction, 521 causes of, 521–522 extinction recovery, 523–524 organisms which went extinct, 522–523 mass extinctions, 510 End-Ordovician mass extinction, 511–513 Late Devonian mass extinction, 513–515 post-Cretaceous world, 530–532 survival in mass extinction event, 533 types of extinctions, 505–508 vulnerability to extinction, 508–510 Extrusive igneous rocks, 35, 36f Falsifiable hypothesis, 5 Fastest dinosaurs, 17 Feather, 493 -likes structures in dinosaurs, 346 structure of, 474f Feathered dinosaurs, 454f Feces (coprolites), 368–370 Feet of cursorial animals, 313f Femur, 148, 149f Fighting dinosaurs, 401 Fingers, of tyrannosaurids, 219 Fish-like ancestors, tetrapods origin from, 9 Fish-lizards, see Ichthyosaur Flat bones, 128 Flesh and skeleton of ostrich, 488f Fleshed head, ofalligator, 330f Flesh reconstruction of saurischian, 330f Flight, origin of, 469; see also Birds; Wings advantages of flight, 491–492 Avialae and avian characteristics, 482 Aves, 487–488 Ornithothoraces, 485–486 Ornithurae, 486–487 birds, flight muscles in, 495f Euornithes and end cretaceous extinction, 502 feathers, evolution of, 502 flight, evolution of, 498 “Ground up” hypothesis, 500–501 temporal paradox of bird evolution, 501–502 “Trees Down” hypothesis, 498–499 Maniraptoriformes, groups within, 469 Alvarezsauria, 476 Deinonychosauria, 480–482 Maniraptora, 471–476 Ornithomimosauria, 470–471 Oviraptorosauria, 478–479 Paraves, 480 Therizinosauria, 477–478 powered flying, adaptations for, 489 extremely efficient respiratory system, 495–496 feathers, 493 lightweight skeleton, 496–498 powerful flight muscles, 493–495 stabilized skeleton, 492–493 wings, 492 Floodplain deposits, 39 Fluvial deposits, 39 Flying reptiles (pterosaurs), 233–243 Folivores, 349 Food web depicting relationships, 291, 292f

540

INDEX

Foot of Deinonychus antirrhopus, 481f of elephant, 313f of sauropod, 313f Foot postures of dog, 309f, 384f of horse, 309f, 384f of human, 309f, 384f of monkey, 309f, 384f of sheep, 309f, 384f Footprint of dinosaur, 11 formation and preservation, 378–379, 378f, 379f taphonomy, 379–381 Forearm of bird, bones in, 492f Forelimbs, 296f of badger, 312f of cheetah, 312f of human and whale, 302f of tyrannosaurids, 219 Forster, Cathy, 15 Fossil, 255, 267; see also Rocks becoming a fossil, 256 body fossils, 268 carbon films/compression fossils, 269–270 compression fossils, 269–270 -containing rocks, 45 to determine relative ages of rocks, 45, 45f evidence, for early life, 106–108 from Green River Formation, 278f impression, 269 invertebrates, 285 leaves, 291f living, 256 long-lived, 45 mold-and-cast, 270 permineralization, 266f, 270, 271f recrystallization, 270 replacement, 271–272 short-lived, 45 unaltered, 268–269 of vascular plants, 514f Fossil Butte National Monument, fossil leaves recovered from, 291f Fossiliferous limestone, 37f Fossilized feces, 368 Fossil record ancient life recorded in, 30 evolutionary transitions in, 70 transition fossils, 71 Fossorial locomotion, adaptations for, 316–319 Fourth trochanter, 145–148 Fractionation, 105 Frilled ornithischians, 174 Ceratopsia, 178–181 Ceratopsidae, 182–184 Coronosauria, 181–182 Pachycephalosauria, 175–178 Frugivores, 349 Functional morphology, 125, 302 Furcula, of theropods, 208 Futalognkosaurus dukei, 206 Galapagos islands, 68 Galileo, 5 Gallimimus skull, 471f

Gamma (γ) decay, 47 Gastralia, 158 of ornithischian dinosaurs, 157 Gastroliths, 367 Genetic mutation, 65–66 Genotype, 55 Geocentrism, 5 Geochemistry, 17 Geochronological isotopes, 48 Geological time scale, 108f Geologic time, 51 four eras of, 98f Geologic timescale, 49–51, 50f Geology, 17 Geosphere, 279 ancient environments, proxies for physical parameters of, 281 depositional environments, 281 fossil invertebrates, 285 paleosols, 281–282 phytoliths, 282 plant fossils, 282–284, 283f pollen, 282 light, 280 oxygen, 279 precipitation/water, 280–281 substrate, 280 temperature, 279 German shepherd, 304f skeletal forelimbs of, 305f Gharial, skull of, 359f Ghost lineages, 508 Ghost taxa, 508 Giant supercontinent, 32 Giraffe, skeleton of, 196f Gliding, forces at work during, 490f Global extinctions, 507 Global Positioning System (GPS), 32–33 Gneiss, 36f Gobi Desert, 281 Golden retriever, skull of, 329f Gondwana, 33 “Gooey” rock, 23 Gorge feeding, 358 Gorgosaurus, 260 Gould, Stephen J., 72 GPS, see Global Positioning System Gradualism, 72 vs. punctuated equilibrium, 72–73 Grallator, 393 Granite, 35, 35f Granivores, 350 Grant, Alan, 14 Graphite, 105 Graviportal sauropod, hindlimb of, 311f Gravitational forces, 27 Grazers, 350 Great Bone Wars, 11 Great Dying, 515 Great Oxygenation Event, 106 Green River Formation, fossil from, 278f Green trilobite fossils, 46 Grizzly bears, 66f Ground and pore waters, 265 “Ground up” hypothesis, 500–501 Gryposaurus, 334f Guinea pig, 56, 56f Gymnosperm, 291 Habitat of an organism, 287 Hadean, 21

