Stupid as a Fish?: The Surprising Intelligence Under Water [2024 ed.] 366268375X, 9783662683750

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Horst Bleckmann

Stupid as a Fish? The Surprising Intelligence Under Water

Stupid as a Fish?

Horst Bleckmann

Stupid as a Fish? The Surprising Intelligence Under Water

Horst Bleckmann Institut für Zoologie Universität Bonn Bonn, Nordrhein-Westfalen, Germany

ISBN 978-3-662-68375-0 ISBN 978-3-662-68376-7  (eBook) https://doi.org/10.1007/978-3-662-68376-7 This book is a translation of the original German edition “Dumm wie ein Fisch?” by Bleckmann, Horst, published by Springer-Verlag GmbH, DE in 2023. The translation was done with the help of an artificial intelligence machine translation tool. A subsequent human revision was done primarily in terms of content, so that the book will read stylistically differently from a conventional translation. Springer Nature works continuously to further the development of tools for the production of books and on the related technologies to support the authors. Translation from the German language edition: “Dumm wie ein Fisch?” by Horst Bleckmann, © SpringerVerlag GmbH Deutschland, ein Teil von Springer Nature 2023. Published by Springer Berlin Heidelberg. All Rights Reserved. © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer-Verlag GmbH, DE, part of Springer Nature 2024 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer-Verlag GmbH, DE, part of Springer Nature. The registered company address is: Heidelberger Platz 3, 14197 Berlin, Germany Paper in this product is recyclable.

For Angelika, Julia and Lisa

Foreword

As dumb as a fish: what people know about fish A world underwater: There are about 33,000 species of fish, the most diverse group among vertebrates. The number of mammal species is only about 5500, and the number of bird species is about 10,000. Fish live in ponds, rivers, and the oceans of our Earth. From puddles in dry areas to the depths of the oceans, they inhabit almost all waters of our planet. Their sensory physiological performances are as diverse as the environmental conditions under which they live: Some fish can perceive and generate electrical fields and orient themselves excellently with the help of their sense of sight or lateral line system. Many fish orient themselves on their migrations over thousands of kilometers with the help of their sense of smell, sense of hearing, or even with the help of the Earth’s magnetic field. The sensory information of the fish is processed by a brain that is similar in many parts in structure and function to the mammalian brain. It is therefore not surprising that many cognitive performances of fish are similar to those of birds and mammals. It is an amazing kaleidoscope that the author opens up about the behavior, cognitive abilities, and the world of senses of fish. Fish live in water, a medium that is rather foreign to us. Terrestrial vertebrates such as dogs, cats, or birds are much more familiar to us. For many of us, fish remain strange cold-blooded creatures to which we do not attribute great behavioral achievements. The brilliantly written book of an internationally significant biologist will thoroughly dispel this prejudice. There is an almost overwhelming amount of specialist literature on fish, due to the scientific interest of biologists, but also because of their high vii

viii      Foreword

economic importance for our nutrition. In the daily press, we often read about fishing quota regulations within the European Union. In addition, there are reports from hobby anglers, aquarists, and sport divers, whose leisure activities are significantly influenced by fish. Therefore, there is an immense amount of enthusiast literature—but also outstanding TV documentaries like “The Blue Planet”, which bring us closer to the world under water. What was missing was a scientific presentation about the sensory and behavioral biology of this remarkable and mostly underestimated group of animals for laypeople. Karl von Frisch broke new ground with his book “Aus dem Leben der Bienen” (“From the Life of Bees”) many decades ago, later Bert Hölldobler and Edward O. Wilson (“The Ants”) masterfully dealt with ants. Konrad Lorenz brought us closer to the life of geese and domestic dogs. The cognitive abilities of birds were recently described in the book “Die Genies der Lüfte” (“The Geniuses of the Skies”) by Jennifer Ackermann. At least we never considered birds and mammals to be stupid. The structures and functions of living beings and their implementation in innovative technologies, as well as the preservation of biodiversity, connect the author of these lines with the book author. This is complemented by decades of familiar and friendly collaboration in the shared university faculty: the background against which a botanist is allowed to write the foreword to a fish book. The author Horst Bleckmann is one of the most renowned sensory physiologists. He studied in Giessen and Frankfurt and worked for many years in California (Scripps Institution of Oceanography), but also at Ohio State University, Oregon State University, University of Melbourne, Shanghai Ocean University, and other institutions. Since 1994, he has been a full professor of Zoology and Neurobiology at the University of Bonn. His area of interest as a neuro-, sensory-, and behavioral biologist includes not only fish, but also crocodiles, squids, seals, sea snakes, peregrine falcons, semiaquatic spiders, spitting cobras, and the infrared sense of insects. His work is recognized and awarded worldwide (including the Karl-Ritter-von-Frisch Medal of the German Zoological Society), he is a member of the Academy of Sciences and Literature in Mainz, the Austrian Academy of Sciences, and the National Academy of Sciences Leopoldina. The most extraordinary thing about his work is the ability to see his own research in a broad framework and context: He not only recognizes possible applications of biological results for technical innovations (bionics), but also sees with great clarity the long-emerging environmental changes in the broad context of the loss

Foreword     ix

of biodiversity, globalization, and the world population that is far too high for the carrying capacity of our earth. “It is probably already 5 past twelve” he warns at the end of this book with regard to the global environmental changes, which not only affect the fish. Bonn im Dezember 2021

Wilhelm Barthlott

Preface

If you are not an aquarist, angler, or scuba diver, you probably know fish mainly as sea bream, carp, or trout on your plate. There it lies, colorless and lifeless, staring at you with glassy eyes, provided it is reasonably fresh. Even fish in an aquarium often leave a rather boring impression on the observer, not least because they cannot change their facial expression and their gill covers move in monotonous uniformity. The idea that fish can also be the subject of exciting scientific investigations may seem rather unlikely to you. As far back as I can remember, I have been interested in animals and their behavior. Initially, I didn’t find fish particularly interesting, they didn’t hold nearly the same fascination for me as African large mammals, dolphins, or birds of prey. As a city child, it was pigs and cattle in the stables of the nearby slaughterhouse, and of course dogs and horses, that interested me. Initially, instead of the desired dog, my parents only gave me a budgerigar. I got my first dog when I was twelve, and a second dog followed when I was nineteen. In training these dogs up to protection dog level III, I learned a lot about animal behavior. My scientific interest in animals and conservation was only awakened by the magazine “Das Tier”. This magazine, published by Bernhard Grzimek, Heini Hedinger, and Konrad Lorenz in 1960, fell into my hands as a thirteen-year-old in the waiting room of a veterinary practice. From then on, it became my constant reading. A few years later, I learned from Konrad Lorenz or from his books that behavioral researchers (ethologists) scientifically study animal behavior. I found this extremely exciting, I wanted to become an ethologist.

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During my biology studies at the University of Giessen, I attended a lecture by Prof. Erich Schwartz on the sensory and nervous systems of animals in my 3rd semester. The goal of sensory biology is to understand which sensory organs animals are equipped with, how sensitive sensory organs respond to environmental stimuli, which information they transmit to the brain, and where and how this information is processed in the brain. Until the fifties of the last century, the brain was still considered a “Black Box”, but new physiological measurement methods allowed the electrical activity of the brain to be recorded down to the level of the individual nerve cell. This made it possible for the first time to attempt to establish a causal relationship between brain activity and simple behaviors. A subfield of ethology had transformed into neuroethology. I found this exciting. At the University of Giessen, Erich Schwartz was the only zoologist who dealt with questions of sensory and behavioral biology during my studies. All other professors in the biological faculty were cell biologists, or they studied the body structure (morphology), metabolism, ecology, or genetics of animals. I also found ecology exciting, but at that time in Giessen, it did not go beyond purely descriptive faunistics. That was too little for me, as I was more interested in physiological or ecological mechanisms and laws. Fish have a sensory system that allows them to perceive local water movements. This system is referred to as the lateral line system. Erich Schwartz was interested in the significance of the lateral line system in the behavior of fish. As a result, I ended up writing my diploma and doctoral thesis not about mammals or birds, but about fish. Surface-feeding fish can use their head lateral line to perceive surface waves involuntarily generated by insects that have fallen into the water, and locate the wave center and thus the prey. How they do this was only partially known. I found the topic fascinating, but I only realized how interesting fish actually are as research objects many years later during a three-year research stay at the Scripps Institution of Oceanography in La Jolla, Southern California. There, the internationally renowned scientists Theodor Holmes Bullock and Glenn Northcutt taught and researched. T.H. Bullock, who died in 2005, was one of the most prominent comparative sensory and neurobiologists during his lifetime, he wrote numerous works on the sensory systems, the function of the central nervous system and the behavior of fish. Northcutt was or is a comparative neuroanatomist. He is particularly interested in the structure and evolution of the brains of fish (and other vertebrates). The aim of my research work in Southern California was to learn more about the central nervous processing of lateral line information in the brains of rays and sharks.

Preface     xiii

When you look in relevant databases, you come across countless popular science books about birds, and that’s a good thing. Books about mammals are less common in the databases, but it becomes really sparse when you search for popular science literature about the sensory biology, the nervous system, and the cognitive abilities of fish. This book is intended to help fill this gap. It is aimed at aquarists, anglers, sport divers, and biology students, as well as anyone interested in animals, their sensory systems, and their behavior. Worldwide, there are approximately 5500 extant (still living) mammal species, 10,000 bird species, 9500 reptile species, and 6700 amphibian species. Together, this amounts to 31,700 species. The number of fish species, at over 33,000, is roughly the same size, meaning that fish make up half of all known vertebrate species. This high number already indicates that fish are an extremely successful group of vertebrates, which, in the course of their evolution, have colonized all aquatic habitats, from the waters of the tropical rainforests to the ponds, lakes, and rivers of the temperate and arctic climate zones. Even the temporary waters in the semi-deserts of the earth are inhabited by some fish species. In the world’s oceans, fish are primarily found near the coast (e.g., in coral reefs, seagrass meadows, lagoons, and mangroves), but they are also found in the open ocean and in the deep sea. It is therefore not surprising that fish show great differences in terms of their size (whale sharks can be up to 14 m long, the minnow Paedocypris progenetica reaches a body length of only 10 mm) and shape, as well as in terms of their sensory systems and their behavioral performances. When I find myself at a party conversing with unfamiliar guests, the question often arises as to what I was scientifically involved with during my active time as a university professor. I then explain that my colleagues and I, among other research areas (e.g., bionics and the infrared sense of some insect and snake species), have primarily studied the sensory and central nervous performances and cognitive abilities of fish. The facial expression of my counterpart usually unmistakably reveals that there probably isn’t much to research in this regard. This skepticism once culminated in the question of whether fish even have a brain. This book aims to eliminate prejudices and ignorance about fish. It is intended for the interested layperson, who often has little or no basic knowledge in the field of sensory and behavioral biology of fish, but also for biology and teaching students who want to learn more about fish. The research results are simplified in this book, but hopefully always correctly, presented.

xiv      Preface

When writing a non-fiction book, the question always arises as to how precisely one should explain a matter. If you stay too superficial, you lose the particularly interested reader, if you go too deep, there is a risk that some readers will be deterred. After my running partner and educator Uli Groneick had read parts of the manuscript in advance with interest, he asked: “Do you really need to know all this in such detail?” Of course, you don’t have to. To cater to different readers, particularly difficult matters are presented in boxes. Even without knowing the content of these boxes, the rest of the book remains understandable. The book aims to inform the reader about the exciting world of fish. Decide for yourself whether I have succeeded in this. Alfter Germany

Prof. Dr. Horst Bleckmann

Acknowledgment

I thank Wilhelm Barthlott (Bonn), Theo Bakker (Bonn), Gerhard von der Emde (Bonn), Fabian Herder (Bonn), Joachim Mogdans (Bonn), Dennis Rödder (Bonn), Vera Schlüssel (Bonn), Stefan Schuster (Bayreuth), Guido Westhoff (Hamburg), and Mario Wullimann (München) for suggestions, discussions, and improvement proposals. Uli Groneick has taken on the task as an educator and running partner, and my neighbor Heinz Imbach as a master painter, to read parts of the manuscript and make suggestions on how the text can be kept understandable for “non-fish burdened” laypeople. I also received valuable help from Gerold Hensch (Hattingen), with whom I shared a school desk and who, as a trained economist, also pointed out passages that were too difficult for laypeople. I hope that the text has become more readable through their constructive criticism. I thank Ms. Dung (Bonn) and Mr. Lay (Breisach) for their help in creating the illustrations. Special thanks go to Ms. Mechler from Springer Verlag for the good cooperation during all phases of this book project.

xv

Contents

1 General Introduction 1 References 3 2 What is a Fish? 5 References 9 3 The Sensory World of Fish 11 3.1 The Sense of Smell 14 3.1.1 Olfactory Organs 14 3.1.2 Sensitivity of the Sense of Smell 16 3.1.3 Chemical Messengers and Pheromones 17 3.1.4 Escape Reactions 18 3.1.5 Spatial Orientation 19 3.1.6 Smell and Water Pollution 19 3.2 The Sense of Taste 20 3.2.1 Taste Organs 20 3.2.2 Sensitivity of the Sense of Taste 21 3.3 The Visual System 22 3.3.1 The Vertebrate Eye 22 3.3.2 Light in the Aquatic Habitat 26 3.3.3 Further Adaptations of the Fish Eye 30 3.4 The Sense of Touch 37 3.4.1 Touch Receptors Using the Example of Humans 37 xvii

xviii      Contents

3.4.2 Touch Receptors of Fish 38 3.4.3 Fish Read Braille 40 3.5 The Lateral Line System 43 3.5.1 Lateral Line Organs 43 3.5.2 Function of the Canal System 46 3.5.3 Biologically Relevant Stimuli 50 3.5.4 Hydrodynamic Noise 52 3.5.5 Lateral Line and Behavior 53 3.6 The Sense of Balance 62 3.6.1 Anatomy of the Inner Ear 62 3.6.2 Function and Performance of the Sense of Balance 63 3.7 The Sense of Hearing 64 3.7.1 The Ear of Mammals 64 3.7.2 The Ear of Fish 66 3.7.3 The Ears of Fish (Hearing Generalists) 69 3.7.4 Sound Localization 70 3.7.5 How Well and Why Can Fish Hear? 72 3.7.6 Why Can Mute Fish Hear? 74 3.8 The Electric Ssense 75 3.8.1 Ampullary Organs 75 3.8.2 Passive Electric Sense 77 3.8.3 Active Electric Sense 79 3.8.4 The Electric Sense of the Elephant Nose Fish 83 3.8.5 Jamming Avoidance Behavior 86 3.9 The Magnetic Sense 89 3.9.1 The Discovery of the Magnetic Sense 89 3.9.2 The Earth’s Magnetic Field 90 3.9.3 The Magnetic Sense of Bony Fish 90 3.9.4 The Magnetic Sense of Cartilaginous Fish 93 3.9.5 Magnetic Field Receptors 95 3.10 The Sense of Pain 96 3.10.1 Do Fish Feel Pain? 96 3.10.2 Unconscious Pain Perception 97 3.10.3 Conscious Pain Perception 98 3.11 Why So Many Senses? 100 References 102

Contents     xix

4 The Central Nervous System of Fish 107 4.1 Structure of the Brain 107 4.2 Evolution of the Brain 114 4.3 Comparison Fish Brain—Mammalian Brain 115 4.4 Physiology of the Fish Brain 118 4.4.1 Neuronal Maps 118 4.4.2 Reafference Principle 119 4.4.3 Sensory Pathways 122 References 123 5 Behavior 125 5.1 Evolution and Behavior 125 5.1.1 Group Selection 128 5.1.2 The King Selection 131 References 133 6 Cognitive Abilities of Fish 135 6.1 How is Intelligence Measured? 135 6.2 The Performance of Small Brains 137 6.3 Cognition without Cortex? 138 6.4 What is Cognition? 140 6.5 Learning and Memory 141 6.6 Optical Illusions 145 6.7 Object Categorization 148 6.8 Reversal Learning 151 6.9 Symmetry Perception 152 6.10 Spatial Orientation 153 6.11 Topographic Memory 154 6.12 Emotional Memory 156 6.13 Numerical Competence 156 6.14 Perception of Movement 160 6.15 Archerfish 161 6.16 Tool Use 166 6.17 Cleaner Fish 167 6.18 Social Learning 171 6.18.1 Enemy Avoidance 171 6.18.2 Aggression and Dominance 173 6.18.3 Mate Selection 176 6.18.4 Cooperation 177

xx      Contents

6.18.5 Tit for Tat 179 6.18.6 Mutualism 180 6.18.7 Social Life and Stress Management 181 6.18.8 Fish Personalities 181 References 184 7 Threat to Fish Fauna 187 7.1 Global Biodiversity Crisis 187 7.2 Freshwater Fish 189 7.2.1 Water Pollution 189 7.2.2 Plastic, Microplastic, and Other Waste 191 7.2.3 Straightening of Rivers 191 7.2.4 Locks and Dams 192 7.2.5 Water Extraction for Agriculture 195 7.3 Marine Fish 195 7.3.1 Commercial Fishing 195 7.3.2 Pollution of the World’s Oceans 198 7.3.3 Fish Farms 198 7.3.4 Coral Reefs 199 7.3.5 Pet Trade 200 7.3.6 Tourism 201 7.3.7 Acoustic Water Pollution 203 7.3.8 Invasive Species 204 7.3.9 Deny, delay, do nothing 205 References 206

1 General Introduction

Fish, like all animals, constantly receive information from their environment using sensory organs. Some sensory organs are easily recognizable as such, others are barely or not at all visible to the naked eye. For example, the large eyes of many fish species are striking, indicating to even the layman that many fish have excellent vision. In addition to vision, the sense of smell and taste of many fish species is also very well developed. Fish, unlike mammals, do not have earlobes or ear openings, yet many fish have excellent hearing. The sense of touch has great, but often underestimated, importance for us. A gentle touch can comfort or trigger a pleasant tickling sensation, while a firm touch is usually perceived as unpleasant. With the sense of touch, we can recognize a familiar object even in the dark and can—in conjunction with joint receptors and temperature sensors in the fingers—even roughly determine its material properties. Fish also have a sense of touch, which is excellently developed in many species, but has so far been little researched. In addition to the sense of touch, fish also have a “remote sense of touch” with which they can perceive local water movements and pressure gradients. This sense is based on their lateral line system. Many fish can sense weak, foreign or self-generated electric fields. In addition to the lateral line system, this sense gives them the ability to communicate within the species, for spatial orientation, and for the perception of prey, enemies or inanimate objects. Many fish use the Earth’s magnetic field for near or far orientation. Without a magnetic sense, migrations over long distances in the open ocean would probably not be possible at all. Until recently, it was doubted that fish feel pain. However, recent studies suggest that this is the case. © The Author(s), under exclusive license to Springer-Verlag GmbH, DE, part of Springer Nature 2024 H. Bleckmann, Stupid as a Fish?, https://doi.org/10.1007/978-3-662-68376-7_1

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2     H. Bleckmann

In addition to a multitude of high-performance sensory systems, fish have complex brains that process the information received from the sensory organs and subsequently generate behavior. The organization of the fish brain largely resembles that of the mammalian brain. The same applies to the physiological mechanisms by which fish brains function at the cellular and network level. Since the behavior of fish is subject to the same selection mechanisms as the behavior of mammals and birds, many fish also show extraordinary cognitive performances. Worth mentioning in this context is, for example, the cleaner wrasse Labroides dimidiatus living in tropical reefs. This fish frees other fish (clients) from parasites and can distinguish and serve up to 300 “clients” individually. Through comparative studies, zoologists have learned a lot about the sensory systems and cognitive abilities of fish in the last fifty years. However, the exciting results achieved in this process have unfortunately remained largely hidden even from the interested layman. As a scientist, one should be critical. Therefore, I have always endeavored to encourage my students to think critically. When a university professor, teacher, politician, journalist, or the Pope makes a claim, one should at least ask the question “how does he actually know that?” for important topics. If one does this, one will often find that the interlocutor cannot substantiate many of his claims, so the claims are based more on a subjective, usually emotional assessment or belief. The damage that non-science-based opinions can cause is evidenced by many fake news from recent history. During my doctorate, I attended a lecture on biophilosophy at the University of Giessen. I wasn’t particularly interested in the topic, but as a good doctoral student, I felt obliged to attend all the lectures offered as part of the Biological Colloquium. The speaker began his lecture with the introduction: “When you get into a conversation with a stranger at a party, the question of what you studied comes up sooner or later. If the answer is chemistry, the interlocutor immediately makes it clear that he has no idea about chemistry. The same happens when you mention mathematics, physics, or engineering as your field of study. Often, ignorance in the natural sciences is even seen as something positive, or at least as something excusable. If you tell your counterpart in the conversation that you are a zoologist and are interested in animal behavior, everyone is an expert (or expert woman), regardless of whether it is about evolutionary or behavioral biological topics (sociologists, educators, and psychologists probably have similar experiences). Plausible explanations and limited personal experiences are apparently enough for most people to believe they have understood the world. Even educated laypeople or politicians are often not aware that even plausible explanations can be wrong. And even correlations do not say

1  General Introduction     3

anything about whether there is a direct causal relationship between two variables. A frequently cited example is the decline in storks and the simultaneous decline in the human birth rate in the sixties of the last century. And arguing about the correctness or falsity of claims that cannot be refuted is a pure waste of time.” The content of this book is based on the results of scientific investigations. The authors of the investigations are often not mentioned, as their names will be meaningless to most readers. However, at the end of each chapter, journal articles and books are listed that the particularly interested reader can refer to for further reading on specific questions. Carl von Linnaeus introduced the two-part naming system (binomial nomenclature) for the designation of plant species in 1753. The binomial nomenclature was then incorporated into the 10th edition of his book “Systema naturae” in 1758. The binomial nomenclature stipulates that each animal and plant species is designated by a noun and a lowercase word (usually an adjective). For example, the scientific name of modern humans is Homo sapiens. Homo refers to the genus and sapiens to the species. It is common to write the scientific name of an animal or plant species in italics. I have followed this tradition. In this book, in addition to the common names, the Latin or Greek names of the discussed fish species are usually mentioned. This has three reasons: 1. A clear species assignment is often not possible with the help of the common name. 2. The experimental result achieved in the research of only one fish species must not be generalized. Because if, for example, the examined fish species can distinguish colors, this does not mean that all fish can distinguish colors. Other, even closely related fish species could be colorblind or even blind (e.g., many cave fish). 3. The scientific species names are intended to give the particularly interested reader the opportunity to learn more about the respective species—e.g., through reference works or an internet search. In some cases, instead of the species name, only the abbreviation sp. (for species ) is given as an addition behind the genus name (e.g., Gasterosteus sp. ). In this case, the exact species is either not known, or what has been said applies to several species of this genus.

References Linne, C. von. (1735). Systema naturae, sive regna tria naturae systematice proposita per classes, ordines, genera, & species. Wehner, R., & Gehring, W. (2013). Zoologie. Georg Thieme Verlag.