Hadean Period, Earth in, 21f Hadrosaur pes (foot) of, 169f tail of, 158f Hadrosaurid, 169f, 171f, 334 Hadrosauridae, 171–173 Hadrosaurid lower jaw, 358f Hadrosaurid teeth, 356f Hadrosaurs, 33, 171–173 Hadrosaur tooth, 157f Hadrosaurus, 11 Hadrosaurus foulkii, 172, 172f Hagfish, 111 Hair, 82 “Half-life”, concept of, 48 Halite, 37 Hallucigenia, 109, 110f Haversian system, 130 Heart, four-chambered, 460–461 Heat in Earth’s interior, 24 Herbivores, 349 Herbivorous dinosaurs’ diet, 373–374 Herbivory, 350–353 advantages, 351 disadvantages, 351 traits associated with, 157–158 Heritability, 54–56 Herrerasaurus, 119, 119f, 120, 190f, 520 skeletal reconstructions of, 450f Hesperornis, skeletal reconstruction of, 487f Hesperosuchus agilis, 118f Heterocephalus glaber, 441, 442f Heterodont dentition in American black bear, 353f Heterodontosaurid dinosaurs, 354f Heterodonty, 353 Heterotherms, 441, 442 Heterothermy, 443 Hindlimb of cursorial theropod, 311f of digitigrade Amur leopard, 309f of elephant, 310f of graviportal sauropod, 311f of horse, 310f of Lambeosaurus, 309f of plantigrade polar bear, 309f of Tyrannosaurus rex, 309f of unguligrade horse, 309f Histology, 17 Historical science, 3–4 Hoatzins, 316, 500f Holtz, Tom, 15 Holzmaden, 248 Homeothermic, 442 Homeothermy, 443 Homodont, 353f, 354 Homologous structures, 75 Homologous trait, 86 Homoplasies, 83 Homoplastic traits, 83 Homoplasy, 83 Homo sp. H. erectus, 71, 80 H. habilus, 71, 80 H. neanderthalensis, 71, 80 H. sapiens, 51, 71, 80 Hooklets, 473 Hopanes, 105 Horned dinosaurs, 59 Horner, Jack, 14

INDEX Horse chewing muscles in, 364f foot postures in, 309f, 384f hindlimbs of, 310f skeleton, 307f ungual and hoof of, 383f Hot conditions, hypothesis that life began under, 102–103 Human digitally reconstructing face, 328f diversity, 64–65 foot postures in, 309f, 384f overprint, 16 proportional changes during development of, 432f sexual dimorphism in pelvic structure, 409f skeleton, 128f, 195f, 310f Hummingbird eggs, 424f Hunting, 404 Hutchinson, John, 15 Hutton, James, 41–43 Hutton’s unconformities, 43 Hydrogen, isotopes of, 47, 47f Hydrothermal vents, 102, 102f Hydroxyapatite, 265, 271 Hydroxylapatite, 127 Hydroxylapatite-collagen composite, 127 Hypacrosaurus, 334, 431 Hypercarnivores, 349 Hyperextensible joints, toe with, 480 Hypothermic, 442 Hypothesis, 4, 7 falsifiable hypothesis, 5 parsimonious hypothesis, 4 scientific hypothesis, 5 testable hypothesis, 5 Hypothesis testing experimentation, 6 meta-analysis, 6 prediction, 5 systematic review, 6 Hypsodonty, 355 Icarosaurus siefkeri, 228, 229f Ichnology, 390 Ichnotaxonomy, 390–394 Ichthyornis, 486 Ichthyosaur, 10, 81, 81f, 122, 246–248, 249f Igneous rocks, 34–35, 38 Iguana, 144f Iguanodon, 10, 11, 169, 170 articulated manus (hand) of, 170f early reconstruction of, 171f Impact-extinction hypothesis, 527 Impression fossils, 269 Index fossils, 45, 46 Infilled tracks, 378 Inherited characters, 56 Injuries, 396–404 Insecta, 490–491 Insectivores, 349 Insects, 518 Insertion, 131 Intermediate-sized dinosaurs, 455 Interplanetary seeding, 103 Interpretations, observations and, 3 Interstellar bodies, collisions between, 22 Interstellar dust cloud, 22 Intramembranous bones, 128–129 Intrusive igneous rocks, 35, 36f

Invalid scientific hypothesis, 5 Invertebrate paleontologists, 8 Iridium, 526–527, 526f Irregular bones, 128 Island arcs, 28 Isotopes, 47 Jaw joint set, of ornithischian dinosaurs, 156 Jaw shape, musculature, and articulation, 360–362 Jeholornis, 418f Jumping, 319–321 Juramaia sinensis, 226f, 523f Jurassic Park movies, 14 Jurassic Period (201–145 Ma), 50, 120–121 Kamuysaurus japonicus, 261f Kangaroo, skeleton of, 320f Kentrosaurus sp. articulated mount of, 163f K. aethiopicus, 162 Kitten, 432f Knee of horse and human, 307f Korolev crater on Mars, 4f K–Pg extinction, see Cretaceous– Paleogene extinction K–T extinction, see End-Cretaceous extinction Lacustrine rocks, 39 LAGs, see Lines of arrested growth Lambeosaurinae, 173 Lambeosaurines, 334, 411 Lambeosaurus, 308 hindlimb of, 309f pubis of, 156f Lampreys, 111, 111f Late Cretaceous Period, 33, 33f Late Devonian mass extinction, 513–515 Lateral mandibular fenestrae, 145 Lateral-medial, 134 Late Triassic Period, 33, 33f Laurasia, 33 Lava, 35 Lava lamp, 24, 25f Law of Lateral Continuity, 41, 41f Law of Original Horizontality, 41 Law of Superposition, 40, 40f Lazarus taxa, 507, 508 Leidy, Joseph, 11, 12f Leopard shark (Triakis semifasciata), 141f Leptoceratopsidae, 181–182 Lesothosaurus, 159, 357, 521 skull of, 357f Life, origin of, 97, 122–123; see also Evolution defining life, 97–99 from early multicellular life to the time of the dinosaurs, 108 Cambrian Period (541–485 Ma), 109 Carboniferous Period (359–299 Ma), 113–114 Devonian Period (419–359 Ma), 112–113 Ediacaran Period (635–541 Ma), 108–109, 109f faunal succession, 108 Ordovician Period (485–444 Ma), 110–111

541

Permian Period (299–252 Ma), 114–116 Silurian Period (444–419 Ma), 111–112 eukaryotic cells, 123 evidence for early life, 104 chemical evidence, 105 fossil evidence, 106–108 mineral evidence, 105–106 hypotheses for, 99 that life began in shallow bodies of water, 101–102 that life began under extremely hot conditions, 102–103 that life came from space, 103–104 Mesozoic Era, 108, 116 Cretaceous Period (145–65 Ma), 121–122 Jurassic Period (201–145 Ma), 120–121 Triassic Period (252–201 Ma), 116, 117–120, 117f Triassic–Jurassic extinction event, 123 Life sciences, 3 Lightweight skeleton, 496–498 Limestone, 37, 37f Lines of arrested growth (LAGs), 131, 457, 457f Linnaeus, Carl, 78 Linnaeus’s system, 80 Lipids, 98 Liquid water, 21 Lithification, 37 Lithosphere, 25 Living fossil, 256 “Lizard-hipped” dinosaurs, 150 Lizards, 89f, 227–228 Lobe-finned coelacanth, 508f Lobe-finned fish (sarcopterygians), 112 Local extinctions, 506 Locomotion; see also Running arboreal locomotion, adaptations for, 314–316 cursorial locomotion adaptations stability and efficiency, 311–314 stride length, adaptations that increase, 305–308 stride rate, increasing, 308–311 fossorial locomotion, adaptations for, 316–319 saltatorial locomotion, adaptations for, 319–321 London’s Natural History Museum, 10 Long bones, 128 Longisquama insignis, 228, 229f Long-necked sauropod dinosaurs, 17 Lower jaws of Camarasaurus, 365f of Diplodocus, 365f Lungs, 461–464 of archosaurs, 463 of birds, 463 of dinosaurs, 17 Lycopsids, 513 Lyell, Charles, 42, 43, 50 Machaeroprosopus mccauleyi, 231f McPhee, John, 51 Macro-biomolecules, 98 Macroevolution, 69–70 microevolution vs., 69–71

542

INDEX

Macronaria, 202 Titanosauria, 203–207 Macronarians, 363 Magma, 27, 34 Magnetic field of Earth, 24, 31 Magnetic minerals, 281 Magnetometer, 31 Magyarosaurus sp., 206f M. dacus, 206 Mahajangasuchus insignis, skull (cast) of, 145f Maiasaura sp., 432 M. peeblesorum, 14, 430–431 manus (hand) of, 170f skull (cast) of, 156f Maiasaurus, 291 humerus of Maiasaurus skeleton, 149f Majungasaurus, skull of, 362f Mammalia (Bats), 83, 491 Mammal lungs, 463 Mammals, 226–227, 441 Mammuthus primigenius, 264f Maniraptora, 471–476 Maniraptoran dinosaur, 339f, 472 Maniraptoriformes, 218, 220, 352f groups within, 469 Alvarezsauria, 476 Deinonychosauria, 480–482 Maniraptora, 471–476 Ornithomimosauria, 470–471 Oviraptorosauria, 478–479 Paraves, 480 Therizinosauria, 477–478 Mantell, Gideon, 10 Mantell, Mary Ann, 10 Mantle, 23, 24 Manus (hand) of Maiasaura, 170f Marginocephalia, 166, 174 Ceratopsia, 178–181 Ceratopsidae, 182–184 Coronosauria, 181–182 Pachycephalosauria, 175–178 Mariana trench, 28 Marine organisms, 517–518 Marine reptiles, three main groups of, 253–254 Marrow, 132 Marsh, Othniel Charles, 11–13, 13f Marsh deer skeleton, 308f Mass death assemblages, 394–395 Mass extinctions, 506, 510 End-Ordovician mass extinction, 511–513 Late Devonian mass extinction, 513–515 Mass homeothermy, 443 Massospodylus nest with embryos, 197f Massospondylus, 196–197 Mating behaviors and reproductive strategies, 408 Meandering river, 263, 264f Medullary bone in fossils of Tyrannosaurus rex, 416f trabecular network of, 415f Megalosauria, 215–216 Megalosaurus, 10 Megatherium, skeleton of, 318f Mei Long, 482f Melanosomes, 344 Mesohippus, 72 Mesozoic animals that are not dinosaurs, 225

extant Mesozoic lineages, 226 crocodiles, 230–233 mammals, 226–227 squamates, 227–228 turtles, 228–230 flying reptiles (pterosaurs), 233–243 marine reptiles, three main groups of, 253–254 pterosaurs, evolutionary history of, 253 swimming reptiles, 243 Ichthyosaurs, 246–248 Mosasaurs, 251–253 Plesiosaurs, 249–251 Mesozoic dinosaurs, 15 Mesozoic Era, 108, 116 Cretaceous Period (145–65 Ma), 121–122 Jurassic Period (201–145 Ma), 120–121 Triassic Period (252–201 Ma), 116, 117–120, 117f Mesozoic turtles, 230 Meta-analysis, 6 Metabolic rates at the cellular and molecular levels, 466 of dinosaurs, 465 increase in, 465–466 of sauropods, 465 Metabolic strategies used by dinosaurs, 446 bipedality, 450 environmental distribution, 451–452 epidermally derived insulation, 452–454 four-chambered heart, 460–461 herding and migration, 450–451 incubation and brooding, 455 large size, 452 lungs and respiration, 461–464 mechanisms to shed heat, 454–455 rapid and/or continuous growth, 456–460 upright posture, 448–449 Metabolism, 98, 439–443 defined, 440 Metamorphic rocks, 34–36, 38 Metatarsal track, 381f Meteorites, 22 Mexican long-tongued bat, 491f Microbial activity, 266 Microbial paleontologists, 8 Microevolution, 67 vs. macroevolution, 69–71 Microraptor, 372 M. gui, 454f, 499, 499f Mid-Atlantic Ridge, 30, 30f Mid-ocean ridges, 26, 30, 31f Migration of animals in herds, 394 Miller, Stanley, 100 Miller–Urey experiments, 100, 101f Mimicry, 341 Minerals, 22, 78 characteristics of, 34 evidence for early life, 105–106 storing, 132 Minimum number of elements (MNE), 451 Miracinonyx, 73 Mistaken extinctions, 507, 508 MNE, see Minimum number of elements Modern rift valley, occurrence and extent of, 522f Mold-and-cast fossils, 270 Monkey, foot postures in, 309f, 384f