2 What is a Fish?

Fish in the narrower sense are aquatic vertebrates that possess a jaw joint, breathe with gills, and have several paired and unpaired fins. Since water is not as easily displaced as air, the typical fish is spindle-shaped, laterally flattened, and shows a gradual transition of the three body regions head, trunk, and tail. Also typical are the skin teeth of sharks (they correspond in structure and development to the teeth of vertebrates) and the scales of bony fish, which consist of bone plates layered like roof tiles. The skeleton of sharks and rays is cartilaginous. In bony fish, as the name suggests, the skeleton is almost completely ossified. In a broader sense, the term fish also includes jawless hagfish and lampreys. Although fish are a group of animals with a similar body structure, they do not form a closed lineage community. After all, the land vertebrates emerged from a group of fish in the course of evolutionary history. The hagfish and lampreys, with over 100 still living (extant) species, form a residual group of the once widespread jawless vertebrates, which first appeared 450 to 470 million years ago. Hagfish are exclusively marine, they lack, like the lampreys, paired fins. They feed on worms, dead fish, and beached whales. Lampreys live in the sea or in freshwater (e.g., the river lamprey). Even saltwater living, i.e., marine lampreys, spend their lives as larvae initially in rivers and streams. Only after transformation (metamorphosis) into the adult form do they migrate to the sea, and after reaching sexual maturity, they return to their home waters for mating and egg laying. Lampreys are parasites. They attach themselves to living fish with a suction disc and tear out pieces of tissue with horn teeth. © The Author(s), under exclusive license to Springer-Verlag GmbH, DE, part of Springer Nature 2024 H. Bleckmann, Stupid as a Fish?, https://doi.org/10.1007/978-3-662-68376-7_2

5

6     H. Bleckmann

Sharks are, as they sometimes attack swimmers or divers, probably known to everyone from press reports. About 50 shark attacks on humans are counted each year, up to 15 of which are fatal. In contrast, about 100 million sharks are killed by humans each year. Falling coconuts kill about 150 people each year, and according to the World Health Organization, traffic causes up to 1.2 million deaths worldwide. Sharks are therefore only slightly dangerous to humans. My only encounter with sharks was on my first dive. I attended a marine biology congress on Heron Island (Australia), where the latest findings on the sensory systems and central nervous systems of fish were presented and discussed. As usual, all participants had an afternoon at their disposal. One excursion offered by the organizers for this afternoon was a dive to a coral reef off the island. A valid diving certificate was a prerequisite for participation, which I did not have at the time. The solution offered to me and Christopher Brown (an American zoologist) was a two-hour crash course in the hotel’s swimming pool. After we had reached our diving area, a diving instructor was provided to us for safety reasons. Once we arrived at the anchor point, we slowly descended with the help of the anchor rope. At a depth of ten meters, we reached the flat sandy bottom where we were to spend the next thirty minutes. After a short time, the first reef sharks appeared. They approached curiously, but immediately retreated when we moved towards them. Back in Germany, I immediately signed up for a diving course. My logbook now lists almost 100 dives, most of them in the Red Sea, but also some off the coast of Kenya and the Florida Keys. I vividly remember a dive in the Florida Keys. I attended a conference organized by DARPA (Defense Advanced Research Projects Agency) in Florida. DARPA is an agency of the United States Department of Defense and also supports basic research by German scientists, provided their field of work appears relevant. As in Australia, we had an afternoon at our disposal. Among the conference participants were two combat swimmers from the United States Army. Somewhat naively, I joined their dive as a proud holder of a recently acquired diving certificate. The combat swimmers watched my diving efforts for about thirty seconds, grabbed me by the valve of the air tank, and pulled me down with them. We didn’t see any sharks on this dive, but we did see large barracudas, which left a lasting impression on me with their sharp teeth and rigid gaze. Sharks belong to the cartilaginous fish. Although cartilaginous fish do not have a bony skeleton, they descend from bone-bearing ancestors. This is evidenced by their characteristic skin teeth. Cartilaginous fish first appeared

2  What is a Fish?     7

as predatory, agile open-sea swimmers about 400 million years ago (in the Lower Devonian). In addition to sharks with about 500 species, the cartilaginous fish include rays with about 630 species and chimaeras with more than 30 species. Almost all cartilaginous fish live in the sea, but some shark and ray species are found temporarily or exclusively in the estuaries and lower reaches of large rivers. The cartilaginous fish have remained almost unchanged in their essential structural features for several million years. The extant bony fishes include the ray-finned fishes (their fins consist exclusively of skin and bony fin rays) and the lobe-finned fishes (their pectoral and pelvic fins are muscular and supported by bone elements). Evolutionarily, the bony fishes are about as far removed from the cartilaginous fishes as mammals are from birds. Fossil bony fishes appear before the cartilaginous fishes. The oldest extant bony fishes include the lungfishes (lungfish, eel), the cartilaginous ganoids (sturgeon, spoonbill sturgeon), the bony ganoids (alligator gar, pike) and the bowfins (mudfish). Approximately 96% of all extant bony fishes belong to the true bony fishes, the Teleostei. These include, for example, the goldfish (Carassius auratus), the brown trout (Trutta trutta) and the pike (Esox lucius). The oldest representatives of the Teleostei already existed in the Triassic period about 220 million years ago. The true bony fishes reached their greatest diversity of forms between 144 and 65 million years ago and in the early Tertiary (66 to 2.6 million years ago). In contrast to the cartilaginous fishes, the original bony fishes lived almost exclusively in freshwater. With the beginning of the Mesozoic era (250 to 66 million years ago), fossils are almost exclusively marine Teleostei. Since the early Tertiary, numerous forms have again penetrated into the river systems of the continents. The evolution of the Teleostei has in part proceeded extremely quickly. For example, a large part of the approximately 500 cichlid species of Lake Victoria in Africa only emerged within the last 15,000 years. For comparison: mammals first appeared on earth about 300 million years ago, humans have existed for about 3 million years. Although freshwater only accounts for 3% of the total water on earth, today about 40% of all Teleostei live in freshwater. These include, among others, the perch, carp and brown trout. In the recent fish fauna, the lobe-finned fishes are represented by only eight species, which occur exclusively on the southern continents. They had their greatest diversity of forms in the Devonian (420 to 360 million years ago) and only occurred in freshwater. The land vertebrates emerged from the lobe-finned fishes, which include the lungfish (six species) and the coelacanths (two species). The simplified family tree shown in Fig. 2.1 shows that the coelacanths are more closely related to the land vertebrates than to the true bony fishes (Teleostei).

8     H. Bleckmann

Terrestrial vertebrates Lobe-finned fishes

Lungfishes

Coelacanths

True bony fish Extant bony fish

Bowfins Gars

Sturgeons Ray-finned fishes

Bichirs

Cartilaginous fishes Lampreys

Hagfishes Fig. 2.1  Simplified family tree of the fishes and land vertebrates

This book deals almost exclusively with cartilaginous fishes (excluding sea cats) and true bony fishes (Teleostei). The reason for the limitation to cartilaginous fishes and true bony fishes is that we have the most knowledge about the sensory biology, the brain and the behavior of rays and sharks and the true bony fishes. Whenever this book talks about “fish”, the reader should keep this limitation in mind.

2  What is a Fish?     9

Summary In this chapter, the reader learns which vertebrates belong to the fishes, how many extant fish species there are, what differences exist between cartilaginous fishes, true bony fishes, hagfish, lampreys and lobe-finned fishes, and how the evolution of fishes has proceeded. A simplified family tree of the fishes is shown for further explanation.

References Fiedler, K. (1991). Wirbeltiere. 2. Teil: Fische. In D. Starck (Ed.), Lehrbuch der Speziellen Zoologie. Gustav Fischer Verlag. Helfmann, G., Collette, B. B., Faey, D. E., & Bowen, B. W. (2009). The diversity of fishes: Biology, evolution, and ecology. Wiley-Blackwell. Nelson, J. S. (2006). Fishes of the World. Wiley.

3 The Sensory World of Fish

You probably learned in school that humans have five senses. These are the sense of sight, hearing, smell, taste, and touch. There are also a multitude of other senses, such as the sense of balance, rotational sense, temperature sense, and pain sense. Just like us, almost all fish have all of the mentioned sensory systems. In addition, many animal species have an electric sense and a magnetic sense. Fish of different species often inhabit very different habitats, which is why many fish are equipped with very different sensory systems. The respective equipment with sensory organs largely determines which environmental stimuli a fish perceives. Each fish (each animal) thus lives in its own sensory world, which can completely differ from the sensory world of other animals (just think of the sensory world of a tapeworm living in the intestines of mammals or that of a golden eagle). To find out which sensory systems fish are equipped with and what behavioral performances can be achieved with these sensory systems, there are numerous methods (see Box 1). Box 1 Methods of sensory and behavioral biology. How can we find out which environmental stimuli fish can perceive, where and how these stimuli are processed in the brain, and what behavioral performances fish are capable of? An important research approach is to observe fish in their natural habitat, carefully record and quantify their behavior. With this method, for example, we can learn that clownfish (Amphiprion percual) prefer to stay near sea anemones, hide their young in a sea anemone, and defend the sea anemone against predators. If we want to learn about the sensory performances and cognitive abilities of fish, we must conduct controlled behavioral experiments in the field or in the lab. A method often used in this context is operant conditioning.

© The Author(s), under exclusive license to Springer-Verlag GmbH, DE, part of Springer Nature 2024 H. Bleckmann, Stupid as a Fish?, https://doi.org/10.1007/978-3-662-68376-7_3

11

12     H. Bleckmann Let’s assume we want to know if goldfish (Carassius auratus) can see colors. To answer this question, we show the fish two differently colored objects at the same time (e.g., a blue and a yellow triangle). If the test fish swims randomly to the blue object, it is rewarded with food. If it swims to the yellow object, the food reward is omitted. If the fish can distinguish colors, they will prefer to swim to the blue object after some time. To avoid location training, we must of course randomly swap the locations where the objects are presented. To avoid giving the animals additional distinguishing features, the objects should have the same shape, size, and surface texture and smell the same. If our test fish reliably (e.g., in 70% of ten trials on three consecutive test days) only swim to the blue object, we can use statistical methods to indicate the probability with which the fish can distinguish, for example, blue from green. To provide the final proof, another control test is still missing, because the fish could also have distinguished the objects based on their gray values (a yellow object appears brighter on a black and white image than a blue object). Only when the fish recognize the blue object reliably in the environment of several differently bright (differently gray) objects, have we provided proof that they can distinguish blue from yellow. The experimenter must absolutely avoid giving the test animal unconscious hidden clues about the correct solution during behavioral experiments. Before the first World War, Clever Hans—the horse of the mathematics teacher Wilhelm von Osten—attracted great attention. Clever Hans could apparently solve arithmetic problems and count objects or people. If, for example, the horse was given the arithmetic problem 3 x 3, it scraped nine times with a front hoof. The horse’s arithmetic performances soon also made behavioral scientists curious, who did not believe in the horse’s arithmetic skills. A thirteen-member commission led by philosophy professor Carl Stumpf, who was a member of the Prussian Academy of Sciences, finally got to the bottom of the phenomenon. The members of the commission initially suspected a trick or fraud on the part of the mathematics teacher. However, the commission’s experiments showed that the horse also solved a task correctly when von Osten was not present and a stranger posed the task. The experiments also showed that the horse only solved the task when the stranger could calculate, i.e., knew the correct solution. The researchers finally found out that Clever Hans recognized from the smallest changes in facial expression and body posture of his human counterpart when he had to stop scraping with a front hoof. Unconsciously, the questioners adopted a different facial expression before the decisive “correct” last hoof scrape. In addition, after the “correct answer”, they expressed—unintentionally—signals of relief with their body language, which “Clever Hans” perceived in about 90% of all cases and converted into the desired behavior. One can also use the method of operant conditioning to learn something about the cognitive abilities of an animal. With the help of operant conditioning (if the fish does something right, it gets food, if it does something wrong, it gets nothing), we can, for example, find out whether or how well fish can orient themselves spatially, which strategies they use in the process, and which brain areas they need for their orientation performance (see further below). In addition to operant conditioning, there is classical conditioning. It was discovered by the Russian physician and physiologist Ivan Petrovich Pavlov, who died in 1936. Pavlov showed that a natural, usually innate (unconditioned)

3  The Sensory World of Fish     13

reaction to a stimulus can be supplemented by learning a new (conditioned) reaction. Pavlov was able to prove this through experiments with dogs. When a dog smells food, it triggers salivation (innate reaction). If Pavlov produced a sound a few seconds before feeding the dog, the salivation (unconditional reaction) began after only a few attempts immediately after the sound (condtitoned reaction). The dog had learned that it always received a food reward after the sound. You probably know something similar from your dog. When you reach for the leash at the coat rack, the dog wags its tail. It has learned that after you reach for the leash, you always take it for a walk. In this case, the walk, not the food, is the reward. With the help of classical conditioning, one can also learn a lot about the sensory systems and cognitive abilities of an animal. For example, one can find out whether fish can hear. The gill cover movement or the breathing rate are suitable as behavioral responses, and instead of rewarding, we punish the fish. To find out whether a fish can hear, we record the frequency of its gill cover movement with a camera. At rest, the fish closes and opens its gill covers about once every two seconds. If a sound is produced for a few seconds using a speaker and at the end of the sound the fish is given a harmless but unpleasant electric shock, its breathing rate changes for a short time (unconditioned reaction). After a few attempts, one observes a change in the breathing rate even if the electric shock is omitted (conditioned reaction, the fish is now classically conditioned). Because as soon as it hears the sound, the fish expects a mild electric shock based on its negative experiences. The result is a change in its breathing rate. With this simple method, one can prove that fish can hear. The method of classical conditioning is versatile, because we can now also find out how sensitive a fish is and which frequencies it can hear, whether and how well it can distinguish different frequencies or volumes, and whether or how accurately it can determine the direction and distance of a sound source (see further below). Instead of the breathing rate, we could also record the heart rate, because that also changes when a fish expects an unpleasant stimulus. However, one must always consider in conditioning experiments that not every reaction can be conditioned with any stimulus. Rats associate sounds with pain sensations, triggered by weak electric shocks. But they associate nausea, caused for example by X-ray radiation, with the food they last consumed. The rats will avoid this food in the future, as nausea under natural conditions indicates poisoning. On the other hand, it is not possible to condition a sound signal with nausea or a certain taste with pain. These are stimulus-reaction combinations that never occur in normal life. How can one find out what information a sensory organ sends to the brain? This question can be clearly answered with physiological methods. Let’s first take an example from technology. We want to know whether or what voltage is present at the socket in our living room. We buy a voltage meter at the hardware store, plug one electrode of the meter into the positive pole and the other into the negative pole of the socket. After switching on the meter, we get a result of 230 V and 50 Hz (Hz = oscillations per second) in Germany. If we want to know whether or how sensitive sensory cells react to a stimulus, we proceed in a similar way. We measure the voltage difference between the inside and outside of a sensory cell, i.e., the membrane potential of the cell, using microelectrodes (these electrodes have a tip diameter of less than one

14     H. Bleckmann thousandth of a millimeter). Depending on the type of sensory cell, the membrane potential is between −40 and −80 mV (1 V equals 1000 mV). If the sensory cell is stimulated with an adequate stimulus (e.g., light sensory cells with light, olfactory sensory cells with fragrances, auditory sensory cells with sound waves), the membrane potential of the cell changes. The electrical cell response can be quantified and correlated with various stimulus parameters (e.g., frequency, amplitude, or duration). Similar to how a socket sends electricity through a light bulb or LED connected to it by a cable (thus making the lamp light up), sensory organs send voltage impulses (nerve impulses) to the brain with the help of ultra-thin cables (afferent nerve fibers). Each nerve impulse consists of a voltage change lasting approximately one millisecond (one second has 1000 ms) and about 80 mV in size, which can be recorded with microelectrodes. With this method, one learns, for example, which stimuli a sensory cell responds to and how sensitive it is, whether and what influence the frequency or amplitude of the stimulus has on the response of the sensory cell, and thus also whether and how the parameters stimulus frequency, stimulus amplitude, and stimulus location are mapped (encoded) in the nervous system.

In addition to sensory organs with which animals perceive external stimuli, there are also sensory cells or organs for internal stimuli. These sensory organs measure, among other things, the carbon dioxide content in the blood, the temperature of the brain, the position and movement of the joints, and the length and strength of the muscles and tendons. These sensory organs, referred to as proprioceptors (as opposed to exteroceptors), are not covered in this book.

3.1 The Sense of Smell 3.1.1 Olfactory Organs All vertebrates have a sense of smell and taste. Fish use these two senses for food search and selection, the search and detection of sexual partners, the recognition of relatives, the avoidance of enemies, but also for intraspecific communication and spatial orientation. Among the odorous substances that fish can perceive particularly well are amino acids, bile salts, sex hormones, and tissue hormones. Amino acids are not only found in the mucus of living fish, but also in the tissue of dead fish. Unlike land vertebrates, fish do not have a nose. Instead, they have paired olfactory pits with strongly folded lamellae, which serve to increase the surface area (Fig. 3.1). In bony fish, the nasal pits are located on the top, in

3  The Sensory World of Fish     15

Front nose opening

Rear nose opening

Olfactory folds with olfactory epithelium Fig. 3.1  Nasal pit of the minnow with olfactory folds and olfactory epithelium. Top left: Enlarged olfactory sensory cell. (Adapted from Hildebrandt et al., 2021; with kind permission from Springer Verlag GmbH Germany. All Rights Reserved)

cartilaginous fish on the bottom of the snout. Water enters through the front opening of the nasal pits and exits through the back. The nasal pits of most fish are—unlike in land vertebrates and lungfish—not connected to the oral or pharyngeal cavity. A prerequisite for smelling is a continuous flow of water through the nasal openings. This is achieved by active pumping mechanisms (in slime fish), forward swimming (in pikes, minnows, and many sharks), by gill cover movements (e.g., in sticklebacks) or small, constantly moving “hairs” of the olfactory mucosa (in eels). The olfactory folds (lamellae), whose number and folding can vary greatly among different species of fish, are covered by a mucous membrane. The actual olfactory sensory cells are located in this mucous membrane, they constantly renew themselves. Their number can reach up to 500,000/mm2 in fish with a very good sense of smell (e.g., rays, sharks, and eels). The different olfactory abilities of fish become clear when measuring the size of their olfactory mucosa. The area of the olfactory mucosa in the European eel (Anguilla anguilla) reaches 1.4% and in the gudgeon (Gobio gobio) up to 3.5% of the body surface. Among the fish with less well-developed sense of smell are the flying fish (genus Beloniformes), anglerfish (deep-sea fish from eleven different families) as well as sticklebacks (Gasterosteus sp.) and pikes (Esox lucius). In pikes, which primarily orient themselves visually, the area of the olfactory mucosa only reaches 0.2% of the body surface.

16     H. Bleckmann

In order for fish to smell a substance dissolved in water, this substance (the scent molecules) must come into contact with olfactory sensory cells. To increase the probability of contact, in addition to a folding of the olfactory mucosa, there is a further increase in surface area. This is achieved by the olfactory sensory cells of the fish having small “hairs” (so-called cilia or microvilli) on the side facing the nasal cavity. As soon as a scent molecule comes into contact with a hair of an olfactory sensory cell, the electrical behavior of this cell changes. The comparison with a door lock is intended to show how this happens. Door locks are designed in such a way that they can ideally only be opened with the matching key. The cell wall of olfactory sensory cells contains numerous receptor proteins (analogous to the door lock) that only change their shape (conformation) when they come into contact with certain scent molecules (analogous to the key). The result is that ion channels in the cell membrane are opened and ions (electrically charged atoms, for example potassium, calcium or sodium ions) flow into the olfactory sensory cell. This changes the electrical potential (more precisely the membrane potential) of the olfactory sensory cell. As a result, the olfactory sensory cells send electrical impulses (nerve impulses) directly to the brain without switching to nerve fibers, the number of which increases or decreases with increasing scent concentration. Which and how many olfactory sensory cells generate nerve impulses depends on the type of scent molecules, since each olfactory sensory cell only forms one type of lock (only one type of receptor protein), i.e. its ion channels can only be “opened” by very specific scent molecules (keys) (physiological measurements have confirmed that each olfactory sensory cell only reacts to very specific classes of scents). The information from the olfactory sensory cells reaches the smell centers in the brain via the olfactory nerve. Since fish have many different types of olfactory sensory cells, each of which only reacts to very specific scent molecules, the smell centers in the brain can identify scents by comparing the electrical activity of different olfactory nerve fibers and thus distinguish them from other scents (scent molecules). The sense of smell in mammals, including humans, works in a very similar way.

3.1.2 Sensitivity of the Sense of Smell The sense of smell in fish is extraordinarily sensitive. Eels theoretically still perceive certain alcohols (e.g., β-phenylethanol) when 1 cm3 of this alcohol is dissolved in eighty-five times the volume of Lake Constance. Lake

3  The Sensory World of Fish     17

Constance contains approx. 50 billion cubic meters of water. At this dilution, only one to two molecules of the scent could have been in the eel’s nasal cavity. Sharks still smell blood in a dilution of 1 to 500 million. An extract from grouper is still perceived when the dilution is 1 to 10 million. Catfish (Plotosus japonicus) smell changes in the acidity (pH value) of the water. They are particularly sensitive in the range of natural seawater (pH value 8.1 to 8.2). In this range, Plotosus still reacts in behavioral experiments when the pH value changes by only 0.1. Plotosus uses this ability to track down worms buried in the sand. These exhale carbon dioxide, resulting in a decrease in the pH value of the water.

3.1.3 Chemical Messengers and Pheromones Many fish live in constant darkness (e.g., deep-sea fish) or in turbid, suspended matter-rich waters (many freshwater fish). Under these conditions, vision has only a minor importance, but chemical signals and pheromones are all the more important. A pheromone is a chemical messenger or a mixture of chemical messengers that a fish (an animal) involuntarily releases, thereby unconsciously altering the behavior of conspecifics, regardless of learning processes. Every dog owner knows this. A female dog in heat releases pheromones, which are perceived by males even in extremely low concentrations and trigger innate searching behavior. Males of the goby Bathygobius soporator vehemently defend their territory against foreign males, but not against females. These only trigger courtship behavior in the males. Courtship behavior can also be triggered without the presence of a female. In this case, a small amount of water in which a female was kept is sufficient. The reason for the males’ behavior are pheromones, which mating-ready females of Bathygobius soporator release into the water. The mating behavior of many fish is also temporally synchronized with the help of pheromones. Males of the dwarf gourami Colisa lalia only start building a foam nest and putting on their wedding dress after chemical contact with a female. Sticklebacks (Gasterosteus aculeatus) recognize their eggs and offspring by smell. This is a prerequisite for the parents not to eat their eggs or their own offspring. Salmon (e.g., Oncorhynchus kisuch ), char (Salvelinus sp.) and sticklebacks (Gasterosteus sp.) recognize close relatives by smell. By recognizing kinship, the risk of harmful inbreeding is reduced. Chemical signals also serve species recognition and the avoidance of predatory fish. Socially living fish often recognize dominant animals by their smell.

18     H. Bleckmann

3.1.4 Escape Reactions Karl von Frisch discovered as early as the beginning of the last century that injured minnows (Phoxinus phoxinus) trigger fear in conspecifics. He observed how a kingfisher’s just-caught minnow slipped from its beak and fell back into the water. All the minnows in the vicinity then fled. Karl von Frisch found out in subsequent experiments that injuries in minnows mechanically damage fright substance cells in the deeper layers of the skin, which then release their fright substance. According to current knowledge, only fish belonging to the Ostariophysans (true bony fish with a bony connection between the swim bladder and the inner ear) release alarm substances. Within the Ostariophysans, this has so far been proven for 78 species. All fish in the vicinity of an injured conspecific smell the fright substance, but the innate behavioral reaction triggered by it can be quite different. Some fish hide in a nearby shelter, others swim away in panic or huddle together in fear. Others still stop all movement when they come into contact with fright substances. Often, fish avoid the place where a fright substance was released for several days. In a typical experiment, 0.002 mg of crushed fish skin was enough to trigger a fright reaction in minnows kept in a 14-L aquarium. It is likely that fish alarmed by fright substances have a selection advantage as they are warned of predators. The question remains, however, what evolutionary advantage the fish that releases the fright substance has. Possibly, fish in a swarm are related to each other, in this case kin selection (see further below) would explain the seemingly selfless behavior of the fish. During the mating season, the testosterone level in the blood of many fish increases. At the same time, the alarm cells of the skin stop producing fright substance. This represents an adaptation to reproduction, because during egg laying many freshwater fish rub against the gravelly substrate on which they spawn. This leads to skin injuries, which under normal conditions would lead to the release of fright substances and thus to the interruption of egg laying. If it is the fright substance of another species, escape behavior must first be acquired through experience. Fish also learn to associate a certain smell with enemies. Experienced minnows (Phoxinus phoxinus) flee or let themselves sink motionless to the ground as soon as they perceive the smell of a pike. If the pike has caught a minnow, the fright substance of the eaten fish passes through the pike’s digestive system (or that of another predatory fish) mostly undamaged. The predator is thus marked by smell, its location is henceforth avoided by potential prey fish.

3  The Sensory World of Fish     19

3.1.5 Spatial Orientation The family of salmonids, also known as trout or salmon, includes salmon, trout, whitefish, and grayling. Some species (anadromous species, e.g., the Atlantic salmon Salmo salar ) migrate to the open sea from freshwater at a certain time of the year, only to return to their home waters to spawn after several years. Other species spend their entire lives in flowing waters, where they often undertake long migrations. Yet other species (potamodromous species, e.g., rainbow trout) seek freshwater lakes after their juvenile development, into which their home waters flow. These species also return to their home river or stream to spawn. In addition to the species mentioned, there are salmon species that spend their entire lives in the open sea. There, some species also undertake long migrations. For a long time, it was a mystery how salmon orient themselves during their migrations. As early as the penultimate century, researchers suspected that these fish find their home waters using their sense of smell. This assumption has been confirmed by ablation experiments (blocking the nasal pits or severing the olfactory nerves) and has led to the assumption that salmon are imprinted on the smell of their home river before descending to the sea or a freshwater lake. Other experiments suggest that descending conspecifics release substances (pheromones?) that guide the ascending fish. Both could ensure that anadromous fish find the river or stream section where they hatched and grew up, even after several years. In another experiment, researchers showed that salmon follow the arm of water at an artificial fork that contains water from their home stream. Intact Atlantic salmon find the mouth of their home waters even when they are released 100 km away from the mouth in the sea. If their sense of smell is blocked, they are no longer able to do this. The larvae of coral fish return to their home reef after a several-month period as plankton organisms in the open sea. Coral reefs emit a smell typical for each reef, which is apparently recognized by the larvae. In a two-choice experiment, they preferred the water of their home reef over the water of neighboring reefs. It is assumed that the larvae recognize their home reef with their sense of smell and seek it out specifically. Acoustic and magnetic field information also play an important role in this orientation performance.

3.1.6 Smell and Water Pollution The pollution of rivers, streams, lakes, and coastal seas by nitrates and phosphates from agriculture is a widespread problem. This is compounded by

20     H. Bleckmann

insecticides, herbicides, and fungicides, as well as hydrocarbons and detergents from private households and industry. Other extremely harmful environmental toxins are heavy metals such as copper, cadmium, zinc, and lead, which are highly toxic to fish even in extremely low concentrations. Even if fish seemingly survive unaffected in a polluted section of water, their olfactory sensory cells are severely damaged by a variety of pollutants that accumulate in the olfactory epithelium. This can involve degeneration of the olfactory sensory cells or influence the molecular processes in the olfactory sensory cells. A decrease in the sense of smell and the subtle impairments in fish behavior caused by this can be observed even at extremely low pollutant concentrations. Physiological experiments have shown that even the slightest concentrations of copper and cadmium suppress the electrical responses of olfactory sensory cells within a few minutes.