Mononykus olecranus, 476 skeletal mount (cast) of, 476 Monophyletic group, 82 Mosasaurs, 122, 246f, 251–253 mounted skeleton of, 252f Moths, peppered, 63–64 Mountain goat, feet of, 280f Mudstones, 38 Mule, 61, 62f Mummified bird foot, 383f Murchison Meteorite, 103 Muscles, providing attachment sites for, 131 Muscle tissue, 126 Mutation, 65–66 Nanotyrannus, 411 Nanuqsaurus, 452, 452f National Aeronautical and Space Administration (NASA), 99 Natural History Museum, of London, 10 Natural sciences, 3 Natural selection, 57, 66–67 modes of, 57 directional selection, 57–58 diversifying selection (or disruptive selection), 58–59 sexual selection, 59–61 stabilizing selection, 59 Nectarivore, 350 Nemicolopterus, 235 Neognathae, 487 Neornithes, 487 Nervous tissue, 126 Nests and egg laying strategies, 426–428 Neural spine, 399f Neutrons, 46 Niche, 287 Nigersaurus, 15 Nitrogen-14, 48 Nodosauridae, 165 Nomingia, 479 N. gobiensis, 479, 479f Non-avian dinosaurs, 304, 508, 511 Nonconformity, 43, 43f Non-vertebrate organisms, 291 Norrell, Mark, 15 North American Grizzly bear, 507f Notocolossus, 194f Nucleotides, 99 Numerical age dating, 48 Obligate scavengers, 293 Observations, 2 and interpretations, 3 Obsidian, 35 Oceanic–Continental convergent boundary, 28, 28f Oceanic crust, 25 Oceanic–Oceanic convergent boundary, 26, 27, 27f, 28 Offspring, organisms producing more, 56 Olfaction, 294 On the Origin of Species (Charles Darwin), 53–55 Ootaxonomy, 423–424 features to classify eggshells mineral structure, 425–426 morphology, 423 pore structure, 424–425 surface ornamentation, 424

INDEX Opabinia, 109, 110f Opisthocomus hoazin, 500f Ordovician Period (485–444 Ma), 110–111 Organic compounds, 102 Organismal factors, 267 Origin, 131 Ornamentation of dinosaur, 333 ceratopsians, 334–335 ornithopods, 334 sauropods, 335–336 theropods, 337–339 thyreophorans, 336–337 Ornithischia, 149, 166 Ornithischian dinosaurs, 155 armored ornithischians, 159 Ankylosauria, 164–165 Stegosauria, 161–165 bird foot ornithischians, 166 Hadrosauridae, 171–173 Saurolophidae, 173–174 Styracosterna, 167–171 definition, 184–185 diagnostic characters, 155 Herbivory, traits associated with, 157–158 posture, 158–159 earliest ornithischian, 186 frilled ornithischians, 174 Ceratopsia, 178–181 Ceratopsidae, 182–184 Coronosauria, 181–182 Pachycephalosauria, 175–178 and saurischians, 186 Ornithischians, 150, 520, 523 Ornithodira, 147 Ornithodirans, 116 Ornithomimid, 17, 332 foot of, 390f Ornithomimosauria, 470–471 Ornithopoda, 166 Hadrosauridae, 171–173 Saurolophidae, 173–174 Styracosterna, 167–171 Ornithopods, 334, 392 tracks, 393f Ornithothoraces, 485–486 Ornithurae, 486–487 Oryctodromeus skeletons, 318–319 Ossified tendons, of ornithischian dinosaurs, 157 Osteoblasts, 126, 130 Osteoclasts, 130 Osteocytes, 126, 130 Osteology, 303 Osteons, 126, 129 Ostrich eggs, 424f flesh and skeleton of, 488f skeleton, 307f Ostrich mimic, 470f Ostrom, John, 14 Oviraptor, 14, 421, 422, 426, 427, 430, 478 eggs, 423 nest, 428 pelvis from, 419f Oviraptorosauria, 478–479 Oviraptor philoceratops, 422 skull of, 478f Oviraptor specimen, 479f Ovis canadensis, 177 skull of, 179f