3.2 The Sense of Taste 3.2.1 Taste Organs In terrestrial vertebrates, a clear distinction can be made between the sense of smell and the sense of taste. With the sense of smell, terrestrial vertebrates perceive molecules that reach them through the air. In contrast, the sense of taste only perceives molecules (or food particles) that are in the aqueous fluid of the oral cavity. Since fish live in water, a functional separation between the sense of smell and taste is difficult. Nevertheless, probably all fish have an independent, high-performance sense of taste. This primarily serves the function of food selection and food control. The taste sensory cells of fish, like those of all other vertebrates, are located in taste buds (Fig. 3.2). Fish have three different types of taste buds. It is assumed that some fish taste buds also respond to mechanical stimuli. In humans, the taste of food depends on the consistency of the food, which is determined with mechanoreceptors in the oral cavity. The taste buds of fish can contain up to 150 taste sensory cells. These are constantly renewed, similar to olfactory sensory cells. To increase the surface area, taste cells form either a single rod (microvillus) or several rods (microvilli). In fish, taste buds are found not only in the oral cavity, but also on the gills, the barbels, the fins, and the entire body surface (catfish, for example, have up to 175,000 on each body side). Taste buds inform a fish about taste substances, i.e., potential food. In addition to the taste buds, many fish also have individual taste sensory cells in the skin, their density can reach up to 4000/

3  The Sensory World of Fish     21 Microvillus

Microvilli

Sensory cells

Afferent nerve fibers Fig. 3.2  Taste bud of a true bony fish. To increase the surface area of the taste sensory cells, either a single rod (microvillus) or numerous thin rods (microvilli) are used

mm2 (e.g., on the head of roaches, Rutilis rutilis ). On the anterior dorsal fin of the Mediterranean rockling Gaidropsarus mediterraneus, there are up to six million taste sensory cells, in addition to numerous taste buds located on the first fin ray. Other species, e.g., sticklebacks (Spinachia spinachia), eels (Anguilla anguilla) and blennies (Blennius pholis) appear to have no individual taste sensory cells in the skin. Taste sensory cells function similarly to olfactory sensory cells, but unlike these, they have no direct connection to the brain, but are innervated by taste nerve fibers. When certain chemical substances (e.g., amino acids) or food particles come into contact with the surface of a taste sensory cell, the electrical properties of this cell change, similar to olfactory sensory cells. The taste sensory cell then releases a chemical messenger (neurotransmitter) that binds to specific receptors of taste nerve fibers. The nerve fibers then generate nerve impulses that are transmitted to the brain. In addition to taste sensory cells, fish have free nerve endings in the skin that also react to chemical substances (e.g., table salt, amino acids).

3.2.2 Sensitivity of the Sense of Taste The sense of taste is highly developed in many fish. Unlike in terrestrial vertebrates, however, it does not serve to perceive sugars and salts. For example, the sensitivity of minnows (Phoxinus phoxinus) to table salt is 180 times lower and to cane sugar 500 times lower than in humans. Fish also show a

22     H. Bleckmann

strong insensitivity to substances that taste bitter. In contrast, the taste sensory cells of fish react very sensitively to amino acids. These are released into the water by both living and dead fish. Many fish (e.g., goldfish, Carassius auratus, or the rabbitfish Siganus sp. found in the tropical Indo-Pacific) repeatedly take up substrate with their mouths, only to spit it out again. Upon closer examination, it was found that during this process, the fish separate food particles from grains of sand and other substrate with a sophisticated organ, the palatal organ (Fig. 3.3). After sucking in water, most of the food particles present in the mouth are recognized and distinguished from inedible particles by taste sensory cells. Through numerous locally forming, opposing protrusions, each of which is equipped with taste buds at the end, most of the food particles present in the mouth are identified and trapped. Subsequently, the water remaining in the mouth, along with the sand and other inedible particles, is spit out again. Then the trapping mechanism is released, so that all food particles can be swallowed, a process that is constantly repeated during foraging. Given the complexity of this behavior, it is not surprising that goldfish require about 20% of their brain just to control this food sorting machine.

3.3 The Visual System 3.3.1 The Vertebrate Eye Of all the sensory organs, eyes have always attracted human attention due to their striking appearance and their great importance for the behavior of many animals. Even Darwin wondered how such a highly complex organ as the human eye could have evolved through natural selection. That this is indeed the case is evidenced by numerous comparative and molecular biological studies. Light-sensitive molecules are found in many unicellular organisms. Over the course of evolution, many organisms have then developed light-sensitive sensory pads as well as simple pit and cup eyes, and finally highly complex lens eyes. Unfortunately, even in the 21st century, there are still people (e.g., creationists) who do not believe in evolution or scientific findings. As a rule, these people have not taken the trouble to deal more closely with the phenomenon of biological evolution. Just like most terrestrial vertebrates, most fish can also see excellently. Physical laws and biological constraints determine both on land and in water how eyes must be constructed so that an animal can optimally see moving and stationary objects under the prevailing light conditions in its

3  The Sensory World of Fish     23

Palatal organ

posterior

Food

Flow direction a

Sand

Gill arches

1

Palatal organ Stones

2

3 Wash out b Fig. 3.3  a An organ located in the mouth cavity of goldfish (Carassius auratus) (palatal organ) separates food particles from the substrate in conjunction with the gill arches. b After intake of substrate, almost all food particles (red) present in the substrate are recognized by taste  buds (red lines and red semicircles). 1 Sand, pebbles (blue) and food particles are actively taken up. 2 The food particles are recognized and trapped by the palatal organ. 3 Sand and pebbles are then spit  back out. After that, the trapping mechanism is released and the food particles are swallowed. Posterior: located further back. (Adapted from Hildebrandt et al., 2021; with kind permission from Springer Verlag GmbH Germany, All Rights Reserved)

natural habitat. Physics limits the degrees of freedom available to nature in the development of eyes, but it also shows which selection pressures must have been effective in the evolution of eyes. The structural composition of the vertebrate eye is shown in Fig. 3.4. From the outside in, vertebrate eyes consist of a transparent cornea, an iris, lens, a vitreous body, a retina, and a pigment layer. Unlike in terrestrial vertebrates, in fish, the cornea of the eyes does not have a light-refracting function, as the refractive index of water hardly differs from that of the

24     H. Bleckmann

transparent cornea. In order for a sharp image to still be formed on the retina, the eye lens of fish, unlike that of terrestrial vertebrates, must provide all the refractive power. This is achieved by a spherical shape (the lenses of most terrestrial vertebrates are flattened, see Fig. 3.4). The iris surrounds the eye hole (the pupil), which in fish can be circular (as in many mammals and birds) but also transversely elliptical, transversely oval, or oval. Guanine crystals can be embedded directly behind the retina. They cause the light rays falling into the eye to be reflected from the back of the eye—similar as in house cats. This increases the light sensitivity of the eyes, as each light ray passes through the retina a second time. The price for the increase in light sensitivity is a decrease in visual acuity. The actual light-sensing cells, i.e., the cells that react to light exposure with a change in their electrical potential, are located in the retina. Two types of light-sensitive cells can be distinguished in color-sensitive vertebrates: the light-sensitive rods responsible for night vision and the cones responsible for day vision, but which are significantly less light-sensitive. The low light sensitivity of the cones is understandable, as there is always enough light during the day. The pupil of most bony fish has a constant diameter, so it does not change—unlike in mammals—or changes only slightly with changing light conditions. To still achieve adaptation to different light conditions, in fish the light-sensitive cells in the retina migrate towards or away from the light. In contrast to bony fish, cartilaginous fish can adjust their pupil size to the respective light conditions. In darkness, their pupils dilate, in brightness, they contract

Chorioidea Sclera Iris

Lens

Retina

Ciliary muscle

Optic nerve

Pupil

a

b

Rod

Cone

Fig. 3.4  a Vertebrate eye with lens, pupil, iris, choroid, sclera, retina, and optic nerve in cross-section, b Rods and cones.  (Modified, from Fritsche, Biology for Beginners; with kind permission from Springer Verlag GmbH Germany, All Rights Reserved)

3  The Sensory World of Fish     25

again. Eels, sand-dwelling flatfish, stargazers (Uranoscopus) and gut fish (Carapus) can also adjust the pupil size to different light conditions. Eyes have the task of capturing light and sharply imaging objects on the retina regardless of distance. The adequate stimulus for light sensory organs are electromagnetic rays in a certain wavelength range (light). Before humans invented artificial light sources (e.g., light bulbs or LEDs), the sun, moon, and stars, along with fire, were the only abiotic light sources. In humans, the visible wavelength range of electromagnetic radiation extends from 390 nm (blue) to 760 nm (red) (1 nm = 1 millionth of a millimeter), in many fish species this range extends into short-wave ultraviolet or longwave infrared. Light that contains all wavelengths in the range from 390 nm to 760 nm is perceived by us as white light. If white light falls on an object, it appears black if the light is completely absorbed by the object. If the light is completely reflected by an object, it appears white to us. If different wavelengths are reflected (or absorbed) to different extents, an object appears colored. If an object predominantly reflects short-wave light, it appears blue, if it predominantly reflects long-wave light, it appears red. The image of an object on the retina is formed without time delay. A time delay of several milliseconds only occurs due to the image processing in the retina. These processes are faster the greater the demands on the temporal resolution of a visual system. Temporal resolution, or flicker fusion frequency, describes the number of light flashes (images) that can still be separately perceived by a visual system in one second. The temporal resolution of the human eye under normal light conditions is 25 to at most 70 Hz. Below a refresh rate of about 25 Hz, the image of a television or computer monitor begins to flicker. At very low image refresh rates, successive individual images are finally recognized. A high temporal resolution of the visual system allows to recognize even very fast events. In fast-swimming predatory fish such as swordfish, tuna, and some shark species, the temporal resolution of the visual system is therefore up to ten times greater than in slow-swimming fish such as goldfish or carp. This is possible, among other things, because the aforementioned predatory fish (e.g., the tuna Xiphias gladius ) can raise the temperature of their eyes and brains by up to 15°C above the temperature of the surrounding water when hunting. The visual system of fish faces many challenges. Near the shore and in shallow water, the light conditions are similar to those on land. All colors are present, so underwater plants, corals, sponges, the sandy bottom, or stones and rocks make it easier for fish to orient themselves spatially and recognize objects. In the open sea, the conditions are completely different. There are no landmarks, and with increasing water depth, it eventually becomes

26     H. Bleckmann

so dark that only fish with highly light-sensitive eyes can see anything. The light conditions in the upper water layers are completely different on a cloudless summer day than on a cloudy night. Nevertheless, the eyes must transmit all the information necessary for survival to the brain, regardless of the respective environmental brightness. To adapt to different light conditions, the eyes of diurnal fish are built differently than those of nocturnal fish or fish living in the light-poor deep sea. Large eyes are often found in diurnal predatory fish, but also often in crepuscular fish or deep-sea fish. Small eyes are typical for bottom dwellers, they orient themselves in murky water mainly with their sense of smell (e.g., catfish and loaches) or with their electric sense (e.g., weakly electric fish). Deep-sea fish or cave-dwelling fish often have rudimentory eyes, in extreme cases the eyes are completely absent.

3.3.2 Light in the Aquatic Habitat Regardless of the time of day, completely different optical conditions prevail in water than on land. When light hits the water surface, depending on the angle of incidence, only part of the light rays penetrate the water, the rest is reflected by the water surface. This reflection increases with decreasing sun position (smaller angle of incidence) or increasing wave movement of the water surface. As a result it is slightly darker even at shallow water depths during the day than on land. Water also acts like an optical filter. The longwave component of light (the red component) is absorbed more strongly (already 100% in the top two meters) than the short-wave component (the ultraviolet and blue component). As divers know from experience, this is why you can only see the many colors of its inhabitants in a coral reef on the top two to three meters, after that the yellow and then the green tones disappear after the red. In bright sunlight, the surface of the seas appears deep blue because the red and yellow rays are completely absorbed and the short-wave blue rays predominate among the rays reflected upwards. Even in clear weather, 80% of the incoming light is absorbed in the top ten meters, and even under optimal conditions, light or the blue component of light hardly reaches a depth of 1000 m. Without light, eyes are useless, which is why some deep-sea fish, but also most cave fish, have regressed their eyes. The deep-sea ray Benthobatis still has eyes, but these have neither a retina nor an iris or lens. The fact that many deep-sea fish still have eyes is due to the fact that many inhabitants of the deep sea communicate with luminous organs. At the same time, however, they unintentionally attract predatory

3  The Sensory World of Fish     27

fish with their luminous organs. Regressed, non-functional eyes are found in the approximately 150 species of blind cave fish, e.g., in the tetra Astyanax mexicanas, available in the aquarium trade, which lives in caves in the Sierra del Abra in northeastern Mexico. Many freshwater fish are found in turbid, suspended matter-rich waters. In these waters, the light conditions are so poor that eyes are only useful for close range orientation. The conversion of light into an electrical response takes place in the light sensory cells of the retina, the rods and cones. These cells contain light-sensitive molecules (retinal), which even can be found in some bacteria (e.g., the archaebacterium Halobacterium salinarum ). Retinal is an organic molecule that changes its shape (conformation) when exposed to light. Retinal, in combination with a protein, forms the actual visual pigment, rhodopsin. A change in the shape of retinal leads to the closing of ion channels in the membrane of light sensory cells. As a result, the membrane potential of these cells changes. The information associated with this is first transferred to bipolar cells and then to the optic nerve fibers. The retina of color-blind fish contains only rods, while the retina of color- sensitive fish, like the retina of many mammals including humans, contains both rods and cones (Fig. 3.4 below). The human retina contains three types of cones. Some fish have up to four types of cones, each containing different visual pigments. This results in the different types of cones having different wavelength sensitivities. Depending on the visual pigment, the sensitivity peak of a cone is in the blue, green, or red range. Many fish also have cones with a sensitivity peak in the ultraviolet range (e.g., the goldfish Crassius auratus and the minnow Phoxinus phoxinus ) or in the infrared range (e.g., the tilapia Oreochromis mossambicus ). Only the comparison of the electrical activity of the different types of cones leads to color perception. For example, if only blue-sensitive cones are stimulated, an object appears blue; if only red-sensitive cones are stimulated, it appears red. Similar to a color television, almost any color can be constructed by the brain by mixing the colors red, green, and blue (by comparing the activity of red-sensitive, green-sensitive, and blue-sensitive cones) (physically there are no colors, only electromagnetic radiation of different wavelengths. Color sensation is only created in the brain). That many fish can distinguish colors as well as a human has been demonstrated in a variety of species (e.g., Phoxinus laevis, Rhodeus amarus, Idus melanotus, Tinca vulgaris ). Humans recognize colors (or the corresponding wavelengths) and gray values largely independent of the spectral composition and brightness of the ambient light. Thus, a yellow shirt still appears yellow to us in the red twilight of a disco, even though no yellow light is reflected from the yellow shirt under these conditions. A white shirt reflects much less light in the dark

28     H. Bleckmann

than a gray shirt in the light, yet the white shirt still appears white to us in the dark and not gray. Our brain therefore judges the light reflected from a shirt (object) in relation to the ambient brightness and the spectral composition of the ambient light. This ability is referred to as color or brightness constancy. Behavioral experiments have shown that the visual system of fish also exhibits color and brightness constancy. This is important, as brightness and spectral composition of light change with increasing water depth. In addition to color and brightness, fish also discriminate the contour, shape, motion, and spatial depth of objects. With old cameras, you had to manually focus the image in the viewfinder before each shot (modern cameras have an autofocus that automatically takes over the focusing). When focusing, the distance between the lens (or the lens system in the case of multiple lenses) and the film is continuously changed. At the “Infinity” setting, the image plane and film plane coincide at large object distances, making the image appear sharp. As an object (e.g., an animal) approaches, the image goes behind the film plane, becoming blurry. This can be corrected by increasing the distance between the lens and the film, so that close objects are now sharply depicted again. In the mammalian eye, focusing is achieved by changing the shape of the lens: as a mammal approaches an object, the initially flattened lens takes on the shape of a sphere. This increases the refractive index of the lens. The eyes of fish work differently. Like a camera, fish eyes vary the distance between the lens and the retina depending on object distance, a process that—like the change in lens shape—is referred to as accommodation. In general, in animals, the eyes at rest are adjusted to the distance that is most important in the natural habitat of the respective species. In coral reef fish, the eyes are adjusted for near vision, as they search for their food in the sand or mud or graze the algae and polyps from coral stocks. If coral reef fish want to see a distant object clearly, they move their lens towards the retina. In most sharks, the eyes at rest are adjusted for distant vision. To recognize close objects, sharks move their lens away from the retina. The brightness is usually several orders of magnitude (by a factor of 1,000 to 1,000,000) lower at night than during the day. Nevertheless, fish— like many terrestrial vertebrates—can see well both during the day and at night. The eyes of these fish obviously adapt to the different light conditions. This process is referred to as light or dark adaptation. The amount of light that reaches the retina is regulated in most terrestrial vertebrates by the pupillary reflex. During the day, the pupil is narrow, allowing only a small amount of light to reach the retina. As light intensity decreases towards evening, the pupil widens, thereby increasing the light supply to

3  The Sensory World of Fish     29

the retina (in this process, as with a camera, the depth of field automatically decreases). Rods are extremely light-sensitive and are used exclusively for twilight and night vision. Since there is only one type of rod, rods do not enable color vision, but only vision in grayscale (at night, all cats are gray). Cones are less light-sensitive. They are used for daytime vision. When it gets dark, color-sensitive fish eyes—just like our eyes—switch from cone vision to rod vision. In the fish eye, there are two additional mechanisms of light-dark adaptation. With strong brightness, the light-sensing cells are increasingly shielded from the incoming light by pigment migration in the retina. Conversely, there are fish that retract their light-sensing cells into the pigment layer of the eye in strong brightness. Some coral reef fish living directly under the water surface have a “sun visor” at the upper edge of their eyes. This protects the retina from too intense sunlight. There are additional molecular mechanisms of light and dark adaptation in the vertebrate eye, but these will not be discussed here. The light that reaches a fish at greater water depths consists, as already mentioned above, only of the short-wave blue component. Many fish absorb blue light with fluorescent scales, which then reflect it in a different color. If you photograph these fish through a yellow filter, they glow under UV radiation in the colors green, yellow or red. The reason for this is that the yellow filter filters out the blue light and only then the other colors become visible. Over 180 fluorescent fish species have been detected so far, including both sharks and rays as well as true bony fish. It was unclear what advantage these fish have from their fluorescent surface. In anatomical and physiological  studies, it was finally found out that the cornea in the eye of many of these fish species acts like a yellow filter. Therefore, fluorescent fish can recognize conspecifics even in weak blue light and communicate with them. For predators that lack a yellow filter in the eye, these fish remain almost invisible. Light rays change their direction at the interface of two media of different optical density, they are refracted (this becomes visible, for example, when you hold a straw obliquely into the water. The straw appears to have a kink at the immersion point). The angle of refraction of a light ray also depends on its wavelength (color). Obliquely incident short-wave blue light is refracted more strongly at the interface between an optically thinner and an optically denser medium than long-wave red light. White light that falls through a glass prism is therefore broken down into its spectral colors, a phenomenon we know from the rainbow (in a rainbow, the sunlight is broken down into its colored components by raindrops). The wavelength-dependent refractive index of light inevitably leads to imaging errors in optical

30     H. Bleckmann

lenses, this is referred to as chromatic aberration. To keep chromatic aberration low, good cameras have not only one, but several lenses. Fish eyes have found another solution: They have lenses whose material has different refractive properties from the inside to the outside. This ensures that, regardless of the wavelength of the incident light, a sharp image is always created on the retina.

3.3.3 Further Adaptations of the Fish Eye With their eye muscles, some bony fish can move their eyes synchronously or even independently of each other. The latter is often found in fish that fixate their prey before snapping (e.g., seahorses, many wrasses, and flatfish). The eyes of the mudskipper (Periophthalmus), the rockskipper (Blenniella) and the sandfish (Limnichthytes fasciatus)  ), are extraordinarily mobile, the eyes of these fishes are frog-like on top of the head (Fig. 3.5). Sandfish live in the shallow waters of Indo-Pacific coral reefs. They burrow into the ground so that only the upward-facing eyes protrude from the sand. Sandfish, like chameleons, can move their two eyes independently in any direction. Sandfish feed on zooplankton. When a sandfish spots a plankton organism, it darts forward, opens its mouth quickly, and thus sucks in the prey. This hunting technique requires a precise estimation of prey distance. The necessary accuracy of distance estimation is achieved through a telescopic two-lens system (Fig. 3.5). Unlike other fish, the lenses of the sandfish eye are not spherical, but oval. The cornea is thickened and thus takes on the function of an additional lens. Together with the main lens of the eye, an enlarged image is created on the central part of the retina, similar to the beam path in binoculars. The rest of the retina serves the function of a wide-angle lens, thus covering the entire field of vision. Sandfish can even determine the distance to a prey object with just one eye. With a special muscle, they adjust the degree of curvature of the cornea until the image on the retina is sharp. Thus, the degree of curvature of the cornea provides an indirect measure of prey distance. Many fish live in ocean depths where sunlight barely penetrates. The world of these fish is not only dark, but also visually unstructured or only weakly structured. Eighty percent of all animals living in the deep sea have light organs. Many deep-sea fish can not only see the light emitted by these organs, but can also precisely determine the location of the point-like light source. For example, the predatory hatchetfish Argyropelecus sp. living at depths of up to 800 m can still distinguish two points of light six meters

3  The Sensory World of Fish     31 Cornea Corneal lens

Lens

Retina

a

b

Fig. 3.5  The eyes of the sandfish Limnichthytes fasciatus can independently rotate in almost all directions. This fish lives in well-lit shallow water and lurks with its stalk eyes protruding from the sand (a) for prey. b The eyes of the sandfish have a corneal lens in addition to the normal lens. When the fish spots a prey animal, it shoots out of the sand, opens its mouth from about 20 cm away, and sucks the prey into its mouth due to the resulting negative pressure. (Modified, after Heldmaier et al., 2003; with kind permission from Springer Verlag GmbH Germany, All Rights Reserved)

away even  if they are only 1 centimeter apart. For this localization accuracy, deep-sea fish have developed oversized tubular eyes (telescope or tube eyes) (Fig. 3.6a, b). They can rotate these eyes perpendicular to the longitudinal axis by 90° and therefore can look both forward and upward. An overlap of the visual fields also allows the fish to estimate distances, even though important distance features such as relative size or partial occlusion of objects are not present in the deep sea. On the side of the main eye, some deep-sea fish have pouches lined with a retina and a transparent cornea facing downwards (i.e., opposite to the main axis of the pupil of the main eye). This extends the field of view downwards (Fig. 3.6c). In some species of fish, there is another complication. In these fish (e.g., Dolichopteryx ), the light first hits a layer of guanine crystals that act like a mirror. The guanine crystals are arranged such that they deflect the light rays and focus them on the retina of the secondary eye. The retina of the tubular eyes of many deep-sea fish is adapted to the sparse light conditions of the deep sea. Rods are long and therefore contain many visual pigment molecules. This increases their light sensitivity. The visual pigment of deep-sea fish has its absorption maximum in the blue

32     H. Bleckmann

a Cornea extended Cornea

Lens

Lens Accessory retina

Accessory retina Secondary eye

b

Main retina

Direction of movement

c

Secondary lens Below

Fig. 3.6  a Opistoproctus soleatus with tubular eyes. This fish lives in tropical waters at a depth of 500 to 700 m. b Diagram of the tubular eye of a deep-sea fish. In addition to the main retina, which is used for forward vision, the eye has a lateral cornea and a secondary retina. This allows the fish to see objects that are located to the side of it. c Main eye with secondary eye of the deep-sea fish Bathylchops exilis. With the main eye, the fish captures objects in the forward direction, with the secondary eye it simultanously can look down. (Modified, after Heldmaier et al., 2003; with kind permission from Springer Verlag GmbH Germany, All Rights Reserved)

range (at 470 to 480 nm), an adaptation to the high blue component of the light in deeper water layers. In some fish species, the retina contains up to seven layers of rods to increase light sensitivity (Fig. 3.7). To further increase light sensitivity, the eyes of many deep-sea fish have a tapetum lucidum, which reflects every light beam falling on the retina. This makes the eye more sensitive, but this increase in sensitivity comes at the expense of visual acuity. Surface-feeding fish are specialized in hunting insects that have fallen into the water. These fish include species of the genus Aplocheilus and the butterfly fish Pantodon buchholzi, as well as the four-eyed fish Anableps tetrophthalmus. Anableps lives off the coasts of southern Mexico, Central America, and South America and prefers to stay at or just below the water surface. The eyes of Anableps are divided in two, but have only one pupil, which is divided into an area for seeing above water and one for seeing below the water (Fig. 3.8). Consequently, each eye of Anableps contains two retinae. Objects above the water surface are imaged on the retina of the lower half of the eye, objects below the water surface on the retina of the upper half of the eye. That part of

3  The Sensory World of Fish     33

Lens

a

Pigment epithelium

Rod outer segment

Cell body with nucleus Rods

b

Light

Fig. 3.7  a Eye of the deep-sea fish Diretmus argenteus. To increase the light sensitivity of the eye, the retina consists of up to seven layers of rods in some places. The arrow corresponds to forward direction. b Diagram of a three-layered retina. The outer segments of the rods are in some cases only connected to the cell body of the rods by thin stalks. (Modified, after Heldmaier et al., 2003; with kind permission from Springer Verlag GmbH Germany, All Rights Reserved)

the cornea of the Anableps eye that is exposed to air is hardly curved, thus producing little refractive power. The oval lens of the eye presents its flat side to the light above the water surface and its strong curvature to the light below the water surface. This allows for sharp vision both above and below the water surface. The information from the two retinae is processed in separate brain regions.