Owen, Richard, 10 Oxygen, 105, 266 Oxygen mixing, 513 Pachycephalosaur, 176f Pachycephalosauria, 175–178 Pachycephalosaurus, 361 P. wyomingensis, 178f skull of, 176f, 361f Pacific lamprey, 111, 111f Padian, Kevin, 14 Pakicetus fossils, 69, 69f Palaeognathae, 487 Paleobotanists, 8 Paleocene–Eocene Thermal Maximum, 532 Paleoclimatologists, 8 Paleoecologists, 8 Paleoecology, 277, 292 Paleomagnetism, 31 Paleontological hypotheses, 9 Paleontology, 8 dinosaur paleontology, 1 history of, 10–15 importance of studying, 16–18 and science, 9–10 Paleopathologies, 396 disease, 402–404 injuries, 396–404 Paleosols, 281–282 Palimpsest, 378 Palynologists, 8 Palynology, 282 Pangea, 32, 117, 120 formation of, 52 Pannotia, 109 Panspermia, 103 Papilio polyxenes, 491f Parahippus, 72 Parallel striations, 512f Paranthodon, multiple views of teeth from, 160f Parasaurolophus, 334, 334f manus (hand) of, 170f skeletal drawings of, 366f skeleton of, 167f skull (cast) of, 174f Paraves, 480 Pareiasaurs, 115, 115f Parental care, 428 developmental strategies, 429–432 evidence for, 432–434 physiology and reproduction, 434–435 Parsimonious evolutionary relationship, 93–94 Parsimonious hypothesis, 4 Past, study of, 16 Patagotitan, 205f forelimb of, 200f P. mayorum, 206 skeletal reconstruction of, 206f Peabody, George, 13 Peabody Museum, 13 Peafowl, 60, 60f Peer-reviewed literature, 6 Pelican ribcage of, 493f semi-lunate carpal in the wrist of, 473f Pelicanus onocrotalus, 493f Pelvis, 150 from Oviraptor, 419f

543

Penguin, 81, 81f Peppered moths, 63–64, 64f Periods, 50 Permian Gorgonopsid, 519f Permian insects, 518f Permian labyrinthodont amphibian, 519f Permian Period (299–252 Ma), 114–116 Permian seas, life that flourished in, 518f Permineralization, 265, 266f, 270, 271f Permineralized ammonite, 270f Phanerozoic Eon, 50, 111 Phenetic taxonomy, 81 Phenotype, 54, 55 Phenotypic variation, 54 Phorusrhacidae, 531 Phosphatization, 272 Photosynthesis, 56–57 Phylogenesis, 82 Phylogenetic relationships based on morphology and molecular evidence, 94 Phylogenetics, 77, 91–93 Phylogenetic systematics, 82 Physical environment, 278 Physical sciences, 3 Physiology and metabolism of dinosaur, 439 ectothermy advantages to, 444 disadvantages to, 444–445 endothermy advantages to, 445 disadvantages to, 445–446 kind of metabolism of dinosaurs, 464 metabolic rates at the cellular and molecular levels, 466 of dinosaurs, 465 increase in, 465–466 of sauropods, 465 metabolic strategies, 446 bipedality, 450 environmental distribution, 451–452 epidermally derived insulation, 452–454 four-chambered heart, 460–461 herding and migration, 450–451 incubation and brooding, 455 large size, 452 lungs and respiration, 461–464 mechanisms to shed heat, 454–455 rapid and/or continuous growth, 456–460 upright posture, 448–449 Phytoliths, 282, 282f, 369 Phytosaurs, 231f Pied-billed grebe, 210f Piscivores, 349 Pizzlies, 67 Placoderms, 111 Planetary structure, 23 Plant-eating dinosaurs, 357 Plant fossils, 282–284, 283f Plantigrade foot posture, 308 Plantigrade polar bear, hindlimbs of, 309f Plants, 518 Plate boundaries, 31 Plateosaurus, 521 P. engelhardti, 195f, 196 skeleton of, 197f

544

INDEX

Plate tectonics, 23–25 theory of, 32 Plesiosauromorphs, 249, 250, 250f, 251 Plesiosaurs, 249–251 Pliohippus, 72 Pliosauromorph plesiosaurs, 249 Pliosauromorphs, 249, 250, 250f Pliosaurs, 81, 250 Pliosaurus, 81, 81f Plutonic igneous rocks, 35, 36f Pneumatic skeleton, of theropods, 209 Pneumatization, 199 Podilymbus podiceps, skeleton of, 210f Poikilotherms, 441 Polar bear lizard, 452 Polar bears, 66–67, 66f skeleton, 308f Pollen, 282 Poopetrator, 369 Poop production, 368 Poposaurus gracilis, artistic reconstruction of, 450f Populations, change in, 61 drug resistance, 64 human diversity, 64–65 peppered moths, 63–64, 64f selective breeding of dogs and cats, 63 wild corn, 61–63 Populations with varying traits, 54 Pore waters, ground and, 265 Porphyrin, 93 Post-cranial skeletal pneumaticity (PSP), 199, 234, 496 Post-cranial skeleton, 132 Postosuchus kirkpatricki, 119f Powered flight, 489–490 forces at work during, 489f Powered flying, adaptations for, 489 feathers, 493 lightweight skeleton, 496–498 powerful flight muscles, 493–495 respiratory system, extremely efficient, 495–496 stabilized skeleton, 492–493 wings, 492 Powerful flight muscles, 493–495 Predation and scavenging, 261–262 Predentary bone, of ornithischian dinosaurs, 156 Prediction, testing by, 5, 6 Preserved skin, 331–332 Prestosuchus, 520f P. chiniquensis, 232f Primary consumers, 289 Principle of Crosscutting Relationships, 41, 42f Principle of Faunal Succession, 44 Principle of Inclusions, 42, 42f Principles of Geology, 42 Pronghorn, 73 Prosthemadera novaeseelandiae, 485f Proteins, 98 Protium, 47 Protoceratops, 14, 181–182, 182f, 422 hatchling, 423f pelvis of, 150f Protoceratopsidae, 182 Protons, 46 Proximal-distal, 134–135 Pseudofossils, 108 Pseudosuchia, 116, 147