34     H. Bleckmann Upper pupil

Retina I

Cornea

Air

Iris

Water

Lens Optic nerve

Lower pupil Iris

Retina II

Fig. 3.8  Four-eyed fish Anableps tetrophthalmus. The eye is divided in two and contains an area for seeing above and one for seeing below water. (Modified, after Hildebrandt et al., 2021; with kind permission of Springer Verlag GmbH Germany, All Rights Reserved)

Some fish species even live temporarily outside of water. These species include the mudskippers of the genus Periophthalmus that live in mangroves and the rockskippers of the genus Blenniella found on rocky coasts. In these fish, the cornea of the eye is flattened and no longer produces refractive power, it only serves to protect the eyes. Some flying fish (Exocoetidae) catapult themselves out of the water when fleeing and sail long distances just above the water surface. The retina of these “flying” fish is shaped like a three-sided pyramid. The front side is directed upwards and forwards, the back side downwards and backwards. This eye design allows flying fish to see both underwater and to monitor the airspace above the water from all sides during the flight phase. In many deep-sea fish, numerous light-sensing cells are each located in a cup-shaped structure. Each cup is surrounded by a pigment epithelium that has reflective properties due to embedded guanine crystals. Retinas with light-sensing cells grouped in cups were first described in 1906. Two decades later, grouped light-sensing cells lying in cups were also found in the retina of the freshwater Mormyrid Gnathonemus petersii. Current research results show that grouped retinas occur in at least forty fish species in seventeen of seventy partly unrelated families of true bony fish. This is an indication that grouped retinas have evolved several times independently of each other. The grouped retinas of deep-sea fish contain only blue-sensitive rods because of the short-wave light prevailing in the deep sea. In contrast, the rods and cones in freshwater Mormyrids are predominantly red-sensitive, as in the streams and rivers where Gnathonemius occurs, the blue component of the light is absorbed by suspended particles and therefore long-wave light

3  The Sensory World of Fish     35

predominates. Grouped retinas have so far not been described in cartilaginous fish or other vertebrate groups. The retina of the eyes of the weakly electric elephantnose fish Gnathonemus petersii is very well studied (Fig. 3.9). It contains highly sensitive rods that lie outside or below cups. In addition, the retina of Gnathonemus contains light-sensitive cones at the bottom of each cup. To ensure that these are still excited even in weak light, the cup walls made of guanine crystals reflect the light rays so that they reach all cones at the bottom of the cup. Elephantnose fish live in West and Central Africa in streams and rivers that contain many organic suspended particles. The reflective layer of the pigment epithelium of each cup ensures that the brightness at the bottom of a cup is about five times greater than the brightness directly above a cup. This brightness is sufficient to excite the comparatively light-insensitive cones at the bottom of the cup even under unfavorable light conditions. At the same time, the cup edge made of guanine crystals shields the light from the highly light-sensitive rods lying below the cup, so they only receive about 20% of the brightness above the cup. This ensures that the light-sensitive rods do not receive too much light, so they remain fully functional Light

to the brain Bipolar cell

Cones Rods

Reflective layer

Fig. 3.9  Section of the retina of the elephantnose fish Gnathonemus petersii. The honeycomb-shaped retina consists of numerous hexagonal cups, whose walls reflect light through embedded guanine crystals. At the bottom of the cups are cones, and below the cups are numerous rods. All light sensory cells of a cup project onto the same bipolar cell (only one bipolar cell is drawn), which passes its information to the brain of Gnathonemus

36     H. Bleckmann

even during the day. Together with the cones, this results in a total system with high light sensitivity. Originally, scientists had suspected that grouped retinas only had the function of increasing the light sensitivity of the eyes. Current studies have shown, however, that the eye of Gnathonemus has another function. To understand this, one must know that all rods and cones belonging to a cup send their information to the same nerve cell (bipolar cell) (Fig. 3.9). This causes each bipolar cell to be excited by extremely small amounts of light. Since all light sensory cells of a cup converge on a common bipolar cell, the visual acuity of the elephantnose fish is low (fifteen times lower than that of a goldfish). Therefore, elephantnose fish cannot see small suspended particles in the water. At the same time, the high light sensitivity of the eye ensures that large predatory fish (e.g., hunting catfish) are detected early by Gnathonemus even under poor light conditions. Electromagnetic waves radiated by the sun are unpolarized, i.e., the electric field vectors (E-vectors) of light waves are perpendicular to the direction of light propagation and constantly change their direction. On average all directions are equally likely. Polarization filters only allow E-vectors of a certain direction to pass (Fig. 3.10). They are used in photography to suppress unwanted reflections and thus increase image contrast. Many fish (e.g., cichlids, salmonids, cyprinids, and pomacentrids) have functional polarization filters in their eyes. As in photography, these serve to increase contrast. Polarization vision allows fish to recognize at close range even the smallest zooplankton organisms against a homogeneous background. As soon as the background and the object have an E-vector difference of more than 10°, this recognition mechanism works. Many fish also use polarization vision for intraspecific communication. For instance, the skin of many reef bass contains pigment cells Polarization filter E-vectors Sonne Unpolarized light

Polarized light

Fig. 3.10  Effect of a polarization filter. Light radiated by the sun is unpolarized, i.e., the E-vectors point in all directions. When light passes through a polarization filter, the E-vectors only point in one direction after passing through the filter, the light is polarized

3  The Sensory World of Fish     37

(chromatophores) that polarize light upon reflection. This results in species-specific patterns that change dramatically depending on the viewer’s perspective and ensures that even the smallest movements of a conspecific are immediately recognized by the reef bass. Fish also use their polarization vision for spatial orientation. Among other things, polarization vision allows them to orient themselves according to the position of the sun. What is the mechanism of polarized vision? No upstream polarization filter has been found in the eyes of fish. However, in addition to the normal light sensitive cells, the retina contains light sensitive cells that are polarization sensitive. The sensitivity maximum of these cells lies in the UV range (approx. 500 nm wavelength). Therefore, the electrical cell responses do not depend on the wavelength of light, but only on E-vector orientation. The mechanism that leads to polarization sensitivity is not yet known, but it has something to do with the shape and spatial arrangement of the visual cells in the eye.

3.4 The Sense of Touch 3.4.1 Touch Receptors Using the Example of Humans Presumably all animals have touch  receptors. These register every touch, but also pressure and vibration. The sense of touch is a contact sense and thus differs from all other senses. In human skin, there are six types of touch receptors (Pacinian corpuscles, Ruffini corpuscles, Meissner corpuscles, Merkel cells, hair follicle receptors, and free nerve endings), which differ in their shape (structure), size, location in the skin, and thus in their function. Depending on the type of sensory organ, the sensitivity, size of the skin area that must be deformed for effective stimulation, and the duration that a sensory organ responds to a prolonged skin deformation, vary. With the touch receptors of our fingertips, we can not only estimate the roughness of a surface, but also the shape and size of objects, a performance that only our visual system is capable of. With temperature sensors in the skin and mechanosensors that measure the position of joints and the degree of muscle contraction, we also receive information about the temperature and weight of an object, i.e., its material properties. Touch can be pleasant (when we are stroked) or unpleasant (when someone scratches us) and thus strongly influence our feeling. But our skin can do even more. For example, after a few minutes we no longer sense prolonged mechanical stimuli, caused e.g. by wearing clothes. The reason for this is that skin receptors become insensitive

38     H. Bleckmann

(adapt) to persistent uniform stimulation. Despite a decrease in sensitivity caused by adaptation, we immediately feel when a fly, louse, or spider is crawling up our arm under our sleeve. This shows that the skin distinguishes between different forms of stimuli and can selectively switch sensation on or off.

3.4.2 Touch Receptors of Fish Fish also have a sense of touch, but this has been less studied compared to all other sensory systems. The sense of touch in fish consists of a network of free nerve endings that extend into the uppermost layers of the skin. Some of these nerve endings are located in deeper layers of the skin in small capsules that are similar in structure to the Merkel cells of mammalian skin and are therefore also called Merkel cells. Merkel cells have been found in lampreys, lungfish, and some teleosts. They mainly occur in the skin of the lips, the oral cavity, the head, and the trunk. The number of Merkel cells per square millimeter of skin can be  very high, in minnows (Phoxinus phoxinus) up to one hundred Merkel cells per square millimeter of skin were counted. Merkel cells have not yet been detected in  hagfish, cartilaginous fish, and all bony fish not belonging to the teleosts. The touch receptors of fish not only respond to light touch, but also to a bending of the skin (caused e.g. by trunk or fin movements). The touch receptors of fish are highly sensitive, a skin depression by only 0.02 mm already leads to an electrical response. The numerous free nerve endings in the skin of fish often respond not only to touch, but also to chemical, thermal, or harmful stimuli. Fish use their sense of touch not only to perceive touch, but also to obtain tactile information about the substrate on which they live, as well as other fish or conspecifics. With their sense of touch, fish (including rays) detect and locate small prey animals living in the sand. Many fish (e.g., hagfish, some cartilaginous fish, and many teleosts) possess—usually near the mouth—long barbels. Their number is species-specific (from one barbel in cod to 12 barbels in many catfish) and is therefore used as a distinguishing feature. The length of the barbels is also species-specific and varies between 2 to 6% of the body length. In some species (e.g., the deep-sea fish Ultimostomias mirabilis ), the barbels are up to ten times longer as the entire fish. The barbels of many fish are branched, this applies for example to some African catfish (Mochokidae). Barbels are covered with normal skin and usually contain

3  The Sensory World of Fish     39

muscles, with which they can be actively moved. The morphological diversity of the barbels already indicates that their function is highly diverse (Fig. 3.11). In the skin of the barbels of many fish, not only touch receptors are located, but also up to 450 taste cells per square millimeter. With their barbels, fish detect food particles at night, in murky water, or in the deep sea. Among the fish whose barbels do not have taste buds are the Japanese sawshark (Pristiophorus japonicus) and the striped dwarf catfish (Mystus vittatus). Both species use their barbels exclusively for active touch. The dorsal, pectoral, or ventral fins of many fish species have fin rays, which can also be up to ten times as long as the entire fish (Fig. 3.12). In the skin of the fin rays are touch receptors, in some species also numerous taste buds. With fin rays located on the ventral side, these fish detect, among other things, food particles and prey animals in the substrate.

b

a

d

c

Fig. 3.11  The barbels of various fish species. a Deep-sea fish Ultimostomias mirabilis, b African catfish Clarias gariepinus, c Atlantic cod Gadus morhua, d Devil angler Linophryne arborifera. (Modified, after Kasumyan 2011; with kind permission from Plaiades Publishing Ltd. All Rights Reserved)

40     H. Bleckmann

3.4.3 Fish Read Braille As already mentioned, we have an excellent sense of touch. This becomes particularly clear when watching a blind person read Braille. Braille is a dot script developed in 1825 by the Frenchman Louis Braille. Braille consists of tactile dots, raised from the paper by about one millimeter (Braille characters), which - depending on the letter in the alphabet - have a certain distance and a certain arrangement. For reading, blind people scan up to 150 words per minute with a fingertip. If nerve impulses are derived from the mechanosensitive fibers of the fingertip in a test person, each nerve fiber responds to each Braille character (in the experiment, the characters are moved past a stationary finger) with only one nerve impulse. If a letter consists of five  dots, for example, only one nerve impulse is generated in five different nerve fibers. This is the physiological prerequisite for blind people to read Braille. The round goby Neogobius melanostomus is a small European freshwater fish, originally living in the brackish waters of the Black and Azov Seas. As

a

b

c

d

Fig. 3.12  Fish with enlarged fins or extended fin rays. a Flying gurnard Dactyloptena sp., b Paradise threadfin Polynemus paradiseus, c Threadfin Polynemus quinquarius, d Tripod fish Bathypterois sp.  (Modified, after Kasumyan 2011; with kind permission from Plaiades Publishing Ltd. All Rights Reserved)

3  The Sensory World of Fish     41

a stowaway in the ballast tanks of numerous ships, this goby has recently spread explosively in the brackish water areas of the North and Baltic Seas as well as in the river systems of the Rhine, Elbe, and Danube. The rays of the pectoral fins of the round goby contain, like the fin rays of other fish species, numerous mechanosensitive nerve endings and Merkel cells. The gobies use their pectoral fins to explore the surface texture of the substrate, to anchor themselves to the substrate in currents, or to move or burrow purposefully on the substrate. The American researchers Hardy and Hale wanted to know what tactile information round gobies can obtain with their pectoral fins. For this purpose, they conducted the same experiments with gobies as colleagues did with their human test subjects. Hardy and Hale moved the Braille characters along the tip of a pectoral fin ray of the goby, recording the nerve impulses generated by the touch receptors of the pectoral fin ray. The responses were similar to the responses that researchers had derived from the mechanoreceptors of the human fingertip. If round gobies could read, they would be able to decipher Braille with their pectoral fin rays.

a

b

c Fig. 3.13 Deep-sea fish with nose-like protrusion a Longnose chimaera Rhinochimaera atlantica, b Elephant fish Callorhynchus callorhynchus, c Lizard eel Aldrovandia affinis.  (Modified, after Kasumyan 2011; with kind permission from Plaiades Publishing Ltd. All Rights Reserved)

42     H. Bleckmann

Fig. 3.14  Head of the minnow Phoxinus phoxinus in side view (left) and top view (right). The head is covered with numerous breeding bumps.  (Modified, after Kasumyan 2011; with kind permission from Plaiades Publishing Ltd. All Rights Reserved)

Many fish have a nose-like protrusion extending over their front end, referred to as a snout or rostrum. Examples are the “snout” of the elephant fish Callorhynchus callorhynchus as well as the rostrum of the longnose chimaera Rhinochimaera atlantica and the lizard eel Aldrovandia affinis (Fig. 3.13). In the swordfish Xiphias gladius, the extremely long rostrum serves to reduce drag when swimming fast. Flow sensors in the rostrum are probably used to measure (control) the swimming speed. The rostrum of many fish species contains numerous mechanoreceptors, and in electro-sensitive species, also electroreceptors. Many fish search for prey in the substrate with aid of their rostrum (e.g., worms, insect larvae, or small crustaceans), in this case, the rostrum usually contains taste buds in addition to touch  receptors. The touch receptors are Merkel cells and free nerve endings. In many unrelated fish, males grow small bumps of keratin (the same keratin that our toenails and fingernails are made of ) on their head and gill covers at the beginning of the breeding season, and in some species also on the body and fins (Fig. 3.14). After the breeding season, these bumps recede. If females develop bumps, they are smaller than in males. Behavioral observations have shown that males maintain direct body contact with females during egg laying using their breeding bumps. The males use their breeding bumps to take the most favorable position for fertilizing the eggs and maintain this position during mating. In some species, breeding bumps have an additional role in nest defense.

3  The Sensory World of Fish     43

3.5 The Lateral Line System 3.5.1 Lateral Line Organs Have you ever tried to catch a fish in the dark with your hand? Even if your aquarium is small, you probably won’t succeed. The fish always swiftly evades your hand movement at the last moment. The reason for this is its “remote sense of touch”. It is based on a system that Stenosis discovered in the 16th century and is referred to as the lateral line system. The name for the lateral line system came from a row of pores (line) visible to the naked eye along the body of most fish species (Fig. 3.15a). Stenosis also recognized that the pores are connected to a thin canal (the lateral line canal). Lateral line canals can be found in almost all fish species in the head region, e.g. above and below the eyes. Stenosis mistakenly assumed that the lateral line system has the function of producing the slime on the fish skin. Based on anatomical studies by Schulze in 1861 and later also by Leydig in 1868, the suspicion that the lateral line system of fish is a sensory system became more concrete. Thus, Leidig discovered small bumps in the cephalic lateral line canals of the ruff Gymnocephalus cernua from which nerve fibers originate. He therefore called these bumps “nerve buttons” (Fig. 3.15b). Today we know that these “nerve buttons” were canal neuromasts. Lateral line canals are filled with fluid that is connected to the water surrounding the fish via canal pores. In bony fish, there is one canal neuromast between two adjacent canal pores, while in cartilaginous fish there are usually several canal neuromasts between pores. The externally visible part of a neuromast consists of a transparent gelatinous structure (the flag or cupula) that protrudes into the canal fluid. Below the cupula lies a sensory epihelium that can contain up to 3000 hair cells. In addition to the canal neuromasts, fish also have free-standing neuromasts. These are located on the scales (skin) of the head, body, and tail fin (Fig. 3.15a). The number of free-standing neuromasts is species-specific. Trout have fewer than 50, while in goldfish up to 1000 free-standing neuromasts were counted on each side. Canal neuromasts and free-standing neuromasts have a similar structure. The sensory cells of the lateral line neuromasts are hair cells (Fig. 3.15b, left), as they also occur in large numbers in the cochlea, the equilibrium receptors, and the semicircular canals of the human inner ear. The hair cells of the lateral line have a marginal located hair-like long extension, the kinocilium. In addition to the kinocilium, hair cells have up to 150 small “hair-like” extensions, which are referred to as stereovilli. The length of the

44     H. Bleckmann

a

Lateral line canal Cupula Sensory epithelium with hair cells Nerve fibers

Kinocilium and stereovilli

b

Sensory hair cell

Fig. 3.15  a Goldfish (Carassius auratus) with clearly visible canal pores (open circles) along the body. Each black dot on the head, body, and tail fin corresponds to a free-standing neuromast. (Adapted from Bleckmann 2007; with kind permission from Elsevier Inc. All Rights Reserved) b Detail from the opened head lateral line canal of the burbot Lota vulgaris with a canal neuromast, which consists of a sensory epithelium (sensory pad) and a cupula lying above it. In the sensory epithelium, there are numerous hair cells that are contacted (innervated) by fibers of the lateral line nerve. Enlarged representation: Single hair cell with kinocilium and stereovilli.  (Adapted from Flock 1965; with kind permission from Taylor and Francis Group. All Rights Reserved)

stereovilli increases continuously from the edge of the hair cell to the kinocilium (Fig. 3.15b, left). Hair cells are oriented in the sensory epithelium of a neuromast so that an axis drawn through the kinocilium and the stereovilli always runs in the longitudinal direction of the neuromast. The sensory epithelium of a neuromast contains two populations of hair cells that

3  The Sensory World of Fish     45

are oriented in opposite directions. Any fluid movement along the cupula leads to a displacement or deflection of the cupula in the direction of the longitudinal axis of a neuromast and thus to the deflection of the kinocilia and stereovilli. In 1908, Hofer discovered that blinded pike (Esox lucius) swim against the walls of the aquarium if their lateral line is surgically destroyed. Hofer’s experiments remained unnoticed for a long time because they were published in a little-known journal. Unaware of Hofer’s experiments, other researchers assumed that fish can perceive low-frequency sound with their lateral line. This assumption was also false. Until recently, the claim persisted that fish could measure water pressure, which increases with water depth, with their lateral line. This assumption is also incorrect. The Dutch zoologist Sven Dijkgraaf demonstrated 1934 that fish can perceive the smallest water movements with their lateral line. The electrical response of hair cells can be recorded with thin electrodes (microelectrodes). The tip of these electrodes has a diameter of less than one thousandth of a millimeter and is inserted directly into the hair cell for measurement. Measurements showed that hair cells are directional-sensitive. If the stereovilli are deflected towards the kinocilium by just a few nanometers (one nanometer equals one millionth of a millimeter), the electrical potential of the hair cell becomes more positive. If the stereovilli bundles are deflected in the opposite direction, it becomes more negative. Each hair cell therefore is sensitive to the direction in which the kinocilium or the microvilli bundles are deflected. All hair cells in the sensory epithelium of a neuromast are aligned in the longitudinal direction of the neuromast. Therefore they respond maximally to water movements in the longitudinal direction of the cupula and minimally to water movements in the transverse direction. How come that even the smallest water movements deflect the cupula of a lateral line neuromast? To understand this, let’s imagine a rod that is flexibly suspended on one side above a vessel filled with oil and dips into the oil with the other side. If we move the vessel with the oil (and thus the oil) sideways, the lower end of the rod is carried along due to the viscosity of the oil, deflecting the rod. Similarly, the cupula of a lateral line neuromast is deflected due to the viscosity of the water (which is of course much smaller than the viscosity of oil) when water moves laterally along the cupula. The deflection amplitude of the cupula is not proportional to the movement amplitude of the water, but proportional to the speed at which the water moves along the cupula. Free-standing neuromasts therefore respond in

46     H. Bleckmann

proportion of the velocity of water particles along their cupula. Since lateral line neuromasts are directional-sensitive, fish perceive not only the velocity but also the local direction of water particle movements on their head and body surface with their lateral line.

3.5.2 Function of the Canal System But why do fish have a lateral line canal system? To understand how this system works, we need to clarify what forces move the fluid inside lateral line canals. Like free-standing neuromasts, canal neuromasts sense fluid movements, in this case, however, the fluid movements inside the canal. As mentioned above, lateral line canals often contain small pores visible to the naked eye, which connect the canal fluid with the water surrounding the fish. As anyone who has ever snorkeled or dived knows, water exerts pressure that increases with water depth. If adjacent canal pores are exposed to the same pressure, no fluid movement occurs in a lateral line canal. Therefore, fish cannot measure pressure with their lateral line. If another fish swims towards a fish or passes it laterally, local pressure differences occur along the lateral line canals, resulting in pressure differences at adjacent canal pores. The same happens when a fish swims towards or past a stationary object. The result is that the canal fluid moves from the pore exposed to the greatest pressure towards adjacent pores and there leaves the canal to equalize pressure. Canal neuromasts therefore are sensitive to the pressure difference between adjacent canal pores. Fish therefore measure not only the direction and velocity amplitude of water movements on their head and body surface with their lateral line system, but also the pressure gradients along their head and trunk lateral line canals. It should be mentioned that the lateral line system of fish exhibits a high morphological diversity (see Box 2). Box 2 Variability of the lateral line system. The lateral line system of fish consists of free-standing neuromasts and lateral line canals (Fig. 3.16a, b). This basic type has been greatly modified in many fish species during their evolution. Freestanding neuromasts can be located in pits, on small elevations, or on thin stalks (Fig. 3.16c). Due to boundary layer phenomena, neuromasts located in pits react much less sensitively to low-frequency water movements than neuromasts on stalks. The sensory epithelium of a neuromast can contain a few to several thousand hair cells, the cupula can be thin and long or thick and short. All of this influences the sensitivity of the lateral line. All fish have free-standing neuromasts, but there are fish without lateral line canals. These are usually

3  The Sensory World of Fish     47

species of a few centimeters in length. But there are also fish with up to five trunk lateral line canals on each side of the body. Lateral line canals have a diameter of 0.1 to 0.2 mm (in many cyprinids), but also of 5 to 7 mm (in some deep-sea fish). Canals with a small diameter have their greatest sensitivity in the frequency range 100 to 150 Hz, those with a large diameter in the frequency range 5 to 20 Hz. Canal pores can have a small or large diameter. The distances between the canal pores can be small or large. The distance between the canal pores determines the spatial resolution of the lateral line canal system. Canals with a small pore distance have a high, those with a large pore distance have a low spatial resolution (Fig. 3.16d). The resulting functional consequences are probably an adaptation to different hydrodynamic environments, but too little is still known about the natural hydrodynamic environment of fish to say this with certainty.

In a uniform (laminar) flow, all water particles move at the same velocity in the same direction. When a laminar flow encounters an obstacle (e.g., a fish standing in the flow), the flow velocity on the fish’s surface decreases due to the friction of water particles on the fish’s skin. Directly above the skin, the flow velocity is zero centimeters per second, and it continuously increases with increasing distance from the skin. The distance measured perpendicular to the fish’s surface, where the water velocity reaches 99% of the main flow’s velocity, is referred to as the boundary layer. The thickness of the boundary layer depends both on flow velocity and the distance of the measurement point from the fish’s snout (Fig. 3.17a). It is 3.5 cm at a flow velocity of 5 cm per second, 5 cm behind the fish’s snout, and this value decreases to 0.16 cm per second at 50 cm per second (the possible influence of fish slime or fish shape was not considered in the calculation). Boundary layer effects also occur in sinusoidal water movements. In this case, the thickness of the boundary layer depends on stimulus frequency. Thus, the boundary layer has a thickness of 0.35 cm at a frequency of 1 Hz, and only 0.035 cm at 100 Hz. Boundary layer effects have a significant impact on the sensitivity of the lateral line. A neuromast standing in a pit lies deep in the boundary layer, so it mainly responds to higher-frequency water movements (as the boundary layer is very thin in this case). A neuromast standing on a stalk mainly responds to low-frequency water movements, as the boundary layer is very thick in this case. By adjusting the distance of the neuromasts from the fish’s surface, the sensitivity of the lateral line can be adapted to the frequencies of biologically relevant signals. At the same time, it is possible to make the system less sensitive to all other frequencies.

48     H. Bleckmann Free-standing neuromast

Canal neuromast high pressure

Cupula

a

Hair cells

b

low pressure

Hair cells

Free-standing neuromasts

c Canal neuromasts Pressure

d Fig. 3.16  a Free-standing neuromast with cupula and sensory hair cells (only two hair cells are drawn) (from Bleckmann 2007, with kind permission from Elsevier Inc. All Rights Reserved). b Detail of a lateral line canal with two canal pores and one canal neuromast. Both free-standing and canal neuromasts contain two populations of hair cells, which are aligned in opposite directions in the sensory  epithelium. Arrows indicate the direction of water movement. Pressure differences above the canal pores lead to fluid movements inside the canal, which are sensed by canal neuromasts. c Diversity of surface neuromasts. These can, from left to right, depending on the type of fish and/or body region, be arranged in differently deep pits, on the fish surface or at the end of a stalk. d Diversity of lateral line canals. Depending on the type of fish and/or body region lateral line canals can vary in diameter, in the size and shape of their pores, and in the size and shape of the canal neuromasts. In some fish species, constrictions (far right) in the lateral line canal cause a local increase in fluid movement and thus a higher sensitivity. (c and d adapted after Herzog 2021, with kind permission from Elsevier Verlag. All Rights Reserved. To achieve a clearer representation, no scales were drawn in the fish skin)

The marine teleost Xiphister atropurpureus has four trunk lateral line canals on each side of the body, each of which has numerous side canals (tubuli) with up to five pores (Fig. 3.18). There are no neuromasts in the

Distance

3  The Sensory World of Fish     49

a

Velocity Thickness of boundary layer

b

99 % = Boundary layer

Velocity

Distance

Fig. 3.17  a Water velocity in a uniform (laminar) flow (left) and within a laminar boundary layer directly above a flat surface (right). Length of the arrows symbolizes water velocity, b Thickness of the boundary layer as a function of the distance from the measurement point on a flat surface (horizontal line). The further the measurement point, the thicker the boundary layer. (Adapted from McHenry and Liao 2013; with kind permission from Springer-Science + Business Media New York. All Rights Reserved)

tubuli. s. Experiments have shown that the lateral line canals of Xiphister represent spatial low-pass filters. Strongly varying spatial pressure gradients are balanced out by the numerous pores at the level of the tubuli, so that hardly any water movements arrive in the main canal even in spatially highly turbulent flow. Since canal neuromasts in Xiphister are only located in the main canal, they are hardly stimulated even with strong spatial pressure fluctuations. Xiphister lives on the west coast of North America in the surf zone, an area that is highly turbulent. Since biological signals overlay turbulent water movements but do not have spatially high-frequency components, they can still be perceived by Xiphister even in turbulent flow. In rays, parts of the lateral line system serve the sense of touch. The neuromasts in the ventral lateral line canals of rays do not respond to water movements, but only to direct contact with the very soft skin. Even a slight indentation of the skin by a few thousandths of a millimeter leads to fluid movements inside the canals located under the skin, and thus to a stimulation of the canal neuromasts.

50     H. Bleckmann

Tubuli Canal pores Canal neuromasts

2 cm Fig. 3.18  The lateral line canals of Xiphister atropurpureus with side canals (tubuli), canal pores (open circles), and canal neuromasts (black dots or ellipses). (Adapted from Klein et al., 2013; with kind permission from Springer Verlag. All Rights Reserved)

3.5.3 Biologically Relevant Stimuli For many decades, researchers, in order to learn more about the function of the fish lateral line, have stimulated this system exclusively with sinusoidal water movements consisting of only one frequency. With this method, they have achieved numerous basic insights. Thus, lateral line nerve fibers respond highly sensitively to water movements and pressure gradients up to a stimulus frequency of 100 to 150 Hz (Fig. 3.19). At a frequency of 100 Hz, a wave amplitude of only 0.0001 mm already leads to a nerve fiber response. Using the same technique, scientists have found that lateral line nerve fibers are also sensitive to the amplitude of sinusoidal water movements. If the stimulus amplitude increases, the number of nerve impulses per unit of time increases. Natural selection can only optimize sensory systems with regard to the perception of natural (biologically relevant) stimuli. At the same time, peripheral sensory systems are usually designed in such a way that they filter out all irrelevant stimuli occurring for an animal in its natural habitat. The question therefore arises as to what biologically relevant lateral line stimuli look like and which hydrodynamic disturbance stimuli (hydrodynamic noise) predominate in the natural habitats of fishes. My former doctoral student Wolf Hanke dealt extensively with this topic. He started from the hypothesis that the water movements caused by a swimming fish represent an important source of hydrodynamic information. Wolf Hanke was able to show with the method of Particle Image

0,5 mV

3  The Sensory World of Fish     51

20 ms

Fig. 3.19  From top to bottom: Goldfish (Carassius auratus) with a small sphere attached to a rod that vibrates on the side of the fish, nerve impulses of a lateral line fiber and the sinusoidal water movements with which the lateral line was stimulated. In the example shown, each half-wave generates two or three nerve impulses that are forwarded to the brain

Velocimetry (Box 3) that individual vortices detach from the tail fin of an undulating swimming fish. These vortices can still be detected even after several minutes. Box 3  Particle Image Velocimetry.  Measuring and quantifying three-dimensional water movements is difficult, but can be achieved with a method known as Particle Image Velocimetry (PIV). The principle of this method is simple: To visualize water movements, you pour about 0.05 mm large particles into the water. As long as the specific weight of these particles corresponds to that of the water, the particles float. With a laser and a lens, a thin layer of light is created, in which all particles floating in the light layer are visible. Since particles

52     H. Bleckmann move in the same direction and at the same speed as the surrounding water particles, all water movements in the light layer are indirectly made visible. To quantify the water movements, the particles are filmed with a high-speed camera. With image analysis programs, the average direction of particle movement and speed can be determined in any chosen section of the image and at any water depth. With PIV, it was found that individual vortices detach from the tail fin of an undulating swimming fish. This finding was initially not surprising, as other researchers had come to the same conclusion using different methods. However, it was surprising that even a small (10 cm long) fish creates water movements while swimming that last for several minutes. Water movements thus contain, similar to scent trails caused by land animals, historical information. That means that hydrodynamic events that occurred several minutes ago can still be traced. Water movements are not only generated by fish, but also by crabs, small crustaceans (zooplankton) and squids, i.e., potential prey of fish. Running water fish, but also fish living in the surf zone of the world’s oceans, are constantly exposed to water movements that make the perception of biologically relevant water movements difficult. These water movements have not yet been measured in the field, but as will be described below, they could also contain important information.

3.5.4 Hydrodynamic Noise Sensory organs should not only enable an organism to perceive biologically important stimuli, but also have the task of suppressing interference stimuli (noise). Studies over the past decades have shown that nature—wherever possible—eliminates noise at the level of the sensory organs through filtering. This also applies, for example, to our auditory system, which is particularly sensitive in the speech range (approx. 250 to 4000 Hz). For sound frequencies below 20 Hz and above approx. 18,000 Hz, our hearing is insensitive due to the structure of the middle ear and the cochlea. Therefore, we can neither hear the ambient air pressure nor the for us meaningless ultrasonic sounds of bats. Our auditory system acts like a mechanical filter that only allows medium frequencies to pass. The lateral line system of fish is also a mechanical filter, the maximum sensitivity of this filter lies in the low-frequency range of approx. 0.1 Hz to 60 Hz (free-standing neuromasts) to approx. 100 Hz (canal neuromasts). Below and above this range, the lateral line system is much less sensitive. However, there are also fish that can perceive frequencies up to 600 Hz with their lateral line. The question remains, what advantage do fish have from being able to perceive both local water movements and local pressure gradients. The

3  The Sensory World of Fish     53

lateral line system of running water fish is constantly exposed to water flow. Since a uniform flow hardly generates pressure gradients, canal neuromasts are not or only slightly stimulated by running water. However, canal neuromasts are sensitive to all higher-frequency fluctuations that are superimposed on the flow. Higher-frequency fluctuations are generated, among other things, by the undulating tail fin of swimming conspecifics.

3.5.5 Lateral Line and Behavior We now know the sensors of the lateral line and know in which frequency range and how sensitive they respond to water movements and pressure gradients. But what do fish use their lateral line system for? With their lateral line fish that live on small crustaceans and fish larvae can detect the water movements generated by swimming zooplankton. The lateral line system is particularly important at night, in the deep sea or in murky water, i.e. under conditions where the visual system can provide little or no information. Fish generate water movements when swimming undulating with their tail fin, these water motions consist of vortices of alternating rotation direction. Both sharks (Mustelus canis) and catfish (Silurus glanis) can perceive these vortices and use them to detect and track prey fish in darkness or murky water. However, sharks only react to these vortices if they also contain scent traces. Apparently, olfactorly stimuli primarily trigger prey-catching behavior in sharks (see also further below). Fish also use their lateral line to perceive stationary objects. One of the first to recognize this was the Mainzer zoologist Christoph von Campenhausen. His study object was the blind cavefish Anoptychthis jordani. Blind cavefish have no functional eyes, as living in eternal darkness has caused them to lose their originally present eyes over the course of their evolution. However, blind cavefish have a well-developed lateral line system. Von Campenhausen noticed that blind cavefish with an intact lateral line hardly ever swim against the wall of their aquarium. The reason for this is that as they approach a wall, the static pressure in front of the fish increases and this increase is perceived by the head lateral line system. Using the method of operant conditioning, Christoph von Campenhausen demonstrated in the early 1980s that blind cavefish can not only perceive stationary objects with their lateral line, but can also distinguish between them (Box 4). The behavioral experiment was simple. An experimental tank was divided into two equal halves by a wall. On the left and right front side of the wall, thin rods were attached in such a way that the rod

54     H. Bleckmann

spacing on one half of the wall was slightly larger than on the other half. Each half of the wall had an opening through which the cavefish had to swim to receive a food reward. Food was only given if the fish passed through the half of the wall with the smallest rod distances. To explore their environment with the lateral line, blind cavefish repeatedly glide at a short distance without fin movement past unknown objects. The water displaced by them flows evenly from front to back. Could it be that these water movements and the changing pressure gradients on the fish’s surface as they pass an object are perceived by blind cavefish and used for object recognition? To clarify this question, the fish were conditioned to swim through the opening in a wall (Fig. 3.20). If they happened to swim through the opening of the half of the wall whose rods had the smaller distance, they were rewarded with food. If they swam through the opening of the other half of the wall, no food reward was given. The cavefish quickly learned that only passing through the half of the wall with the small rod distances was rewarded. To avoid location training, the halves of the wall were randomly swapped in the experiment. Therefore, the only source of information available to the fish was the  rod spacing. To determine the spatial resolution of the lateral line system, the differences in the distances between the rods were reduced as soon as the fish had reliably solved a task. Differences in rod distances of 1.5 mm were still reliably recognized by the cavefish. The British researcher Burt de Perera has continued the experiments of von Campenhausen and his colleagues. She found out that blind cavefish

Fig. 3.20  Blind cavefish (Astyanax mexicanus) in an experimental tank, which is divided into two equal halves by a partition. On the partition are vertical rods, which in the example shown have a smaller distance in the right half of the partition than in the left half. In each half of the partition there is an opening through which the fish can swim

3  The Sensory World of Fish     55

can distinguish between differently shaped and sized objects with their lateral line. They also remember the location of one or more objects in the aquarium. Blind cavefish therefore use their lateral line system not only for object recognition, but also for object discrimination and spatial orientation. Another well-studied example of the biological significance of the lateral line is the prey-catching behavior of surface-feeding fish. These fish usually stay close to the water surface and catch insects that have fallen into the water. The insects reveal their presence by concentric surface waves of the water, which are created when they try to free themselves from their predicament by wriggling leg or wing movements. The frequencies of the waves generated in this way range from 10 Hz to about 100 Hz, a range in which the lateral line system is particularly sensitive. Surface waves of the water also occur when leaves, plant seeds, small branches, or raindrops fall into the water. These waves lack the high-frequency components of the waves generated by insects, so they are ignored by surface-feeding fish. Behavioral experiments have shown that surface-feeding fish can distinguish between surface waves of different frequencies, provided the frequency difference is at least 10%. A 20 Hz wave is therefore reliably distinguished from a 22 Hz wave. Even a small frequency changes, e.g. from 40 Hz to 42 Hz, in a wave signal is recognized by surface-feeding fish. With their lateral line system, surface-feeding fish can not only detect and distinguish the surface waves of water created by insects from other waves, but they can also locate a prey insect. The surface waves emanating from a point-like stimulus source spread out in a circular pattern in all directions. To reach the stimulus source, surface fish first turn towards the wave center. Then they swim forward and stop as soon as they have reached the location of the stimulus source. They therefore know not only the stimulus angle, but also the distance to the wave source. How they determine the distance was the subject of my doctoral thesis. The first question that arises in this case is the question of the physical parameters that are suitable for locating a wave center (Box 4). Box 4 Physical properties of water surface waves. Anyone who has ever taken a vacation by the sea is familiar with the low-frequency waves that constantly arrive at the coasts of the world’s oceans. In these waves, large masses of water move up and down, the restoring force at work is the gravity of the Earth. Therefore, these waves are also referred to as gravity waves. When an insect struggles on the water surface, waves are also generated. However, these surface waves have only a small amplitude and mainly contain frequencies above 13

56     H. Bleckmann Hz. The main restoring force in this case is not gravity, but the surface tension of the water. Therefore, these waves are also referred to as capillary waves. Capillary waves generated by a point-like stimulus source are circular, i.e. they spread uniformly in all directions. Since the degree of curvature of the wave front decreases with increasing distance from the stimulus source, it is one of the information sources used by surface-feeding fish to determine the distance to the stimulus source. But there are further information sources that reveal  source distance. Due to the surface tension of water, the amplitude of capillary surface waves decreases strongly during wave propagation. This decrease (or attenuation) is frequency-dependent, i.e. it increases with increasing wave frequency. After a distance of only 10 cm, the surface waves generated by a struggling insect, because they contain many frequencies, have mainly lost their high-frequency components. High frequencies in a concentric surface wave stimulus therefore indicate that the distance to the stimulus source can only be a few centimeters. Not only the attenuation, but also the propagation velocity of water surface waves depends on wave frequency. Capillary waves spread increasingly faster with increasing wave frequency (from 23 cm per second at 13 Hz to 40 cm per second at 100 Hz). Since high frequencies propagate faster than low frequencies, the surface wave trains generated by insects show a downward frequency modulation, which decreases with increasing distance to the stimulus source. An example from sports should explain this. Imagine several runners who start running at the same time at a constant but different speed. Before the start, all runners have the same distance to the starting point, namely 0 m. Since the runners run at different speeds after the start, the distance between the individual runners increases over time. From the average running speed and the distance covered by the runners, one can calculate the distance to the starting point. The exact mathematical relationships were taught to me many years ago by Rolf Käse on the beach of La Jolla in Southern California. Rolf is an oceanographer and at that time, like me, was working at the Scripps Institution of Oceanography. Rolf knew that prior to the development of satellite-based measurement methods, his colleagues determined the distance to the center of a storm using the gravity waves arriving at the beach. In case of gravity waves, however, the low-frequency waves reach the beach first, followed by the higher-frequency waves. Behavioral experiments have shown that surface-feeding fish use the frequency modulation at the beginning of a wave train for distance localization—like early oceanographers. In addition, these fish use the damping properties and the degree of curvature of the wave front as an information source for determining the distance to the center of a wave stimulus. Depending on availability and reliability, they even weight these three parameters.

Hydrodynamic Scene Analysis We know the problem. When we are talking to a friend in the city center, our hearing is simultaneously confronted with the noise of moving cars, the squeaking of a passing tram, or the conversations of other people. Something similar happens when everyone is talking at once at a birthday party. It then becomes difficult to understand a conversation partner, as the

3  The Sensory World of Fish     57

sound waves of all sound sources overlap. If our hearing system is intact, we can still hear the words of our counterpart out of all other noises (however, this no longer works if you are hard of hearing in one ear or wear a hearing aid). During a conversation, you can even consciously pay attention to any sound source (cocktail party effect). This is referred to as the ability for auditory scene analysis. Researchers have asked whether the lateral line system of fish is also capable of scene analysis. Behavioral experiments with the surface-feeding fish Pantodon buchholzi have shown that this is indeed the case. Surfacefeeding fish can recognize a surface wave and locate the wave center even when several stimulus sources are active at the same time. This is astonishing, as the surface waves emanating from different stimulus sources overlap spatially and temporally. Surface-feeding fish therefore perform a real scene analysis with their lateral line.

Intraspecific Communication Some fish use their lateral line system for intraspecific communication. Male fighting fish (Betta splendens) build foam nests on the water surface, into which the females lay their eggs. After fertilizing the eggs, the males guard the young fish that hatch from the eggs, which initially prefer to stay in the immediate vicinity of the foam nest. Studies by Siegfried Kaus, then a diploma student in the same lab as me, have shown that male fighting fish generate surface waves of frequency 13 Hz with their pectoral fins in case of danger. As soon as these waves reach the juvenile fish, they immediately swim towards the male. The male collects them in his mouth, swims back to the nest, and spits the juvenile fish out there again. Males of many fish species fight for females. The water movements generated by the males during their display with their fins or the entire body serve to intimidate the opponent. Salmon vibrate their entire body just before egg laying. The resulting water movements are perceived by the males with their lateral line system. This allows them to synchronize their mating behavior. Fish schools are referred to as the temporary accumulation of a few to several million fish, usually of the same species. Many schooling fish swim in tight formation and change their direction almost simultaneously. There is no leader in a fish school, all movements are decentralized. The advantage is that no central entity can fail and thus paralyze the swarm behavior. Systems organized without a fixed leader are common in biology and extremely reliable. When a school changes its direction, one of the animals on the edge

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of the school becomes the leader for a brief moment. The strict order of the school is only lifted when the fish rest or disperse to feed. How do schooling fish manage to maintain constant distances to their nearest neighbors? Surprisingly, they manage to do this even when the school has to make quick evasive movements due to danger. During the day, schooling fish mainly use their visual system for this performance. Each individual fish observes its nearest neighbors and follows their movement in a flash. Surprisingly, fish can also school in complete darkness, provided they have an intact lateral line system. If this system is temporarily damaged with antibiotics or a cell poison (e.g., cobalt chloride) (both substances reversibly damage the hair cells of the lateral line), no schooling behavior occurs anymore in the dark.

Energy-Efficient Movement Have you ever wondered why brook trout and other stream fish can stand so effortlessly in a current? To avoid drifting away, they are obviously highly adapted to life in fast running waters. The difference in the performance of various fish species became suddenly clear to me many years ago during experiments in the laboratory of Werner Nachtigall, then chairholder at the University of Saarland. Together with Thomas Breithaupt and Reinhard Blickhan, we examined the water movements in the wake of swimming trout. For the experiments, we had a flow tank available in which we could vary flow velocity over a wide range. Even at a flow velocity of 70 cm per second, the approximately 30 cm long trout had no trouble maintaining their position in the flow tank for several minutes. As fish adapted to fast-flowing waters, trout have an extraordinarily streamlined body and highly efficient swimming musculature. This only became clear to me when we put similarly sized goldfish into the flow  tank. Even at a flow speed of 50 cm per second, these were driven against a downstream grid within a few seconds despite vigorous swimming movements. In addition to an optimized head, body, and fin shape, trout also use sensory information for energy-efficient locomotion. In rivers and streams, trout (and other rheophilic fish) are constantly at risk of drifting downstream. To avoid this, they must either continuously swim against the current or specifically seek out areas with low flow in a body of water. Trout know other tricks to maintain their position in a current with as little energy expenditure as possible. If there is an object (e.g., a stone or a root) in a stream or river, the flow conditions change in its vicinity (Fig. 3.21). Upstream of the object is a zone with increased pressure and significantly reduced flow speed. Immediately next to the object, the flow speed

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Fig. 3.21  Preferred locations of trout near a flow-exposed half-cylinder (top left). To save energy, trout either stay in the high pressure zone in front of the half-cylinder, diagonally next to the half-cylinder, or in the vortex street generated downstream by the half-cylinder (red and blue arrows). The direction of rotation of the arrows corresponds to the direction of rotation of the water in the wake of the cylinder

is increased because the water has to flow around the object. Downstream (in the experiment a half-cylinder was used as an object), individual vortices with opposite directions of rotation detach on the right and left of the half-cylinder. Trout thus have several options to avoid drifting in a current without great energy expenditure. Behavioral experiments by the American researcher James Liao have shown that trout prefer to stay either directly in the high pressure zone in front of the cylinder or downstream in the vortex street behind the cylinder. In this case, they meander passively (a dead trout attached to a string moves in the same way) between the individual vortices, in such a way that only the upstream rotating part of a vortex comes into contact with the body of the trout. Often you can also observe that trout stand motionless diagonally sideways and slightly downstream from the cylinder. Christoph Brücker from the City University of London, with whom I have collaborated for many years, found the reason for this: Behind a flow-exposed object, a zone of reduced pressure and low flow speed forms. Trout use both the downstream force generated by the flow and the upstream force created by the low-pressure zone behind the object. At the locations preferred by trout, these forces cancel each other out, so active movements are only necessary for correction movements even in strong currents. Studies by my former

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doctoral student Adrian Klein and others have shown that trout perform less muscle work at the locations they prefer in a current than when swimming in open water. They also consume less oxygen and therefore less energy there. During the day, trout use their visual system to remain in flow-favorable zones. My former doctoral student Anja Przybilla then showed that if the cylinder is slowly moved perpendicular to flow direction trout can only do this in the dark if they have an intact lateral line system. For a long time, it has been speculated whether schooling fish can save energy through their synchronous swimming style. Since the energy consumption of a single schooling fish can hardly be measured, scientists from the Max Planck Institute for Behavioral Biology Konstanz, the University of Konstanz, and the University of Beijing have built fish-like robots that move undulatorily (wave-like) with a soft tail fin, similar to fish. Experiments have shown that the robot fish save energy when they adapt their tail fin stroke to that of the fish in front of them, with a corresponding time delay necessary depending on their position in the school. The robot fish used the vortices generated by the tail fin of a neighboring robot fish to save energy, a strategy referred to by the researchers as “vortex-phase matching”. For fish swimming directly next to a lead fish, it is particularly energy-efficient to synchronize their tail stroke with that of the lead fish. The greater the distance to the lead fish, the greater the delay to the tail fin stroke of the lead fish must be. Behavioral experiments then provided the final proof that “real” schooling fish behave just as the researchers had predicted based on their experiments with artificial fish. Schooling fish, therefore, use vortices to save energy, similar to a trout standing in a current.

Lateral Line and Social Environment It is known that social distancing and self-isolation have a devastating effect on humans and animals. What was unknown is which circuits in the brain are involved in the perception of the social environment. Lukas Anneser and Erin Schumann from the Max Planck Institute for Brain Research, with the help of other colleagues, discovered a brain molecule that acts as a “sensor” indicating the presence of conspecifics. They chose the zebrafish Danio rerio, which roams in loose schools in nature, as a model organism. The researchers found several genes (sections on the DNA that encode specific proteins with the help of RNA), whose expression (reading) was consistently altered in fish that were raised in social isolation. One of these genes encodes for the parathyroid hormone 2 (pth2), a relatively unknown hormone. Surprisingly,

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the expression of pth2 not only reflected the presence of other zebrafish but also their number in the experimental tank. When zebrafish were kept individually, the concentration of pth2 in the brain decreased. The expression level increased again within 30 minutes when the social isolation of a fish was lifted. Further experiments showed that the fish’s lateral line system controls the expression of pth2. Zebrafish apparently feel the swimming movements of other fish and thus the presence of conspecifics with their lateral line. When the researchers simulated the water movements generated by swimming zebrafish with robot fish, the expression of pth2 also increased. This shows that hydrodynamic stimuli are sufficient to increase the expression of pth2.

Basic Research When one, like me, has spent a lifetime dealing with basic research, the discussion inevitably arises as to what basic research is actually good for. It would be better to spend the money directly on applied research. Many years ago, I applied for the Bennigsen-Foerder Prize of the state of North Rhine-Westphalia, which was then endowed with 100,000 DM (German Mark). The research concept I submitted obviously appealed to the jury, which consisted of politicians, journalists, and scientists, because I was invited to give a lecture in Cologne. There were other applicants besides me, I can still remember two of them. One gave a medical lecture on the topic of rheumatism. After the lecture, he was asked why it was important to study rheumatism. The answer was easy. Rheumatism not only causes great human suffering, but also economic damage in the billions. The second speaker was an economist. He too was able to provide solid arguments as to why his research was important. I wanted to use the funding to investigate the lateral line system of fish. After my lecture, the obligatory question came up as to what benefit my research would have. I didn’t like this question even then, because it subtly implies that pure gain in knowledge does not justify the funds used, as it brings no benefit. Since I was firmly convinced that I would not get the prize anyway, I said to the jury after my lecture: “My research is good for nothing.” To my surprise, some members of the jury began to defend me. Sharks often attack shipwrecked people, so it is important to learn more about their sensory systems. Numerous other arguments were made, emphasizing the potential significance of my sensory biological research. I received the prize. My name was published with the amount of the prize money in the local press. As a result, my neighbors thought the

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money was intended for my private consumption. Of course, this was wrong, because scientific prizes are almost always only used to finance research work. And that’s a good thing. Approximately 50% of all knowledge important to humanity comes from basic research. Without basic research, we would not know that there are cells, molecules, genes, bacteria, or viruses, nor would we know anything about ecological relationships, the insect die-off, the importance of the ozone layer for life on earth, or the way hormones work. Without basic research, we would not have invented steam engines or the Otto engine, there would be no molecular biology, genetic engineering, electric power, or computers. In short, without basic research, we would still live much like our ape-like ancestors (which might be better, according to my wife). For more than 100 years, lateral line research was pure basic research. This has changed fundamentally in the last twenty years. Today, artificial (bionic) lateral line systems are being developed in numerous laboratories with the aim of building miniaturized highly sensitive flow and pressure gradient sensors for technical applications. The jury and I did not know at the time I applied for the Bennigsen-Foerder Prize that lateral line research would  ever experience an application.

3.6 The Sense of Balance 3.6.1 Anatomy of the Inner Ear We become aware of the importance of most sensory organs immediately after birth, as we can see with our eyes, hear with our ears, and smell with our nose. The sense of taste, touch, temperature, and pain are also omnipresent throughout our lives. In contrast, we usually only become aware of the importance of the sense of balance when it fails, as we then become dizzy and can neither stand upright nor walk straight. The inner ear of vertebrates has developed balance or equilibrium organs (the vestibular apparatus) for spatial orientation and movement control, which consist of three semicircular canals (two in lampreys) and three otolith organs. In fish, these organs are called the utricle, saccule, and lagena (Fig. 3.22). The inner ear of mammals and birds is similar to that of fish, but the lagena has developed into a hearing organ (the cochlea) for perceiving sound waves. The three semicircular canals of the inner ear run in planes perpendicular to each other and are directly connected to the utricle. With normal head posture, two of the three canals are horizontally, the third is

3  The Sensory World of Fish     63

vertically oriented. At the end of each canal is an organ similar in structure to the neuromasts of the lateral line. Hair sensory cells lie underneath a gelatinous cupula, which is deflected by the slightest fluid movements in the canals. These fluid movements, which occur with every rotation of the head, are detected by the hair cells. Like us, fish perceive rotational movements in all three spatial planes with their semicircular canals.