Pseudosuchians, 146, 231 Psittacosaurus, 180–181, 181f, 331, 331f, 338 PSP, see Post-cranial skeletal pneumaticity Pteranodon, 235 Pterodaustro, 237f, 242f Pterosaur, 239f Pterosauria (pterosaurs), 491, 496 Pterosaurs, 118, 233–243 evolutionary history of, 253 Pterosaur wing membranes, 241f Pulley system in birds, 494 Puma concolor, 80 Punctuated equilibrium, 72, 72f Purported microfossils, 107 Pygostyle, 479 Pyrite, 272 Pyritization, 272 Python sebae, 142f Quail chick, 430f Qualitative data, 2–3 Quantitative data, 2–3 Quetzalcoatlus, 235, 236f Quill knobs, 475f, 475 Rabbit skeleton of, 320f skull and upper jaw of, 320f Radioactive decay, 47, 48 Radiometric dating, 46–49 Radiometric decay, 48 Rapetosaurus krausei, 205 Ray-finned fish (actinopterygians), 112 Recrystallization, 270 Red beds, 106 Red blood cells, producing, 132 Red gastropod, 45 Reef-building organisms, 514 Regaliceratops, 184 skull of, 184f Relatedness, similarity vs., 80–86 Repenomamus, 372 R. robustus, 373f Replacement, 271–272 Reproduction, of dinosaur, 407 biological sex determination, 407 ornamentation, 409–419 size disparity, 409 eggs, 420 challenge of identifying the egglayer, 421–423 and egg-laying, 436 eggshell structure and classification, 423–426 physical constraints of, 420 production and shelling, 421 larger dinosaurs, copulation of, 435 nests and laying strategies, 426–428 parental care, 428 developmental strategies, 429–432 evidence for, 432–434 physiology and reproduction, 434–435 sauropods, 435–436 Reproduction rates, 56, 509 Reptiles, 10 Reputation rehabilitation, 422f Respiratory system, 461–464 of birds, 463 of dinosaur, 464f

extremely efficient, 495–496 inhalation and exhalation cycles in birds, 463f, 495f of a representative mammal, 462f Resting metabolic rate (RMR), 443 Retroversion, 157 Retroverted pubis, 150 of ornithischian dinosaurs, 155 Rey, Luis, 400 Rhamphorhynchus, 243f R. muensteri, 240f Rib bone of dinosaur, 129, 129f Ridged teeth, of ornithischian dinosaurs, 156–157 Ridge push, 27 Rift basins, 117 Rifting, 27, 117 Rigor, 259–260, 260f Rigor mortis, 259, 260f RMR, see Resting metabolic rate RNA, chemical structure of, 100f “RNA first” hypothesis, 99 Rock cycle, 38, 38f, 41 Rocks, 16, 22, 34; see also Fossil age of radiometric dating, 46–49 stratigraphic dating, 40–46 types and classification, 34–38 distribution of, 30 Rock salt, 37 Rogers, Kristi Curry, 15 Rostral bone, 179 Round melanosomes, 344, 345f Running; see also Locomotion lizards, 481 stability and efficiency, 311–314 stride length, adaptations that increase, 305–308 stride rate, increasing, 308–311 of T. rex, 296 Russian dinosaurs, 33 Rust-red colored sedimentary rocks, 106 Saltatorial locomotion, adaptations for, 319–321 Saluki, 304f skeletal forelimbs of, 305f San Andreas Fault, 29, 29f Saprophytes, 291 Sarcopterygians, 112 Sarcopterygii, 141 Sarcosuchus, 233f S. imperator, 232 Saurischia, 149 Saurischian dinosaurs, 150, 189, 520 definition, 220–221 diagnostic characters, 189–191 Sauropodomorpha, 192 ancestral sauropodomorphs, 196–197 Diplodocoidea, 201–202 Macronaria, 202–207 Sauropoda, 197–201 sauropods, rapid growth of, 221–222 theropoda, 207 Allosauria, 216–217 Ceratosauria, 211–213 Coelophysoidea, 210–211 Coelurosauria, 218–220 Megalosauria, 215–216

INDEX Tetanurae, 213–215 theropods, unique evolutionary features in, 222 Saurischians theropods, 17 Sauroctonus parringtoni, 519f Saurolophidae, 173–174 Saurolophinae, 173, 174 Saurolophines, 411 Saurolophus, skull (cast) of, 174f Sauropoda, 197–204 Sauropod dinosaurs, 17, 68, 335–336, 392 attacking a predator, 443f dorsal vertebra, 200f foot of, 313f forelimb and hindleg of, 392f long-necked, 17, 446f mechanisms to shed heat, 454–455 in skeletal and artistic reconstruction, 449f teeth, 361 Sauropodomorpha, 192 ancestral sauropodomorphs, 196–197 Diplodocoidea, 201–202 Macronaria, 202 Titanosauria, 203–207 Sauropoda, 197–201 Saurornithoides, 14 Scapula, human and horse showing the placement of, 306f Scavengers, 290 Scavenging and predation, 261–262 Schopf, William, 107 Science, 1 defining, 2–4 paleontology and, 9–10 Scientific hypothesis, 5 invalid, 5 Scientific investigation, anatomy of, 4–8 Scientific laws, 7 Scientific name, stylistic rules for expressing, 80 Scientists, 1 Sclerocephalus haeuseri, articulated skeleton of, 519f Scutellosaurus, 160–161 S. lawleri, 160f Sea levels, 513 Sea turtle, 342f skull of, 143f Secondary consumers, 289 Sediment, type of, 265–266 Sedimentary environments, 38–40 Sedimentary rock, 34, 36, 38, 39, 48–49 biochemical, 37 chemical, 37 clastic, 36–37 Seeley, Harry Govier, 150 Seismic and volcanic activity, 31–32 Selective breeding, 61 Self-feeders, 288 Semilunate carpal, 316 Sereno, Paul, 15 Sex determination, biological, 407 ornamentation, 409–419 size disparity, 409 Sexual dimorphism, 60, 333 in birds, 410f in humans, 409f Sexual maturity, indicators of, 333 Sexual recombination, 65 Sexual selection, 59–61