3.6.2 Function and Performance of the Sense of Balance The inner ear of fish not only perceives every rotation of the head but also the position of the head relative to the earth’s gravity. It also informs fish about linear accelerations. All three, the utricle, saccule and the lagena, contain sensory epithelia that—depending on the species of fish—contain up to several hundred thousand hair cells. The cilia or stereovilli of these hair cells protrude into a gelatinous mass in which a small stone (an otolith) or several small stones (otoconia) are embedded. In bony fish, the otoliths consist of calcium carbonate. Depending on the species, they have a different size and shape (for one example see Fig. 3.22b). While the otolith of the utricle rests on the sensory epithelium in normal head position, the otoliths of the saccule and the lagena are each laterally attached to the sensory  epitelium. Since gravity pulls the otoliths downwards, any change in the position of

Anterior vertical canal Posterior vertical canal

Ampullae with sensory epithelia

Utriculus

Semicircular canals

Horizontal canal

Utriculus Lagena Otolith Sacculus

Sacculus

a

Lagena

1 cm

b

Fig. 3.22  a The inner ear of a bony fish with the three semicircular canals and the utricle, saccule, and lagena. (From Hildebrandt et al., 2021, with kind permission from Springer-Verlag GmbH. All Rights Reserved) b Inner ear of the flatnose cod Antimora rostrata with three otoliths. (Reprint with kind permission from Xiaohong Deng)

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the head is perceived by the sensory epithelium of the otolith organs and reported to the brain. In most fish species, the utricle is of great importance for orientation. In addition to the three otolith organs and the semicircular canals, the inner ear of sharks contains another sensory system, the macula neglecta, which contains up to 300,000 hair cells. In the macula neglecta, the stereovilli of the hair cells protrude into the fluid of the inner ear, an otolith is missing. With information of their inner ear, fish always know where up and down is, even at night, in the deep sea, or in the murky water of a slowly flowing river. I once experienced how unpleasant the loss of this spatial information can be while diving. The water of the Indian Ocean was so murky that day that I completely lost my spatial orientation when surfacing. Only the knowledge that the air bubbles escaping from the mouthpiece of the regulator always rise showed me the way to the water surface. Turbulence often occurs in natural flowing waters and in the surf zone of the world’s oceans. Since fish can sense the smallest linear and angular accelerations with their inner ears, they are informed about any change in the direction or speed of the current, even in the dark.

3.7 The Sense of Hearing 3.7.1 The Ear of Mammals The fact that mammals can hear is already recognized by layman by their pinnae. In addition to the pinnae, the hearing system of mammals consists of an ear canal and the—not visible from the outside—middle ear with the tympanum and the auditory ossicles  malleus, incus and stapes. The actual hearing organ of mammals—the cochlea—is located in the inner ear. It has evolved from the lagena of fish. Fish do not have pinnae, a middle ear, or a cochlea. Therefore, it is not surprising that even zoologists have long suspected that fish are deaf. This was consistent with the observation that fish apparently do not make any sounds or noises. Today we know that both assumptions were wrong. The first scientist to provide evidence that fish can hear was Karl von Frisch. He was awarded the Nobel Prize for Medicine in 1973 together with Konrad Lorenz and Nicolaas Tinbergen. Karl von Frisch became particularly well known for his studies on honeybees. He discovered that bees

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communicate the location and quality of a food source to their hive mates using waggle dances. Since experiments with bees cannot be carried out in winter, Karl von Frisch, as a diligent scientist, studied the hearing ability of fish during the cold season. Every aquarist knows this. As soon as you approach the aquarium to feed, the fish swim to the edge of the tank. To test whether fish can hear, Karl von Frisch came up with a simple but ingenious idea. Just before feeding his dwarf catfish, he whistled each time without the catfish being able to see him. Soon, the whistle alone prompted the catfish to seek the edge of the aquarium in anticipation of food. Just a few years later, Stetter showed that minnows, golden orfe, goldfish, gudgeons, and sculpins could also be conditioned to sounds. Since fish lack a cochlea, it remained unclear for a long time what they hear with. In order to specifically search for anatomical structures suitable for hearing, researchers were forced to first deal with the physical basics of hearing (Box 5). Box 5 Physics of hearing. Every object that moves in air or water or changes its volume generates sound waves that spread evenly in all spatial directions. Sound waves consist of a pressure and a movement component. Sound waves modulate the ambient pressure (the air or water pressure) with the frequency of the sound wave. In addition to pressure changes, sound waves cause particle movements: the medium particles (air or water molecules) oscillate with the frequency of the sound wave in the direction of wave propagation. The air or water particles collide with neighboring particles and thus transfer some of their kinetic energy to the neighbors. In sound waves, compression energy is therefore converted into kinetic energy and vice versa. Physically, the two forms of energy of a sound wave are referred to as sound pressure and sound velocity component (velocity of the medium particles oscillating around their rest position). Hearing systems must be built in such a way that they can measure either the sound pressure component, the sound velocity component, or both components. To measure the sound pressure component, animals need sound pressure receivers. In technology, this is usually a microphone that measures the air pressure fluctuations caused by sound waves by setting a membrane vibrating at the frequency of the sound pressure waves. The membrane vibrations are converted into electrical voltage fluctuations and read out as a microphone signal. To measure the particle movement component, engineers, physicists, and biologists use particle image velocimetry in addition to hot-wire anemometers. In the latter measurement method, the air or water particles moved by a sound wave cool a thin heated wire and thereby change its electrical resistance. This resistance change is converted into an electrical signal and thus made visible.

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Mammalian ears are sound pressure receivers. Any change in sound pressure causes movements of the eardrum (analogous to the membrane of a microphone). This leads to a movement of the three auditory ossicles and finally to the stimulation of sensory cells in the cochlea (these cells are similar hair cells as in the lateral line neuromasts of fish). Mammals and birds perceive the sound pressure component, but not the velocity component of a sound wave. Most insects and all spiders can do this, however. They have very thin “hairs” (hearing hairs) that are not visible to the naked eye and are deflected by even the smallest air movements. This deflection is perceived by sensory cells at the base of the hairs and reported to the central nervous system. The hearing hairs of insects and spiders are sound velocity receivers. Since fish neither have pinnae nor an eardrum, auditory ossicles, a cochlea, or hearing hairs, scientists had to look for other structures that might be suitable for hearing. These structures should be designed in such a way that they can detect sound pressure, sound velocity, or both.

3.7.2 The Ear of Fish To measure the sound pressure component, fish, according to the researchers’ considerations, should have an air-filled bladder. Let’s imagine we take a balloon underwater when we dive. As the water depth increases, the ambient pressure rises, causing the size (volume) of the balloon to continuously decrease. When we ascend at the end of the dive, the size of the balloon increases continuously with decreasing water depth (with decreasing pressure) and eventually returns to its original size at the water surface. As a result of this size change, the outer shell of the balloon moves. If we could detect this movement, we would have a simple pressure gauge. Fish do not carry a balloon, but many species have an air-filled swim bladder, whose original function was to regulate buoyancy. Divers use their buoyancy compensator (jacket) for the same purpose. As the volume of the airfilled buoyancy compensator constantly decreases due to increasing water pressure when diving, a diver descends increasingly faster with increasing water depth. To avoid this, he inflates small amounts of air from his compressed air bottle into the buoyancy compensator in a controlled manner. Conversely, he must release air from the buoyancy compensator when ascending to avoid uncontrolled ascent. To regulate buoyancy, fish can also actively regulate the volume of their swim bladder—if they have one—by air separation via their blood vessels.

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In addition to regulating buoyancy, the swim bladder also serves as a hearing aid in many fish. When fish are exposed to an underwater sound wave, the volume of their swim bladder—similar to that of a balloon—varies with the frequency of the sound pressure wave (as the pressure increases, the swim bladder becomes smaller, as the pressure decreases, it becomes larger again). This leads to small (in the range of one millionth of a millimeter), but measurable movements of the swim bladder wall. These movements are transmitted in carp-like fish and catfish, or the Ostariophysans, to the inner ear using small bones, the Weberian ossicles (Fig. 3.23). The Weberian ossicles thus have a similar function as the auditory ossicles in the middle ear of mammals. The movements of the Weberian ossicles cause minimal fluid movements in the inner ear of the fish, which deflect the stereovilli of hair cells (usually those of the utricle) and can thus be percived by the fish. This gives fish the ability to detect even the smallest sound pressure waves. Since most fish with a swim bladder only have one swim bladder (in some fish species the swim bladder is divided), they only have one sound pressure receiver. With only one sound pressure receiver, it is not possible to locate a sound

Inner ear with semicircular canals

Weberian ossicles

Swim bladder

Fig. 3.23  Hearing apparatus of an Ostariophysan. Each pressure change (e.g., due to a sound wave) in the water leads to volume changes of the swim bladder and thus to wall movements of the swim bladder. These wall movements are transferred to Weberian ossicles (blue) and then to the fluid of the inner ear. These fluid movements are sensed by hair cells of the inner ear

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source. Because no matter from which direction the sound comes, the sound pressure receiver (the swim bladder) always experiences the same pressure changes. These considerations led Karl von Frisch to the mistaken assumption in the last century that fish can hear, but cannot locate the source of a sound. The inner ear of fish, similar to the lateral line system, shows an extraordinary anatomical diversity. In more than twenty fish families, there are inner ear specializations that have evolved exclusively to improve sound pressure perception. In some catfish (e.g., Ancistrus sp.), the swim bladder is divided into two parts, each connected to an inner ear and a cephalic lateral line canal. In this case, sound pressure waves move not only the fluid in the inner ear, but also the fluid in a cephalic lateral line canal. In this case, fish probably indirectly use their lateral line system for hearing. The same applies to reef-dwelling butterfly fish (Chaetodontidae). Many fish have two air-filled bladders, branching off from the swim bladder, in close proximity to the inner ear (the sacculus), while in other fish (e.g., in some soldierfish (Holocentridae), cichlids (Cichlidae) and herring-like fish (Clupeidae)) the swim bladder shows elongated extensions that reach to the inner ear. In this way, the vibrating membranes of the swim bladder function as an eardrum. Labyrinth fish have a special cavity for air breathing, which is connected to the inner ear (sacculus) via a thin membrane. Mormyrids (weakly electric fish from Africa, see below) have an air-filled bladder in each inner ear, which separates from the swim bladder during embryonic development. All fish with air-filled bladders coupled to the inner ear have excellent hearing, they can perceive sounds in the frequency range 50 Hz to about 1500 Hz (some species up to 9000 Hz). Herring-like fish from the Alosinae family are the preferred prey of dolphins. Presumably for this reason, they can hear the ultrasonic waves of hunting dolphins (>150,000 Hz) and thus evade the dolphins early. Infrasound waves (0.1 Hz to approx. 20 Hz) alternating electric fields, even if these have an amplitude of only one hundred thousandth of a volt per cm (0.01 μV per cm, 1 μV = 1 thousandth of a volt). If one pole of a 10-V battery is held in the Wadden Sea of the North Sea and the other pole in the Atlantic off New York, a shark can theoretically still sense the electric field generated by the battery. For many years it remained a mystery why the canals of the ampullae of Lorenzini are so long. There are two reasons for this:

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Top side

Bottom side

Fig. 3.25  Canals of the ampullary organs of a ray. Each half of a top and bottom side is shown and separated by a dashed line. (From Hildebrandt et al., 2021, with kind permission from Springer-Verlag GmbH. All Rights Reserved)

Skin

Pore Canal

Ampulla Sensory cell Nerve fibers Fig. 3.26  Ampullary organ of a ray with sensory cells (only three sensory cells are drawn), canal and canal pore (not to be confused with lateral line canals and lateral line canal pores). The ampullary organs measure the potential difference between the canal pore and the sensory cells located at the end of the canal in an ampulla. The potential difference is zero when electric field lines run parallel to the canal, and maximum when they run perpendicular to the longitudinal axis of the canal and parallel to the skin surface. Since the canals of different organs run in different directions (Fig. 3.25), the fish automatically receives information about the direction of the perceived electric field

1. The skin of marine sharks and rays has a low electrical resistance. Therefore, electric field lines penetrate the skin almost unhindered. As a result the potential differences between the skin surface and the inside of the skin (or the sensory cells of the electroreceptors located in the skin) are very small. 2. Due to the high conductivity of seawater, biological current sources can only build up low voltage amplitudes permanently (if you hold the two

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poles of a battery in seawater, the poles will be short-circuited and the battery will quickly run out). Therefore, the electroreceptors of marine cartilaginous fish must be extraordinarily sensitive. Since the canal walls of the ampullae of Lorenzini have a high electrical resistance compared to the skin, the ampullae do not measure the potential difference between the sensory cells and the skin area above the sensory cells, but the potential difference between the sensory cells and the skin area where the pore of the respective canal opens. Due to the great length of the canals, not only a very high sensitivity but also a directional sensitivity of the ampullae of Lorenzini is achieved. If the electric field lines run parallel to the longitudinal axis of a canal, no potential difference can be measured at the sensory cells. However, if the electric field lines run perpendicular to the longitudinal axis of the canal and parallel to the surface of the fish, the sensory cells of the ampulla are maximally stimulated in the presence of an external electric field. Since the canals of different ampullae are arranged in different directions (see Fig. 3.25), sharks and rays receive clear information about the direction of the surrounding electric field lines through the comparison of the neuronal activity of different ampullae of Lorenzini.

3.8.2 Passive Electric Sense The question remains, what bioelectric fields exist in the sea and what is their origin. All aquatic animals, as well as all water plants, are surrounded by weak direct current electric fields. These bioelectric fields are caused by ion flows across cell membranes (e.g., across the membranes of the gills) and can reach an amplitude of up to 500 μV per cm (in injured animals even up to one millivolt per centimeter) measured directly above the skin. The direct current field surrounding each fish is low frequency modulated by gill and fin movements. In 1966, the Dutch zoologist Ad Kalmijn provided evidence that rays (Raja clavata) and sharks (Scyliorhinus canicula) can detect flatfish (Pleuronectes platessa) buried in the sand with their ampullae of Lorenzini. If the fish buried in the sand was electrically isolated, the sharks could no longer find it. Conversely, a battery, if it produced a similar electric field as a flatfish, caused the sharks to dug tenaciously at the source of the field. These experiments also showed that the sense of smell plays only a minor role in locating prey.

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The ability to perceive weak bioelectric fields is not only found in sharks, rays, and sea cats, but also in lampreys, sturgeons, paddlefish, catfish, lungfish, and coelacanths. In addition, all weakly electric fish have ampullary organs (see below). Electroreceptive bony fish have similar ampullary organs to cartilaginous fish, but their ampullae contain fewer than 50 sensory cells. In addition, the long jelly-filled canals of the cartilaginous fish are missing. The reason is that the skin of bony fish, unlike the skin of cartilaginous fish, has a high electrical resistance. This creates sufficiently high potential differences at the sensory cells of the ampullary organs even with short canals when electrically stimulated. The ampullary organs of bony fish, like those of cartilaginous fish, are used to detect prey, conspecifics, and enemies. Paddlefish (Polyodon spathula) live in the Mississippi River system. Young paddlefish use their ampullary organs to locate and catch small crustaceans. On the “spoon” of a paddlefish, an extended forehead part that can reach a third of the total length of the fish (Fig. 3.27), are up to 75,000 ampullary organs. Since paddlefish live in running waters, they only need to wait until a downstream drifting small crustacean is detected by the electroreceptors at the tip of their spoon. With the numerous electroreceptors on their spoon, the sturgeons follow the movement of the small crustacean until it reaches the vicinity of the mouth. Through a rapid sideways movement of the head, the small crustacean is then brought to the mouth. The spoon of the paddlefish thus functions as an electrical antenna. Rays (Raja eglanteria) temporarily stop their gill movements when they perceive a weak low-frequency electric field. This way, they avoid water movements that would reveal their presence to a predator. In nature,

Fig. 3.27 Paddlefish (Polyodon spathula). Paddlefish live in the Mississippi River basin. They were once widespread, but dams, water pollution, and fishing have brought them to the brink of extinction. Paddlefish feed on small crustaceans and zooplankton. (Photo J. S. Müller. All Rights Reserved)

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low-frequency electric fields indicate, among other things, the presence of predatory fish. In addition to bioelectric fields, there are also homogeneous large-scale electric fields in streams, rivers, lakes, and the world’s oceans, caused by water currents or current fluctuations. Some fish apparently can use these fields for spatial orientation. For example, round stingrays (Urolophus halleri) have been conditioned to swim to a sector in the experimental tank that had a certain electrical polarity.

3.8.3 Active Electric Sense Fishermen discovered more than 2000 years ago that some fish can cause shock-like sensations upon touch. It was not until the second half of the 19th century that physicists were able to prove that these phenomena were electric shocks. Tomb paintings from ancient Egypt depict the electric catfish Malapterus electricus, a freshwater fish that generates discharges of several hundred volts. Other strongly electric fish include the South American electric eel Electrophorus electricus, the marine electric ray Torpedo nobiliana, and the stargazer Astroscopus guttatus. Since seawater, unlike freshwater, conducts electric current well, the electric discharges of saltwater fish have relatively low voltage amplitudes but high current strengths. In contrast, the discharges of freshwater fish in poorly conducting water are characterized by high voltages and low current strengths. Strongly electric fish generate their electric discharges with special electric organs that have evolved from transformed muscle cells. The electric discharges of these fish serve for defense as well as for stunning and killing prey. In addition to strongly electric fish, scientists early on discovered fish in the rivers and streams of Africa and South America with organs that resemble the electric organs of strongly electric fish. These fish include the Mormyrids living in Africa and the Gymnotids native to South America. Since touching these fish does not result in a noticeable electric shock, researchers long assumed that the electric organs of Mormyrids and Gymnotids are non-functional. These fish were therefore called pseudo-electric fish. Charles Darwin pointed out that the existence of non-functional organs is inexplicable for any evolutionary biologist. After all, natural selection can only produce organs that have a selective advantage. In the middle of the last century, Harry Grundfest discovered that even the pseudo-electric fish continuously generate electric signals (so-called EODs, derived from “Electric Organ Discharge”). The EODs have an amplitude of only a few volts on the body surface and therefore

80     H. Bleckmann

remained undetected for a long time. The electric signals of the pseudo-electric or weakly electric fish are not suitable for defense or for stunning or killing prey due to their low current strength and voltage, so their function remained a mystery for a long time. The African and South American waters inhabited by weakly electric fish have a low electrical conductivity and are usually turbid. In addition, almost all weakly electric fish are nocturnal and usually have only small, not very powerful eyes. The electric organs of weakly electric fish have evolved from transformed muscle or nerve cells. Two types of weakly electric fish can be distinguished, the pulse dischargers and the wave dischargers. The electric impulses of the pulse dischargers last from less than one to several milliseconds, they are continuously emitted day and night at a variable repetition rate of 1 Hz to about 100 Hz. In contrast, wave dischargers continuously generate sinusoidal signals, which depending on the species, have a frequency between 200 Hz and 2000 Hz (Fig. 3.28). Pulse duration and pulse shape of the pulse dischargers are sex- and species-specific. The same applies to the discharge frequency of the wave dischargers. In 1958, Hans Lissmann of the University of Cambridge proved that weakly electric fish can distinguish between two equally large and equally shaped clay vessels in total darkness, provided one vessel contains aquarium water (water with comparatively high electrical conductivity) and the other distilled water (water with comparatively low electrical conductivity). This proved that weakly electric fish can use their electric sense for object recognition (Box 6). Box 6 Physics of Electrolocation. To understand how weakly electric fish can distinguish objects using their electric sense, a brief detour into physics is helpful. Every inanimate object (every dead material) has an electrical (ohmic) resistance. This can be low (e.g., in a silver or copper wire) or high (e.g., in a stone). As a weakly electric fish approaches a non-conductor or an object with high electrical resistance, the amplitude of the electric organ discharge (EOD) generated by the fish decreases at skin areas closest to the stone. The reason for this is that stones, as non-conductors, repel electric field lines. An object whose conductivity is greater than that of water, on the other hand, attracts electric field lines (Fig. 3.29). This locally leads to an increase of the amplitude of the EOD generated by the fish. Weakly electric fish can sense changes in the amplitude of the EODs with their high-frequency electroreceptors and use them for object recognition. Behavioral experiments have shown that weakly electric fish can still discriminate ohmic resistances in a two-choice test even if they differ by less than one percent.

3  The Sensory World of Fish     81 Gnathonemus petersii

Amplitude (mV)

+ 0 125 µs

– a

300 ms

b

Eigenmannia sp.

Amplitude (mV)

+

0 –

c

5 ms

Fig. 3.28  Electric discharge of a pulse discharger (Gnathonemus petersii) and a wave discharger (Eigenmannia sp.). Note the different time axes. (From Bleckmann et al., 2004; with kind permission of Springer-Verlag GmbH. All Rights Reserved)

Following the discoveries of Lissmann, the search for the electric sensory organs of weakly electric fish began. This search revealed that these fish have two or even three different types of electroreceptors, which are distributed in different densities on the head and body. With their ampullary organs, weakly electric fish as well as rays and sharks exclusively detect low-frequency electric fields. A second type of electroreceptor is only sensitive to high-frequency electric fields, this type is referred to as tuberous receptor or tuberous organ and is only found in weakly electric fish. With tuberous organs, weakly electric fish perceive their own electric discharges, but also the discharges of conspecifics or other weakly electric fish.

82     H. Bleckmann

Gerhard von der Emde from the University of Bonn has been investigating the object discrimination ability of weakly electric fish for many years. According to his studies, weakly electric fish (Gnathonemus petersii ) can use their electric sense not only to distinguish objects, but also to recognize the size and shape of objects, even if they are made of the same material (i.e., have the same electrical (ohmic) resistance). If the animals are offered a cylinder and a pyramid made of the same material in a two-choice test in darkness and are only rewarded when they approach the cylinder, they choose this one after a few days of testing in almost 100% of all cases. For object discrimination, the fish use not only the shape, but also the different volume of the objects. Weakly electric fish also recognize whether objects have a

Gymnarchus niloticus

b

Fig. 3.29  a Electric field (flow of electric current) of the weakly electric fish Gymnarchus niloticus. b Electric field changes due to objects with purely ohmic resistance. The black circle symbolizes an object whose electrical resistance is greater than that of water (the object repels the electric field lines), the hatched circle an object whose ohmic resistance is lower than that of water (the object attracts the electric field lines).  (From Hildebrandt et al., 2021, with kind permission from SpringerVerlag GmbH. All Rights Reserved)

3  The Sensory World of Fish     83

sharp or rounded edges with aid of their electroreceptors. When new objects are presented to the fish without food reward, they prefer the object that most resembles the previously rewarded object. The fish can therefore also generalize. Our brain can transfer the information obtained with one sensory system (e.g., the eyes) to another sensory system. For example, if someone shows us an unknown object, we can find this object in the dark only with our sense of touch among several objects. Our visual system has informed the tactile system about how the object should feel when touched. Weakly electric fish show a similar cognitive performance. If they are shown an electrically shielded object in the light, they can recognize it in the dark only with their electric sense. Whether weakly electric fish can also distinguish between animate (e.g., insect larvae or small crustaceans) and inanimate objects (e.g., stones or dead leaves) is an exciting question that Gerhard von der Emde has also pursued. For these investigations, he again chose the elephantnose fish Gnathonemus petersii (Fig. 3.30). Gnathonemus continuously probes its environment with approximately 0.3 milliseconds (0.0003 s) long EODs. The organs and tissues of fish, small crustaceans, insect larvae, and aquatic plants act like small plate capacitors. Plate capacitors do not have a purely ohmic, but a capacitive resistance. If you send alternating current through a capacitive resistance, it not only changes the amplitude but also the shape (physically one speaks of phase) of electrical impulses (Fig. 3.31). Since the tissues of animate objects exhibit capacitive resistances in addition to ohmic resistances, they not only change the amplitude but also the shape of electrical signals. Behavioral experiments have shown that elephantnose fish can distinguish capacitive resistances from purely ohmic resistances even when both are chosen so that they change the amplitude of the EODs to the same extent.

3.8.4 The Electric Sense of the Elephant Nose Fish Could it be that weakly electric fish can measure (phase) shape changes of their EODs caused by a capacitive (animate) object (Fig. 3.31)? The shape change reaches its maximum at the EODs of Gnathonemus at a capacity of 1 nanofarad (one billionth of a farad) and then weakens again. Most organisms in the habitat of the elephant nose fish, such as aquatic plants, fish, and insect larvae, have capacities between one and fifty nanofarads, so they distort the EODs of Gnathonemus. Behavioral experiments have shown

84     H. Bleckmann

Inside positive

0°

1°

2°

15°

180°

0 Inside negative

Amplitude (mV)

Fig. 3.30  The elephantnose fish Gnathonemus petersii belongs to the family of Mormyridae and is only found in Africa. The German name refers to the trunk-like extension on the lower jaw. (From Bleckmann et al., 2004; with kind permission from Springer-Verlag GmbH. All Rights Reserved)

200µs

10°

Fig. 3.31  Electric organ discharge (EOD) of the elephantnose fish Gnathonemus petersii. Shown is the normal EOD (top left) as well as five artificially phase-shifted EODs. A phase shift of 180° (bottom right) means that the shape of the EOD is exactly opposite to the original signal. Phase shifts of 1° or 2° are so small that they are not visible to the naked eye. Nevertheless, they are recognized by Gnathonemus and used for object differentiation. (From Bleckmann et al., 2004; with kind permission from Springer-Verlag GmbH. All Rights Reserved)

that Gnathonemus recognizes these distortions and uses them to distinguish between animate (e.g., prey) and nonanimate objects (e.g., small stones). This raises the question of the physiological mechanism underlying this extraordinary performance. The tuberous receptor organs responsible for electrolocation in elephant nose fish are called Mormyromasts. Each Mormyromast contains A and B sensory cells (Fig. 3.32), which are

3  The Sensory World of Fish     85 Canal pore

Outer chamber

A-cell inner Chamber B-cell

A-fiber B-fiber A-fiber

Fig. 3.32  Mormyromast of Gnathonemus petersii. The Mormyromast consists of an outer chamber with a pore and an inner chamber, which is connected to the outer chamber via a pore. The outer chambercontains several A sensory cells, the inner chamber several B sensory cells. The sensory cells are each innervated by A and B nerve fibers. While the A sensory cells are insensitive to phase shifts, the B sensory cells respond to phase shifts with a decrease in latency and an increase in the number of nerve impulses even if the phase shift is only 1°. (From Bleckmann et al., 2004; with kind permission from Springer-Verlag GmbH. All Rights Reserved)

innervated by A and B sensory nerve fibers which end in different areas of the brain. Both types of fibers respond in the electrophysiological experiment to the EOD of Gnathonemus after a short latency (time between the start of the EOD and the first stimulus-related nerve impulse) with one or more nerve impulses. To investigate the response properties of the two fiber types, we (Gerhard von der Emde and I) played back to the elephant nose fish computer-stored recordings of their own EODs. While doing so we recorded the responses of A- and B nerve fibers. With the help of the computer, we were able to change the shape (phase) of the EODs so that they were similarly distorted as the EODs near capacitive objects. Our experiments revealed that the responses of A fibers to a normal (undistorted) EOD and a shape-changed (phaseshifted) EOD were nearly identical; shape changes or phase shifts were thus ignored by A sensory cells and thus by A fibers. B fibers or B sensory cells behaved differently: If the EOD was shape-changed (phase-shifted), they

86     H. Bleckmann

responded with a shorter latency and more nerve impulses. A phase shift of only 1°—which corresponds to a temporal signal change of less than one millionth of a second at an EOD duration of 0.3 ms—was sufficient to significantly change the responses (latency, number of nerve impulses) of B fibers. This solved the puzzle of how elephant nose fish can distinguish animate (capacitive) from non-animate (purely ohmic) objects: Apparently, there is a processing mechanism in their central nervous system that compares the number and latency of nerve impulses from A and B fibers originating from the same Mormyromast. If the B fibers of a Mormyromast respond with a shorter latency time and more nerve impulses than the A fibers, there is an animate object near the fish. If the A and B fibers respond with a similar number of nerve impulses and with similar latency, there is a purely ohmic (inanimate) object near the fish. With their electro-sensory system, weakly electric fish can thus not only perceive objects in the dark, but also recognize whether it is a prey animal or a non-living object. Since different prey animals have different complex resistances, Gnathonemus can probably also distinguish different prey animals with its electro-sensory system. When I once presented our experimental results in a lecture, an older gentleman approached me. He identified himself as a retired physics professor and was amazed at the abilities of Gnathonemus to recognize phase differences of 1°. “Technically, it is extremely difficult to measure such small phase differences.” The older gentleman then suggested a few clever experiments to us, all of which we carried out. Unfortunately, none of these experiments provided insights into the cellular mechanism that could explain the high phase sensitivity of the B cells of Gnathonemus.

3.8.5 Jamming Avoidance Behavior Franz Peter Möhres, who researched and taught at the University of Tübingen until the seventies of the last century, was the first to show that weakly electric fish also communicate electrically. Dominant animals, for example, increase their discharge frequency when another fish approaches them, while subordinate animals lower it or even temporarily stop their electric organ discharge completely. Both in pulse dischargers and wave dischargers, electrical communication and electrolocation are disrupted when two closely standing fish discharge their electric organs simultaneously. Pulse dischargers avoid this problem by always generating an EOD immediately after the discharge of a neighboring fish. Wave dischargers, due to their continuous signal generation, do not

3  The Sensory World of Fish     87

have this option. When a conspecific approaches them, their electrical signals interfere with their ability to locate and distinguish objects. To keep the interference as low as possible, the fish change their discharge frequency. The fish with the lower frequency lowers its frequency, the one with the higher frequency increases its frequency (jamming avoidance behavior). Since the fish never make a mistake in this regard, they obviously recognize the sign of the frequency difference (Box 7). Box 7 Jamming avoidance behavior of weakly electric fish. Behavioral experiments have shown that the weakly electric fish Eigenmannia sp. recognizes the sign of the frequency difference between its own EOD and the EOD of a neighbor. Eigenmannia lowers the EOD frequency if the discharge frequency of a neighbor is slightly higher than its own frequency and increases the frequency if the discharge frequency of a neighbor is slightly lower. This way, Eigenmannia avoids interferences that would impair the ability for electrolocation. Before we look for the physiological mechanism for recognizing the sign of the frequency difference, a detour into physics is necessary. If two sinusoidal signals of frequency F1 and F2 overlap, we get a signal with the beat frequency F1—F2 (Fig. 3.33). Experiments have shown that Eigenmannia obtains the information about the frequency difference by analyzing the beat signal. Eigenmannia or the brain of Eigenmannia does not use its own EOD frequency as a reference. Therefore, only the amplitude course and the phase relationship between heavily contaminated and less heavily contaminated skin areas are considered as information sources (due to the strong attenuation of electric fields, the skin areas closest to the interfering neighbor are most heavily contaminated). Eigenmannia determines the sign of the frequency difference by processing phase and amplitude changes that result from the superposition of two EODs. Eigenmannia has two types of tuberous organs respectively two types of afferents that innervate the tuberous organs. One type (P-afferent, P from Probability) responds proportionally to the amplitude of an electrical signal, this type maps the amplitude change in a beat signal. The second type (T-afferent, T from Time) responds to the zero crossings of each full sinusoidal oscillation with a nerve impulse, thus encoding stimulus phase. At the first processing station of the brain, the phase and amplitude information of the superimposed EODs still reach different neurons. At higher processing stations, the information is then interconnected and processed in such a way that higher order neurons emerge that clearly recognize the sign of the frequency difference (Fig. 3.34).

For intraspecific communication, the elephant nose fish Gnathonemus petersii possesses a third type of electroreceptor. This type is referred to as Knollenorgan and is a thousand times more sensitive than a tuberous organ. The high sensitivity of the Knollenorgans is necessary because electric fields in water are greatly attenuated with distance. Therefore, the EODs generated

88     H. Bleckmann 10 Hz

9 Hz

10 Hz + 9 Hz

Fig. 3.33  From top to bottom: signal of frequency F1 (10 Hz), F2 (9 Hz) and the beat signal F1 + F2 generated by adding the two signals

by a conspecific only reach the receiving fish with very small amplitudes at larger fish distances. The high sensitivity of the Knollenorgans ensures that Gnathonemus can still perceive conspecifics up to a distance of one meter. Knollenorgans show another peculiarity. They always respond with a constant latency and only one nerve impulse, regardless of the amplitude or shape of an EOD. The reason for this is that the receiving fish only wants to know if and when a conspecific has discharged its electric organ. Knollenorgans not only respond to the EODs of conspecifics (or another weakly electric fish) with a nerve impulse, but also to self-generated EODs. Since the fish brain “knows” when it has given a command to generate an EOD, this information is useless and would only demand unnecessary computational performance from the brain. To avoid this, the fish brain has found a clever way out during evolution. Every time the brain of Gnathonemus sends a neural command to the electric organ, the same neural command inhibits all brain cells that receive input from the Knollenorgans. This suppresses the responses of the Knollenorgans to their own EOD at the first processing stage in the brain. In addition to the mormyrids and gymnotids, some representatives of the gill bag catfish, spiny catfish, coral catfish, and true catfish also generate electric signals. However, the biological significance of these signals is still largely unknown.

3  The Sensory World of Fish     89

S1

F1

S1 + S2

F1 + F2 (F2 > F1)

T-afferent P-afferent 0

Interference cycle

2

Fig. 3.34  Example of a beat signal S1 + S2, which the electroreceptors (T- and P-afferents) of a fish (Eigenmannia) register, whose electrical discharges S1 (discharge frequency S1) interfere with the electrical discharge S2 of a fish nearby (discharge frequency F2). In the example shown, the frequency of F2 is greater than the frequency of F1. Only one interference cycle is shown. The interference pattern F1 + F2 is characterized by an amplitude modulation in the rhythm of the frequency difference F1 – F2 and a phase shift of the zero crossings compared to the pure S1 signal. The solid vertical lines show the zero crossings of S1, the red dashed lines the zero crossings of the beat signal S1 + S2. If F2 is greater than F1, the zero crossings of the signal S1 + S2 are delayed when the amplitude of the beat signal increases. If the amplitude of the beat signal decreases, the zero crossings of the signal S1 + S2 precede the phase of S1. If F2 is smaller than F1, the zero crossings of the beat signal precede the phase of S1 when the amplitude of the beat signal increases and are delayed when the amplitude of S1 decreases (not shown). This information is used by Eigenmannia to determine the sign of DF. The response of the P-afferent shows no phase coupling, but responds proportionally to the beat amplitude. The T-afferent responds phase-coupled at each zero crossing of the beat signal, regardless of the stimulus amplitude. Below: Each vertical thick black line corresponds to a nerve impulse (action potential). (From Heldmeyer et al., 2003. With kind permission from Springer-Verlag GmbH. All Rights Reserved)

3.9 The Magnetic Sense 3.9.1 The Discovery of the Magnetic Sense Have you ever gotten lost while hiking? You have a good map, but you no longer know exactly where you are. If you don’t have any distant landmarks (like the church tower of the nearby village) available, you have a problem at the latest now. The position of the sun could help in finding the direction or—if you are on a night hike—the North Star or the star pattern in the night sky. If the sky is covered, these sources of information also fail. As a navigation aid, you now theoretically still have the Earth’s magnetic field

90     H. Bleckmann

available, provided you have a compass with you. To determine the magnetic north direction, early seafarers used a magnet compass described by Petrus Peregrinus de Maricourt in 1269 (the compass reached Europe via the Arabs as early as 1190). A magnet compass reliably determines the north direction at any point on Earth. If you know this, all other cardinal directions can be derived from it and used for orientation. The fact that some animals have a magnetic sense was discovered in the mid-sixties of the last century by the Frankfurt zoologist Wolfgang Wiltschko. He found out that robins orient themselves with the help of the Earth’s magnetic field. Since this discovery, a magnetic sense has been demonstrated not only in many other bird species, but also in some amphibians, reptiles, mammals, insects, snails, crabs, and even bacteria. Many fish make long migrations in the open sea, e.g. to reach their spawning grounds. Since fish cannot (or can only poorly) see what is happening outside the water, the sun or the position of the North Star are only limitedly available as sources of information during the migration. How fish orient themselves therefore remained a mystery for a long time.

3.9.2 The Earth’s Magnetic Field The Earth is permanently surrounded by a magnetic field (see section 3.9.1). Therefore, biologists soon came up with the idea after the discovery that some birds have a magnetic sense, that some fish species could also use the Earth’s magnetic field for spatial orientation.

3.9.3 The Magnetic Sense of Bony Fish Like early seafarers, fish could use the Earth’s magnetic field for directional orientation, provided they have a direction-sensitive magnetic field sensor (today, humans use satellite-based positioning systems for this task). An initial indication that fish are actually capable of this was the observation that goldfish (Carassius auratus), eels (Anguilla anguilla), rainbow trout (Oncorhynchus mykiss), zebrafish (Danio rerio) and carp (Cyprinus caprio) often align themselves along magnetic field lines when at rest. Eels (Anguilla anguilla and A. rostrata ), which were caught during their migration and transferred to experimental tanks, preferred the direction in these tanks that corresponded to their natural migration direction at this time of year. When the direction of the magnetic field was artificially changed, they predictably changed their preferred direction. Sockeye salmon (Oncorhynchus nerka) are found on the

3  The Sensory World of Fish     91

Pacific coast of North America. They hatch in freshwater lakes, stay there for one to two years, and then migrate to the open sea. To spawn, they return to the waters where they hatched. During their migration, the salmon prefer either the direction to the open sea or the one from the sea back to their home waters. When the researchers rotated an artificially created magnetic field by 90°, the swimming direction of the salmon also changed by 90°. Similar results were obtained in experiments with European eels (Anguilla anguilla) and the larvae of the haddock (Melanogrammus aeglefinus). This shows that at least some fish or fish larvae can perceive the Earth’s magnetic field and use it for directional orientation. Further evidence followed. For example, my former research assistant Jens Hellinger was able to show in his doctoral thesis that the heart rate of conditioned trout (Oncorhynchus mykiss) decreases when he rotates an artificially created magnetic field by 90°. Geographers introduced spherical coordinates as early as the 15th century, which can be used to uniquely specify any location on the Earth’s surface. The geographical latitude is given from the equator to the north (or south) from 0° to 90°. The geographical longitude refers to an arbitrarily defined prime meridian, which runs through Greenwich (a district in southeast London). By definition, longitudes extend from 0° to 180° to the east and from 0° to 180° to the west. Latitude circles run parallel to the equator (more precisely, to the magnetic equator), longitude circles through the North and South Pole (Fig. 3.35b). The ability to determine the direction (polarity) of the Earth’s magnetic field is sufficient for mere directional orientation. However, for true navigation, a fish must also know its geographical position, only then can the direction and distance to a target be determined (The same applies to car drivers. If your navigation system is to calculate the way to a destination, it must know your location). The necessary information (at least in relation to the north-south direction) is the intensity and the inclination angle of the Earth’s magnetic field. Because not only the inclination angle, but also the magnetic field intensity changes with latitude. Thus, the Earth’s magnetic field at the equator is only about half as large as at the poles. To reach a distant target, another source of information is still missing. The line connecting the magnetic poles to the Earth’s axis is inclined by 11.5°. The result is that the magnetic poles are about 2000 km away from the geographical poles (Fig. 3.35a). The resulting deviation (declination) of the magnetic north from the geographical north direction depends on both longitude and latitude, so it is different for every place on Earth (Fig. 3.35b). Fish (rainbow trout) can perceive the direction, inclination angle, and intensity of the Earth’s magnetic field. If you know the inclination angle, declination angle,

92     H. Bleckmann a

North Pole magnetic south pole

magnetic equator W

O

geopgraphical equator

magnetic north pole South Pole

b

magnetic south pole

North Pole Declination angle α1

magnetic equator W

α2

geographical equator

O

Latitudes

Longitudes

South Pole

Fig. 3.35  a The Earth’s magnetic field. The magnetic field lines (arrows) emerge vertically from the Earth near the South Pole (at the magnetic North Pole) and re-enter the Earth vertically near the North Pole (at the magnetic South Pole). As you get closer to the equator, the angle (inclination angle) at which the magnetic field lines enter or exit the Earth’s surface decreases. Near the magnetic equator, the magnetic field lines run parallel to the Earth’s surface. The Earth can therefore also be considered a bar magnet. (After Hildebrandt et al., 2021; with kind permission from Springer-Verlag GmbH. All Rights Reserved). b An organism can only determine its exact position with the help of the Earth’s magnetic field if it knows both the inclination angle and the declination angle. The declination angle describes the angular deviation between the North Pole and the magnetic South Pole. Both angles change with increasing distance from the poles. The declination angle also changes with the longitude

3  The Sensory World of Fish     93

and magnetic field intensity, you can theoretically determine the coordinates for any geographical location (in reality, the matter is not quite so simple, as the Earth’s magnetic field has anomalies and fluctuations). Behavioral experiments have shown that yellowfin tuna (Thunnus albacares), rainbow trout (Oncorhynchus mykiss) and rockfish (Sebastes inermis) can perceive changes in the intensity of an artificial magnetic field. Trout can probably also determine the inclination angle. Whether fish can also determine the declination angle is not known.

3.9.4 The Magnetic Sense of Cartilaginous Fish Not only bony fish, but also cartilaginous fish orient themselves with the help of the Earth’s magnetic field. One of the first to investigate the magnetic sense of cartilaginous fish was the Dutch zoologist Ad Kalmijn. As early as 1974, he demonstrated that rays and sharks can perceive weak magnetic fields and use them for orientation. Kalmijn was also the first to propose a specific mechanism for magnetic field orientation (Box 8). Box 8 Mechanism of magnetic field orientation in rays and sharks. Do you still remember your physics lessons? There you probably learned that the movement of an electrical conductor in a magnetic field separates electrical charges. The size of the charge separation depends on the strength of the magnetic field and the speed and direction of the electrical conductor moving in the magnetic field. Rays and sharks, since their cells and tissues contain salt-rich, electrically conductive fluids, represent electrical conductors. When a shark or ray swims through the Earth’s magnetic field, electromotive forces are induced—as in any other electrical conductor. These forces are strongest when the shark (the electrical conductor) moves perpendicular to the horizontal component of the Earth’s magnetic field. With the same swimming direction, the forces also increase with increasing swimming speed. If a shark, for example, swims east through the Earth’s magnetic field, current flows from its belly to its back (Fig. 3.36). The resulting voltage gradients are 0.1 μV per cm at a swimming speed of 1 cm per s, so they can still be perceived by sharks and rays (see Section 3.8). If a shark swims west, the current flows in the opposite direction. This reversal of the current direction and the dependence of the current strength on the swimming direction can probably be used by sharks and rays to maintain their course while swimming or to change it deliberately. If sharks are passively transported by a sea current, the same direction-dependent voltage gradients occur as with active movement. The final proof that the mechanism proposed by Kalmijn is used by cartilaginous fish for magnetic field perception for orientation is still pending. Recent findings suggest that another (additional?) mechanism could explain the magnetic sense of rays and sharks. This mechanism is supposed to be based

94     H. Bleckmann horizontal component of the earth's magnetic field

Induced current

shark swimming to the east Fig. 3.36  Shark in the Earth’s magnetic field. In the example shown, the shark is swimming east. The shark’s own movement in the Earth’s magnetic field induces a current, the direction and strength of which depend on the shark’s swimming direction and speed. Theoretically, sharks can measure this current with their electroreceptors and use it for spatial orientation. (After Kalmijn, 1974; with kind permission from Springer Verlag. All Rights Reserved) on the lateral head movements of swimming sharks and rays. These movements also create weak electrical fields in the Earth’s magnetic field. Certain parameters of these fields are independent of the strength of the Earth’s magnetic field or the swimming speed of the sharks and rays and depend solely on the swimming direction. It is therefore now suspected that rays and sharks use this mechanism for magnetic field orientation.

Laboratory studies have confirmed that rays and sharks can use magnetic fields for orientation. Stingrays in a two-choice test seek out the hiding place whose entrance has a certain direction in relation to an artificial magnetic field. Sandbar sharks (Carcharhinus plumbeus) could be conditioned to visit a certain place in the test basin after switching on an artificial magnetic field stimulus. These experiments suggest that the sharks perceived the magnetic field stimuli not with their electroreceptors, but with “real” magnetic field receptors. Sharks (e.g., the blue shark Prionace glauca and the hammerhead shark Sphyrna lewini ) often swim straight ahead over long distances both during day and night. The same has been observed in eagle rays (Myliobatis californica). Since the fish had no optical landmarks available, researchers speculated that they oriented themselves with the help of the Earth’s magnetic field. Since the electro-sensory system of electro-sensitive freshwater fish is much less sensitive than that of rays and sharks (see above), they cannot sense the Earth’s magnetic field with their electroreceptors. Therefore, there must be a special sensory organ for perceiving the Earth’s magnetic field, at least in bony fish.

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3.9.5 Magnetic Field Receptors The search for magnetic field receptors has proven to be extraordinarily difficult in all animal groups. Since the magnetic field lines penetrate the body of an animal unhindered, sensory organs for the perception of magnetic fields can be small and in principle arranged anywhere in the head or body. This is probably the reason why it has been so difficult to definitively identify magnetic field receptors as such. To this day, it is not known with certainty—perhaps with the exception of the electro-sensory mechanism for magnetic field perception proposed by Kalmijn for cartilaginous fish—what magnetic field receptors look like, where they are located in the body, and how they function. If one disregards magnetic field perception by induction, there should be particles in an organism which align themselves in the Earth’s magnetic field similar to a compass needle. The Italian physician and cell researcher Salvatore Bellini observed as early as the beginning of the sixties of the last century that some bacteria can orient themselves with the help of the Earth’s magnetic field. Ten years later, researchers showed that magnetosensitive bacteria have inclusions of magnetite (iron(III) oxide). The water-dwelling bacterium Magnetospirillum gryphiswaldense has tiny cell inclusions of magnetite, which it uses to align itself along the Earth’s magnetic field lines like a compass needle. This enables swimming movements along the field lines and thus movements along nutrient and oxygen gradients. As recent investigations show, the formation of magnetite in magnetosensitive bacteria is carried out with a genetically controlled complex process involving more than 30 proteins. Magnetite inclusions are also found in the tissue of many fish (as well as other animals). It is conceivable that magnetite particles inside nerve cells are passively aligned in the Earth’s magnetic field. If the magnetite particles were connected to mechanosensitive ion channels, the idea is that they could influence the opening state of these channels depending on the intensity and/or direction of the Earth’s magnetic field. This is supposed to lead to electrical cell responses that are transmitted to the brain. Magnetite particles have been found, among other places, in the olfactory mucosa of trout. Therefore, it is suspected that magnetic field receptors are located in the olfactory mucosa of trout. This assumption is supported by physiological experiments. The olfactory mucosa of trout mainly contains the endings of olfactory nerve fibers. As expected these respond to odor stimuli. In addition to the olfactory nerve fibers, fibers of the facial nerve (the trigeminal system) also extend to the olfactory mucosa in trout (and other fish). The New Zealand researcher John Montgomery showed that these

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nerve fibers respond to changes in intensity of an artificially generated magnetic field. When the direction of the magnetic field changed, a neuronal response was absent. It therefore seems to be a system with which trout can measure the intensity of the Earth’s magnetic field. Researchers also suspect that the equilibrium organs of the inner ear are involved in magnetic field perception. Another possible mechanism for the perception of the Earth’s magnetic field is based on molecules that change their state depending on the direction of the Earth’s magnetic field. This mechanism depends on the wavelength of light. Researchers came up with this idea because birds can only orient themselves with the help of the Earth’s magnetic field under shortwave light. The molecules involved include cryptochromes, which have been found in the eyes of birds, newts, and insects. However, it is still unclear whether cryptochromes are actually involved in magnetic field perception. It is also unclear whether cryptochromes are important for the magnetic sense of fish. Light-dependent magnetic field orientation has not yet been demonstrated in fish.

3.10 The Sense of Pain 3.10.1 Do Fish Feel Pain? According to the WWF (World Wildlife Found), 80 million tons of fish are caught in the world’s oceans each year. Assuming an average fish weight of five kilograms, that’s 16 billion fish per year. These high catch numbers have led to a worldwide decline in fish stocks of about 50% between 1970 and 2010. When caught with nets, the fish are slowly crushed to death. If they escape this fate, they suffocate at the latest after the nets are hauled on board the fishing vessels. Often they are gutted and cut up while still alive. Half-dead or dead bycatch, about 40% of the annual catch, is dumped back into the sea. Millions of fish die every day on longlines up to 130 km long and equipped with up to 20,000 bait hooks, but unfortunately also many seabirds, including many gulls and albatrosses. In the global trade of aquarium fish, numerous coral reef fish, often poisoned with cyanide for the catch, die. All these brutal fishing methods are justified with the claim that fish neither feel fear nor pain, thus are not capable of suffering.

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This is justified by the assumption that a conscious perception of pain requires an intact cerebral cortex, which is only present in mammals. Since fish do not have a cerebral cortex, so the argument goes, they could not have either fear or a conscious perception of pain. However, some arguments suggest that fish, like many other animals, do feel fear and pain. Feelings like fear and pain give animals the opportunity to react early to potentially harmful environmental stimuli or to avoid places where they have been hurt in the past. The sense of pain thus has an important protective function, which is of great importance for the survival of animals. Worldwide, there are a few hundred people without the ability to feel pain. These people cannot avoid damaging situations sufficiently, therefore live in constant danger and have a significantly higher risk of death. All this makes it likely that fish also have a sense of pain. Seventeen out of eighteen criteria for pain perception in mammals are met by fish. That many fish can see excellently is evident even to the layman at first glance due to their often large eyes. The matter becomes more difficult when it comes to hearing and smell, as fish have neither pinnae nor a middle ear, a cochlea, or a nose. The question of whether fish have a sense of pain is even more difficult. For many decades, fishermen, fish farmers, anglers, and ichthyologists have denied this. This is understandable, as most fish can neither grimace in pain nor can they scream, groan, or whimper loudly.

3.10.2 Unconscious Pain Perception In the case of pain perception, one must distinguish between an unconscious reaction to harmful stimuli (in this case, we speak of nociception) and a conscious perception of pain. In nociception, the harmful stimulus leads to a reflex-like defensive reaction without conscious pain perception. Our patellar reflex is a good example. When the doctor taps on the patellar tendon below the kneecap with a small hammer, the lower leg automatically (reflexively) moves upwards. Both nociception and conscious pain perception require an animal to have sensory organs that selectively respond to harmful stimuli (e.g., temperature stimuli above 45 °C, mechanical and chemical stimuli that damage tissue). In mammals, especially in humans, the pain system is well studied. Prerequisite for pain perception are nociceptive sensory cells. These are specialized nerve cells of the somatosensory system, which occur both in the skin and—with the exception of the brain and spinal cord—in the internal organs (muscles, heart, viscera, periosteum). The pain fibers of the face reach

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the brain via the facial nerve (trigeminal nerve), all other pain fibers via special pain pathways of the spinal cord. With fibers of the trigeminal nerve and the pain pathways of the spinal cord, pain information in mammals is forwarded to the diencephalon and from there to the forebrain or cerebrum. In the free nerve endings belonging to the mammalian pain system, a distinction is made between thin C nerve fibers and the slightly thicker Aδ nerve fibers. C fibers conduct nerve impulses at a speed of 0.5 to 2 m per s. Aδ fibers at a speed of 10 to 30 m per s. Experiments have shown that the fast-conducting Aδ fibers convey an early, stabbing first pain in us. The Aδ fibers respond selectively either to strong mechanical (crushing, stabbing) or to thermal stimuli (heat, cold). If fish have a conscious perception of pain, they would have to have nociceptive nerve fibers (pain fibers). Anatomical and physiological studies have shown that this is clearly the case: bony fish have both C and Aδ nerve fibers. While in mammals the number of C fibers dominates, bony fish (trout) have significantly more Aδ fibers. In cartilaginous fish (rays and sharks), only Aδ fibers have been detected so far. Both the C fibers and the Aδ fibers of the bony fish respond to damaging mechanical stimuli, damaging temperature stimuli (>40 °C) and damaging chemical stimuli (e.g., acetic acid). Thus, the prerequisites for nociception in fish are clearly given.