Shared derived characters, 82 Sheep, foot postures in, 309f, 384f Shocked quartz, 527, 527f Shock metamorphism, 526 Shonisaurus, skull of, 249f Short bones, 128 Shunosaurus, life reconstruction of, 336f Shuvuuia deserti, 476 Siberian Traps, 516, 528 Sickle cell anemia, 55, 55f, 56 Sicknesses, 396 Silicification, 272 Siljan Ring, 513 Silurian Period (444–419 Ma), 111–112 Similarity vs. relatedness, 80–86 Sinocalliopteryx sp. S. gigas, 372, 372f stomach contents of, 372f Sinornithosaurus, 372 Sinosauropteryx sp., 342, 372, 454f, 474, 474f S. prima, 333f Skeletal adaptations that increase stability and efficiency, 311–312 Skeletal anatomy, 364–368 Skeletal map, navigating, 132–135 Skeletal muscle, 126 Skeleton; see also Bones; Skull Allosaurus, juvenile, 397f Amur leopard, 308f Archaeopteryx lithographica, 484f Deinonychus antirrhopus, 473f elephant, 308f functions of, 131 horse, 308f human, 310f Hypacrosaurus, adult, 412f kangaroo, 320f marsh deer, 308f Megatherium, 318f Oryctodromeus, 319f ostrich, 307f, 488f polar bear, 308f rabbit, 320f Zhouornis hani, 486f Skeletonization, 259f Skin, preserved, 331–332 Skull; see also Skeleton of alligator, 330f of Allosaurus, 330f of crocodylian, 362f of Deinonychus, 362f of Gallimimus, 471f of gharial, 359f of golden retriever, 329f of Lesothosaurus, 357f of Majungasaurus, 362f of Oviraptor philoceratops, 478f of Spinosaurus, 359f of tyrannosaurids, 219–220 of Tyrannosaurus rex, 362f, 410f of Wendiceratops, 365f Smilosuchus adamanensis, 119f Smith, William, 44, 50 Smooth muscle, 126 Snakes, 227–228 Social sciences, 3 Soft tissues, 294, 329, 408 Solar system, 19, 20f and Earth, 21–23 Solnhofen, Germany, 11 Somatic mutations, 65

545

Sordes, flesh reconstruction of, 241f Soundwaves, gravitational anomaly map created using, 527f Space, hypothesis that life came from, 103–104 Speciation, 67–68 Species recognition, 333 Spectroscopy, 103 Spinosaurus, 337, 359f Squamata, 251 Squamates, 227–228 Stabilizing selection, 59, 492–493 Stagonolepis robertsoni, skeletal reconstruction of, 232f “Starvation mode” catabolism, 440 Stegosaur, articulated mount (cast) of, 163 Stegosauria, 161–164 Stegosaurus, 13, 134, 134f, 159, 161–162 skeleton (cast) of, 162f Steno, Nicolaus, 40, 43 Stenonychosaurus, 366f Sternberg, Charles, 13, 14f Stethacanthus, 113, 114f Stomach, 365 Stomach contents, 371–373 Strata, 40 Stratigraphic dating, 40–46 Stride length, adaptations that increase, 305–308 Stride rate, increasing, 308–311 Stromatolites, 107, 107f Struthiomimus fore- and hindlimb proportions in, 484f skeleton (cast) of, 470f Stygimoloch spinifer, 178f Styracosterna, 167–171 Substrate, effects of, 379 Suchomimus, 15, 215f skeleton (cast) of, 216f skull (cast) of, 216f Supercontinents, 52 Suppurative osteomyelitis, 399 Swimming reptiles, 146, 243 Ichthyosaurs, 246–248 Mosasaurs, 251–253 Plesiosaurs, 249–251 Sympatric speciation, 67 Synapomorphies, 82, 85, 138 Synapsids, 143 Synsacrum, 493 Systematic review, 6 Systematics, 82 Systematics and phylogenetic relationships, 77 clades and cladistics, 86 cladogram, reading, 86–87 identifying characters, 88–91 grouping criteria: similarity vs. relatedness, 80–86 parsimonious evolutionary relationship, 93–94 phylogenetic relationships based on morphology and molecular evidence, 94 phylogenetics, 91–93 taxonomic classification, 78 binomial nomenclature, 80 traditional taxonomy, 78–80 Tail feather attachment, 479f Taphonomic biases, 267, 290

546

INDEX

Taphonomic loss, 139, 257 Taphonomy, 256 Taphonomy and fossilization, 255 biostratinomy, 258 bloat, 260–261 rigor, 259–260 scavenging and predation, 261–262 trampling and weathering, 264–265 transport, 262–264 case study, 272–274 diagenesis, 265 amount of oxygen, 266 burial environment and conditions, 267 ground and pore waters, 265 microbial activity, 266 organismal factors, 267 speed of burial, 265 type of sediment, 265–266 entering the rock record, 255–256 fossils, different types of, 267 carbon films/compression fossils, 269–270 impression fossils, 269 mold-and-cast fossils, 270 permineralization, 266f, 270, 271f recrystallization, 270 replacement, 271–272 unaltered fossils, 268–269 soft tissues, preservation of, 274 taphonomy and taphonomic loss, 256–258 Tarbosaurus, 14 Taxonomic classification, 78, 79f binomial nomenclature, 80 traditional taxonomy, 78–80 Tectonic boundaries, 25 Tectonic plate, 25, 26f Teeth of archosaurs, 145 of Carcharodontosaurus, 359f comparison of human tooth to horse tooth, 355f of dinosaurs, 17, 325, 353, 354f from sauropodomorph, 357f and tooth marks, 371 of Tyrannosaurus rex, 220, 359f Temperature of animal’s blood, 440 Teosinte, 62 Terrestrial animals, 244 Terrestrial depositional environments, 39 Terrestrial locomotor modes of vertebrates, 304 Terrestrial titans, 192 ancestral sauropodomorphs, 196–197 Diplodocoidea, 201–202 Macronaria, 202 Titanosauria, 203–207 Sauropoda, 197–201 Terrestrial vertebrates, 447 Terror birds, 531, 531f Tertiary consumers, 290 Testable hypothesis, 5 Tetanurae, 213–215 Tetanuran, skull of, 359f Tetrapoda, 141 Tetrapod bone, 457 Tetrapods bones in the forelimbs of, 84f origin, from fish-like ancestors, 9 Thagomizers, 164f

Thecodont dentition, 145 Theory, 7 Theory of evolution, 7, 11, 53 Therapsids, 114, 115 Theria, 83 Therizinosaur, 423 Therizinosauria, 477–478 Therizinosaurs, 322 Therizinosaurus claws from the manus of, 478f skeletal mount of, 477f Theropoda, 207 Allosauria, 216–217 Ceratosauria, 211–213 Coelophysoidea, 210–211 Coelurosauria, 218–220 Megalosauria, 215–216 Tetanurae, 213–215 Theropod dinosaurs, 207–208, 337–339, 366f, 392, 482f chewing muscles in, 364f fore- and hindlimb proportions in, 484f unique evolutionary features in, 222 Theropod eggs, 423 Theropod synapomorphies, 208–209 Theropod teeth, 208f, 358 of theropods, 208 Theropod tracks, 393f Thyreophora, 159 Ankylosauria, 164–165 Stegosauria, 161–164 Thyreophorans, 336–337 Tiktaalik, 9, 9f, 112, 112f Time averaging, 290 Time-telling, concept of, 43, 45f Tissue, types of, 125–127 Titanoboa, 228f Titanosauria, 203–207 Titanosaur nests, 428 Titanosaur osteoderms, 206f Titanosaurs, 199, 200f skeletal reconstructions of hips and hindlimbs of, 389f Toothless dinosaurs, 374 Tooth morphology, 353–359 Trabecular (spongy) bone, 129 Trace fossils, 268 Tracks individual, 381–384 vs. trackways, 381–389 Trackways, 376f, 384–389, 384f, 390f Traditional taxonomy, 78–80 Traits, sexually selected, 61 Trampling, 264–265 Transform boundary, 26, 29 Transport, 262–264 “Trees Down” hypothesis, 498–499 Triakis semifasciata, 141f Triassic crocodiles, 118 Triassic dinosaur, 158 Triassic–Jurassic extinction event, 120, 123 Triassic Period (252–201 Ma), 33, 33f, 117–120, 117f Triassic saurischians, 521 Triassic therapsid, 227f Triceratops, 13–14, 59, 151, 183, 335 extant phylogenetic bracket of, 92f growth series for, 335f skeleton of, 184f Tridactyl foot, of theropods, 208 Tridactyl footprint, 382f

Trilobites, 115 Tritium, 47 Trochanter, 145–146, 148 Troodon, 423 T. formosus, bone of, 459f Troodontidae, 480 Troodontids, 481 Troodontid teeth, 482f Trophic level, 288 pyramid of, 289f True dinosaurs, 147–150 Tui bird (Prosthemadera novaeseelandiae), 485f Anisodactyly in, 315f Tunguska event, 22, 22f Tunicate, 140, 140f Tupuxuara, skeleton of, 238f Turbinates, in the skulls of endotherms, 461f Turkey skull, 338f Turtle eggshells, 426 Turtles, 228–230 Tyrannosaurid dinosaur, 411 Tyrannosaurid synapomorphies, 219 Tyrannosauripus, 393 Tyrannosauroidea, 218 Tyrannosaur tooth, 263f Tyrannosaurus rex, 40, 79, 80, 207, 210, 292–298 arms of, 219f, 295–296, 297f, 321, 328–329, 329f brain endocast of, 294 chest of, 209f copulation, 419f extant phylogenetic bracket of, 92f fore- and hindlimb proportions in, 484f hindlimb of, 309f leg of, 209f medullary bone in fossils of, 416f running, 296 skull of, 220f, 362f, 411f teeth (cast) of, 220f, 358, 359f Unaltered fossils, 268–269 Uncinate processes, 493 Unconformities, 42, 43 Unguligrade horse, hindlimbs of, 309f Uniformitarianism, concept of, 42 Urey, Harold, 100 Ursus sp. U. americanus, heterodont dentition in, 353f U. arctos horribilis, 507f Variation, sources of, 65 genetic mutation, 65–66 sexual recombination, 65 Velociraptor, 338, 480 V. mongoliensis, 494f Vermivores, 349 Vertebrata, 141 Vertebrate paleontologists, 8 Vertebrates, 125, 519 Vestigial limbs, 227f Vitamins and minerals, storing, 132 Volcanic activity, 31–32 mapping of, 31 Volcanic eruptions, 22 Volcanic glass, 35 Volcanic igneous rocks, 35, 36f

INDEX Volcanic rocks, 49 Volcanism, excessive, 516 Volcanoes, 38 Wadati–Benioff zone, earthquakes in, 32f WAIR hypothesis, see Wing Assisted Inclined Running hypothesis Warm-blooded animals, 530 Warm-bloodedness, 440 Water, 21 first evidence for water on Earth, 51 hypothesis that life began in shallow bodies of, 101–102 sources of water for the earliest oceans, 21

Weathering, 264–265 Wegener, Alfred, 29 Wegener’s hypothesis, 30 Wendiceratops, 335f skull of, 365f W. pinhornensis, skull of, 180f Whale skeleton, 246f Wild corn, 61–63 Williston, Samuel, 500 Wing Assisted Inclined Running (WAIR) hypothesis, 500, 500f Wings, 492 of bat, 83–84, 85f, 235f of birds, 83–84, 85f, 235f of dragonfly, 83–84, 85f of pterosaur, 235f

Woolly mammoth, 264f Woven bone, 416 Yellowstone National Park, 102 Grand Prismatic Spring in, 102f Yinlong, 180 Yutyrannus, 338, 339f Zhenyuanlong suni, 472f Zhonghe, Zhou, 15 Zhouornis hani, skeleton of, 486f Zircon, 104 Zircon crystals, 101 Zuul crurivastator skull of, 165f tail club of, 165f

547