3.10.3 Conscious Pain Perception In contrast to nociception, pain is a subjective emotional sensory perception. According to the definition of the International Association for the Study of Pain (IASP), pain is “an unpleasant sensory and emotional experience associated with actual or potential tissue damage, or described in terms of such damage”. In mammals (including humans), a conscious perception of pain is tied to certain areas of the cerebrum (the neocortex). Mammals from which the neocortex has been surgically removed no longer feel pain, but still react reflexively to harmful stimuli (e.g., by withdrawing a limb when touching a hot object). Fish have a forebrain, but no cortex (see further below), therefore scientists long assumed that fish do not have a conscious perception of pain. This indirect evidence is not very convincing. Without a cerebral cortex (more precisely without a primary visual cortex), a human (a color-capable mammal) cannot perceive colors. Because color perception is predominantly generated in the visual cortex in mammals (physically there are no colors, but only electromagnetic radiation of different wavelengths. The color sensation is created by the brain). Although fish do not have a

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visual cortex, many species, as described above, have excellent color vision. The color perception in goldfish is even better developed than in humans. The color perception in goldfish (and other color-capable fish) must therefore occur in other brain areas than in mammals. In human subjects, it is easy to determine through questioning whether they have a conscious perception of pain. Many mammals are known to make pain-related vocalizations (e.g., screaming, groaning, whimpering). An increased heart rate and respiratory rate also indicate that a human or an animal is consciously experiencing pain. In the case of severe pain, mammals not only refuse to eat, but also avoid the place where the pain was first triggered (this is known from one’s own dog, who refuses to enter the vet’s office again after a bad experience). If fish are exposed to a harmful stimulus (e.g., a weak acid or bee venom), their respiratory rate or the frequency of their gill cover movement increases. In addition, fish (trout) do not eat for several hours. The trout also rub the skin area that came into contact with the acid or bee venom (and therefore hurts?) against objects up to 45 times per minute, a behavior that can last up to one and a half hours. If trout are given a painkiller, this behavior is significantly reduced. If they are given a substance that counteracts the effect of painkillers in mammals, the behavior reoccurs. Zebrafish larvae continuously swim around in search of food. If fiveday-old zebrafish larvae are transferred to water containing different concentrations of diluted acetic acid, they increase their swimming speed. The swimming speed increases significantly with increasing concentration of the diluted acetic acid (0.01%, 0.1%, and 0.25%). The larvae apparently try to escape from the unpleasant location. If the larvae are treated with painkillers (e.g., aspirin, morphine, lidocaine), they return to their normal (slow) swimming speed. These behavioral responses suggest that fish have a conscious perception of pain. If this is the case, the question remains as to where in the fish’s brain the circuits for pain perception are located. By recording brain waves (electrocardiograms), it has been found that the pain information mediated by C-fibers and A-fibers in goldfish and Atlantic salmon Salmo salar—just like in mammals—reaches the forebrain. In trout, brain waves mediated by pain stimuli have also been detected in the midbrain and cerebellum. Which brain areas are active when a sensory system is stimulated can also be investigated with molecular methods. In nerve cells activated by sensory stimuli, certain genes are read off more frequently. This can be made visible and thus it can be determined which nerve cells of the brain were activated by repeated pain stimuli. Using this method, scientists have shown, among

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other things, that damaging stimuli in fish activate nerve cells in similar and in some cases even the same brain areas as in mammals. Further findings suggest that the pain systems of bony fish are organized similarly to those of mammals. The mammalian brain can regulate pain sensitivity down with endogenous painkillers (opioids). This is important in situations where premature surrender of a fight due to injury and the resulting severe pain would lead to certain death. People attacked by bears, lions, or tigers have consistently reported that they felt no pain either during or immediately after the attack. This is despite the fact that in one case a grizzly bear bit out an angler’s eye and in another case a black bear bit off both arms of a geologist working in Alaska. Temporary complete insensitivity to pain is also known from soldiers wounded in combat. In certain areas of the mammalian brain are nerve cells that synthesize and release the opioids necessary for pain shutdown. In mammals, these are enkephalin and endorphin. Both substances have also been found in the brains of bony fish. In order for opioids to be able to downregulate the activity of nerve cells, these must have opioid receptors. Opioid receptors are proteins anchored in the cell membrane to which opioids can dock. Opioid receptors have been detected in the brains of goldfish, catfish, lungfish, zebrafish, and trout. This also suggests that fish have a conscious perception of pain.

3.11 Why So Many Senses? So far, we have treated the various sensory systems of fish separately. In reality, fish and other animals almost always use their multiple senses simultaneously or in a specific temporal order for decision-making. This reduces the probability of error during each individual action phase. If a fish is unsure whether what it sees is a camouflaged, dangerous predator, the information conveyed by other senses (e.g., the sense of smell) can be useful in decision-making. The importance of different senses for the behavior of fish has been studied by Gardiner, Atema, and colleagues on shark species that differ significantly in their ecology and lifestyle. The potentially dangerous to humans, up to 2.5 m long blacktip shark (Carcharhinus limbatus) lives in tropical and subtropical seas up to a depth of 30 m, but also occurs in the estuaries of large rivers. The diet of this mostly restless swimming shark consists mainly of fish, but occasionally also of clams or snails. The up to 3 m long Atlantic nurse shark (Ginglymostoma cirratum) is nocturnal, sluggish, and bottom-dwelling. Its preferred prey includes bony fish, but also sea urchins, crabs, and squids. When hunting, nurse sharks show the typical

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behavior of a suction feeder: they approach their prey to within a few centimeters and then suck in the prey by quickly opening their mouths. The up to 1.5 m large bonnethead shark (Sphyrna tiburo) constantly swims around to take in enough oxygen through its gills. It feeds mainly on crabs, small fish, and snails. The bonnethead shark is the only shark known to also eat plants. Seagrass can make up more than 60% of this shark’s diet. The prey-catching behavior of the three mentioned shark species can be divided into different phases. In the first phase, the sharks perceive a stimulus and evaluate it in terms of its significance. If the stimulus signals prey, the shark is initially alerted. In the second phase, the shark approaches the prey to a short distance. In the third phase, it coordinates its attack movements, attacks the prey, kills it, and eats it. Several sensory systems are involved in the execution of this sequence of actions in all three shark species. Potential prey constantly emit unintentional chemical, optical, acoustic, hydrodynamic, and/or electrical signals that spread at different speeds and distances in the water. In clear water, diurnal sharks can see a prey from a great distance. Both in the open sea and in coastal waters, there are water currents that transport scents over long distances. If a shark crosses a current with scents, it can smell a prey long before it sees it. The water movements emanating from a prey (e.g., those caused by gill movements) are only perceptible at close range (up to approx. 20 cm), the same applies to the electric field that surrounds each prey. The different sensory systems of sharks therefore have different working ranges. This makes it understandable why sharks predominantly use the sensory modality that provides the most reliable information in a certain distance range to the prey. Once the mentioned shark species have smelled a prey, they swim against the current until they reach the prey. To not lose the scent trail while swimming, sharks— similar to a tracking dog—mainly use their sense of smell. In addition, they can sense the current fluctuations usually associated with a scent trail with their lateral line and use it to follow the scent trail. If a shark moves close to the ground, it can also recognize the direction in which it must swim to reach the prey via the direction in which the current drifts it. If the shark loses the scent trail, it turns around and initially swims a bit downstream. After that, it tries again to pick up the scent trail and follow it. As the shark approaches a prey, the scent stimuli become increasingly intense. Only when the shark has reached the immediate vicinity of the prey can it perceive the water movements caused by the prey with the help of the lateral line. Blacktip sharks and hammerhead sharks do not need scent stimuli to trigger the prey-catching action. With good visibility, these sharks attack a prey from any angle and distance, regardless of water currents. In nurse sharks,

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scent stimuli are indispensable. If their sense of smell is blocked, prey-catching behavior can no longer be triggered, even if the prey is directly in front of the shark. Just before the final bite, all three shark species determine the exact position of their prey with the help of hydrodynamic, electrical, and tactile information. If these three sensory modalities are switched off, any prey-catching action triggered by chemical and/or optical signals is aborted in the final phase. The use of multiple sensory systems in prey-catching leads to shorter reaction times, higher sensitivity, greater spatial and temporal resolution, and an improvement in the signal-to-noise ratio. Sharks also use their acoustic system for prey-catching, but the influence of the sense of hearing was not investigated in the study by Gardiner and Atema due to experimental difficulties. Another example is intended to demonstrate the advantage of multimodal information processing. Weakly electric fish can see, hear, smell, and taste, as well as perceive self-generated and externally generated electric fields. The weakly electric fish Gnatonemus petersii is nocturnal and feeds on insect larvae. In principle, it can perceive and locate these using its ampullary and tuberous electroreceptors, its eyes, the lateral line system, and its sense of smell. Behavioral experiments have shown that Gnathonemus primarily finds insect larvae in the dark through active electrolocation. If you switch off the high-frequency electrical sense, the fish still find the insect larvae, but they now need more time. In the light, Gnathonemus primarily uses its sense of sight to locate prey. With an intact sense of smell, the time Gnathonemus needs to track down an insect larva is shortened. If an insect larva moves, it is also perceived with the lateral line system. Summary This chapter describes the sensory systems of fish. These systems include not only the sense of smell, taste, and sight, but also the lateral line system, the sense of touch, balance, hearing, the electric sense, as well as the magnetic sense and the sense of pain. In addition to general information on the structure of these sensory systems, the chapter provides information about the behavioral performances that fish achieve with their various senses.

References Bleckmann, H. (2007). The lateral line system of fish. In T. J. Hara & B. S. Zielinski (Eds.), Sensory systems neuroscience, vol 25. Fish physiology (pp. 411– 453). Elsevier Inc.

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Bleckmann, H., Schmitz, H., & von der Emde, G. (2004). Nature as model for technical sensors. Journal of Comparative Physiology A, 190, 971–981. Branson, E. J. (2008). Fish welfare. Blackwell Publishing Ltd. Brown, G. E., & Brown, J. A. (1993). Social dynamics in salmonid fishes: Do kin make better neighbours? Animal Behaviour, 45, 863–871. Brown, C., Laland, K., & Krause, J. (Eds.). (2006). Fish cognition and behavior. Fish and aquatic resources series (vol 11). Blackwell Publishing. Bullock, T. H., & Heiligenberg, W. (1986). Electroreception. Wiley. Carr, C. E., & Maler, L. (1986). Electroreception in gymnotiform fish. Wiley. Coombs, S., Bleckmann, H., Fay, R. R., & Popper, A. N. (2014). The lateral line system. Springer. Costa, F. V., Rosa, L. V., Quadros, V. A., de Abreu, MS, et al. (2021). The use of zebrafish as a non-traditional model organism in translational pain research: The knowns and the unknowns. Current Neuropharmacology 19. https://doi.org/10.2 174/1570159x19666210311104408. Fay, R. R., & Popper, A. N. (1999). Comparative hearing: Fish and amphibians. Springer. Fischer, E. A. (1980). The relationship between mating system and simultaneous hermaphroditism in the coral reef fish, Hypoplectrus nigricans (Serranidae). Animal Behaviour, 28, 620–633. Flock, A. (1965). The microphonic potential of the lateral line canal organ. Acta Oto-Laryngol 59 (Sup 199), 48–86. Francke, M., Kreysing, M., Mack, A., Engelmann, J., Karl, A., Makarov, F., Guck, J., Kolle, M., Wolburg, H., Pusch, R., von der Emde, G., Schuster, S., Wagner, H. J., & Reichenbach, A. (2013). Grouped retinae and tapetal cups in some teleostian fish: Occurrence, structure, and function. Progress in Retinal and Eye Research, 38, 1–27. Gardiner, J. M., Atema, J., Hueter, R. E., & Motta, P. J. (2014). Multisensory integration and behavioral plasticity in sharks from different ecological niches. PLOS ONE, 9(4), 1–13. Hardy, A. R., & Hale, M. E. (2020). Sensing the structural characteristics of surfaces: Texture encoding by a bottom-dwelling fish. Journal of Experimental Biology, 223. https://doi.org/10.1242/jeb.227280. Heiligenberg, W. (1991). Neural nets in electric fish. MIT Press. Herzog, H. (2020). Form and function in the peripheral lateral line morphology: Implications for adaptedness to hydrodynamic environments. In H. Bleckmann & B. Fritzsch (Eds.), The senses: A comprehensive reference (Vol. 7, pp. 47–65). Elsevier. Hildebrand, J.-P., Bleckmann, H., & Homberg, U. (2021). Penzlin – Lehrbuch der Tierphysiologie. Springer Spektrum. Houde, A. E. (1997). Sex, color, and mate choice in guppies. Princeton University Press.

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Kalmijn, A. J. (1974). The detection of electric fields from inanimate and animate sources other than electric organs. In A. Fessard (Ed.), Handbook of Sensory Physiology. Vol. III/3 Electroreceptors and other specialized receptors in lower vertebrates (Vol. 5, 1. edn., pp. 147–200). Springer. Kasumyan, A. O. (2011). Tactile reception and behavior of fish. Journal of Ichthyology, 51, 1035–1103. Klein, A., Münz, H., & Bleckmann, H. (2013). The functional significance of lateral line canal morphology. Journal of Comparative Physiology A, 199, 735–750. Liao, J. C. (2007). A review of fish swimming mechanics and behaviour in altered flows. Philosophical Transactions of the Royal Society, 362, 1973–1993. McHenry, M. J., & Liao, J. C. (2013). The hydrodynamics of flow stimuli. In S. Coombs, H. Bleckmann, A. N. Popper, & R. R. Fay (Eds.), The lateral line system. Springer Handbook of Auditory Research (pp. 73–98). Springer Science+Business Media. Nyman, C., Fischer, S., Aubin-Horth, N., & Taborsky, B. (2018). Evolutionary conserved neural signature of early life stress affects animal social competence. Proceedings of the Royal Society B: Biological Sciences, 285. https://doi. org/10.1098/rspb.2017.2344. Pitcher, T. J. (1993). Behaviour of teleost fishes. Chapman & Hall. Salwiczek, L. H., Prétôt, L., Demarta, L., Darby Proctor, D., Jennifer Essler, J., Ana, I., Pinto, A. I., Sharon Wismer, S., Stoinski, T., Sarah, F., Brosnan, S. F., & Bshary, R. (2012). Adult cleaner wrasse outperform capuchin monkeys, chimpanzees and orang-utans in a complex foraging task derived from cleaner – client reef fish cooperation. PlOS ONE, 7(11), E49068 (49010.41371/journal. pone.0049068). Sneddon, L. U. (2009). Pain reception in fish: Indicators and endpoints. ILAR Journal, 38, 338–342 Snedden, L. U., Braithwaite, V. A., & Gentle, M. J. (2003). Do fish have nociceptors: Evidence for the evolution of a vertebrate sensory system. Proceedings of the Royal Society B: Biological Sciences, 270, 1115–1121. Soares, M. C. (2017). The neurobiology of mutalistic behavior: The cleanerfish swims into the spotlight. Frontiers in Behavioral Neuroscience, 11, 1–12. https:// doi.org/10.3389/fnbeh.2017.00191. Stacho, M., Herold, C., Rook, N., Wagner, H., Axer, M., Amunts, K., & Güntürkün, O. (2020). A cortex-like canonical circuit in the avian forebrain. Science, 369(eabc5534), 1–12. Taborsky, M. (1984). Broodcare helpers in the cichlid fish Lamprologus brichardi: Their costs and benefits. Animal Behavior, 32, 1236–1252. von der Emde, G., & Bleckmann, H. (1992). Differential responses of two types of electroreceptive afferents to signal distortions may permit capacitance measurement in a weakly electric fish, Gnathonemus petersii. Journal of Comparative Physiology A, 171, 683–694.

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Webb, J. F., Popper, A. N., & Fay, R. R. (2008). Fish bioacoustics. Springer handbook of auditory research. Springer. Witte, K., & Ueding, K. (2003). Sailfin molly females (Poecilia latipinna ) copy the rejection of a male. Behavioral Ecology, 14(3), 389–395.

4 The Central Nervous System of Fish

4.1 Structure of the Brain If you have read this book up to this point, I can confidently recommend the next chapter to you. It deals with the central nervous system (brain) of fish (the spinal cord also belongs to the central nervous system, but is not further discussed in this book). If you dissect the brain from the skull of a dead fish, you only see the outer form, not the interior of the brain. If you want to learn more about the structure of a brain, you have to cut it into thin slices using special devices (microtomes). Microtomes work similarly to a bread or sausage slicing machine, but the slices are only a few thousandths of a millimeter thick. Microtome slices look—like the entire brain—uniformly light and quite homogeneous, individual nerve cells (neurons) cannot be recognized even under a high-resolution microscope. The structure of a brain only becomes apparent to the researcher when he makes individual nerve cells and connections between the nerve cells visible under the light microscope using special staining methods. Almost every nerve cell consists of a cell body (soma), a usually highly branched tree-like region (dendrites) and one or more long extensions (neurites or axons) that end in a terminal button (axonal bouton) (Fig. 4.1). It is estimated that the human brain contains about 86 billion nerve cells. Fish brains have significantly fewer nerve cells, not least because of their small size. Each of these cells makes contact with up to several thousand (in some brain areas up to 100,000) other nerve cells using axons and dendrites. An excited nerve cell releases a chemical messenger (neurotransmitter) at the © The Author(s), under exclusive license to Springer-Verlag GmbH, DE, part of Springer Nature 2024 H. Bleckmann, Stupid as a Fish?, https://doi.org/10.1007/978-3-662-68376-7_4

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Receptors

Dendrites End button Axon Cell body Axon

End button

Fig. 4.1  Nerve cells with cell body (soma), dendrite and axon. At the end of each axon is a synaptic terminal button (axonal bouton), through which a nerve cell makes contact with a downstream nerve cell. In the synaptic terminal button are vesicles filled with messengers (neurotransmitters) (see detail top right). When the neuron fires, its vesicles release a neurotransmitter that binds to special receptors (receptor proteins) in the membrane of the downstream (postsynaptic) nerve cell. If the neurotransmitter release is high enough, the postsynaptic nerve cell then also generates nerve impulses, which are transmitted to neighboring nerve cells via axons. In addition to excitatory synapses, there are also inhibitory synapses, which reduce the neuronal activity of postsynaptic nerve cells.

end of its axons (at the axonal bouton) that binds to specific receptor molecules (transmembrane proteins) of the downstream nerve cells. As a result, these nerve cells are excited or inhibited depending on the receptor molecule. Places where nerve cells transmit signals using chemical messengers are called chemical synapses. In addition to chemical synapses, there are also electrical synapses. These transmit the electrical excitation without chemical messengers through close cell contacts directly from nerve cell to nerve cell. Brains therefore represent extremely complex three-dimensional neuronal networks in which numerous nerve cells are active at any moment. Although the nervous systems of different animals can be very different at the macroscopic level (e.g., the brain of a fly and that of an elephant), they have hardly experienced any qualitative changes in the course of their evolution (Box 8). Box 8 Central Nervous Systems. Central nervous systems, from coelenterates (jellyfish and medusae) to apes and humans, have undergone little qualitative changes in the course of their evolution. Thus, the basic building blocks of central

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nervous systems (nerve cells, receptor proteins, neurotransmitters, etc.) and the physiological mechanisms of information transmission (synaptic transmission, excitation conduction, circuit principles, information storage) in the fish brain are the same as in the brains of worms, annelids, insects, snails, clams, sea urchins, starfish, and mammals. What is observed are quantitative changes, as there are increasingly more of the basic building blocks of the nervous system in animals with increasing higher development. An example from technology should illustrate this principle. From the single-cylinder to the twelve-cylinder gasoline or diesel engine, many components (intake and exhaust valves, piston rings, cylinders, camshaft, connecting rods, spark plugs) are always the same, but the number of components (e.g., the number of cylinders) is larger in larger (more sophisticated) engines. It doesn’t matter whether it’s the engine of a moped, car, diesel locomotive, a diesel-powered cruise ship, or a propeller plane. Variations occur, for example, a two-stroke engine has neither intake nor exhaust valves, and a diesel engine, unlike a gasoline engine, does not need spark plugs. A similar construction principle also applies to central nervous systems. All components “invented” at the beginning of evolution remain largely unchanged, but the number and linkage of components increase with the increasing higher development of the central nervous systems. Thus, in fish and amphibians, the path from the sensory centers to the movement centers (motor centers) is short. In all other vertebrates, especially mammals, the motor centers of the forebrain no longer receive direct input from the sensory centers, but from interposed components, which are referred to as association fields. In these fields, already processed sensory information is processed again, communicated with each other, and only then forwarded to downstream motor centers.

The cognitive abilities of an animal depend solely on the neuronal circuits in its brain. Originally, it was suspected that large brains are more powerful than small brains. This has only been partially confirmed, as a clear correlation between brain size and the cognitive abilities of an animal has not yet been found. This probably has several reasons. Nerve cells can, for example, be small and densely packed or large and widely dispersed in the brain. Despite possible crucial differences in the fine structure of brains, important information is obtained when the brain weight of different animal species is plotted against their body weight (Fig. 4.2). First, it is noticeable that the values of a certain animal group (birds, mammals, reptiles, amphibians, and fish) lie within a polygon. Furthermore, it is noticeable that the polygons show increasingly higher values on average with increasing body weight. This means that in all animal groups the brain weight increases with body weight. However, in all groups, the brain weight increases proportionally slower than the body weight, and the values vary considerably in all animal groups with the same body weight. Fig. 4.2 also shows that the polygons of mammals and birds lie above the polygons for amphibians and

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1000

Brain weight (g)

100

Elephant nose fish

10 1 Mammals Sharks and rays Birds Reptiles Amphibians Teleosts

0,1 0,01

0,001

0,01

0,1 1 10 Body weight (kg)

100

1000

Fig. 4.2  Brain weight as a function of body weight, shown on a logarithmic scale for mammals, birds, reptiles, amphibians, and fish. (Adapted from Allmann 2000; with kind permission from Scientific American Library. All Rights Reserved)

reptiles. At the same body weight, birds and mammals therefore have larger brains on average than amphibians and reptiles. The polygons of the fish (teleosts and cartilaginous fish) overlap with those of the birds and mammals. Large brains are therefore also found in fish, especially in eagle rays and some shark species. Large brains in fish have obviously evolved independently of the large brains of mammals and birds in the course of evolution. An example of a particularly large brain (in relation to body weight) is the elephant nose fish (Fig. 3.30). Its brain has the same relative size as the brain of a mammal of the same weight (Fig. 4.2). The brain of vertebrates is divided into five sections. Starting with the spinal cord, these sections are referred to as the medulla, hindbrain (metencephalon, cerebellum), midbrain, diencephalon, and forebrain (also known as the cerebrum or telencephalon) (Fig. 4.3, above). The cerebellum, which lies on top of the hindbrain, is also part of the vertebrate brain. In mammals, especially in apes, a large part of the forebrain consists of the cerebral cortex (Cortex). Fish, like all vertebrates, have a forebrain, but they lack a cortex. Nerve cells are not evenly distributed in the brain. There are regions

4  The Central Nervous System of Fish     111 a Cerebellum

Midbrain Medulla oblongata

Telencephalon

Metencephalon

Dienephalon

b

Fig. 4.3  a Brain of the goldfish Carassius auratus in side view. b Outline of the brain with nine hypothetical nuclei and their hypothetical connections. Numerous nerve cell bodies are located in each nucleus (only one, three or four nerve cell bodies are shown in each case). The nerve cells of a nucleus send their information to partly distant nuclei  via axons. Arrows indicate the direction of information transfer. Sensory nuclei receive input from the sensory organs, motor ones mainly from the sensory nuclei. Motor nuclei send their information to the muscles using motor nerve fibers (motor neurons)

with dense accumulations of cell bodies and those with few or no cell bodies (Fig. 4.4). A region with a dense accumulation of cell bodies is referred to by neuroanatomists as a nucleus (Fig. 4.4b). A nucleus can contain only a few, but also many thousand cell bodies. The axons of the nerve cells run between the nuclear areas. They connect the various nuclei with each other. Brains therefore consist of a multitude of differently sized nuclei with their input

112     H. Bleckmann

Fig. 4.4  Cross-section through the midbrain of a fish (only one hemisphere is shown). A nucleus that is clearly visible in the cross-section is shown enlarged on the right. (Adapted from Saskia and Schluessel, with kind permission of the authors)

and output connections. All nuclei  are directly or indirectly connected with each other (Fig. 4.4b). In addition to nerve cells, central nervous systems also contain numerous glial cells, which are also important for information processing. One task of comparative neuroanatomy is to describe the size and position of the nuclei in different vertebrate species—including their neuronal connections—and to assign them functionally or structurally meaningful names. In addition, comparative neuroanatomists want to know when and why a particular nucleus (or a particular connection between two, three or more nuclei) arose during evolution and whether or how nuclei and their connections were modified or lost during evolution. Neurophysiologists want to know how the brain processes information. They investigate the rules according to which information is processed, whether and which information is exchanged between nuclei and how brains generate behavior respectively spatial-temporal muscle contractions. It is also experimentally accessible to ask, for example, which nuclei are responsible for emotional behavior. The question of how feelings arise remains experimentally

4  The Central Nervous System of Fish     113

inaccessible. All physiological processes in the brain (in the nerve cells of the brain) are based on known physical-chemical laws. Although all nerve cells work according to similar or even to the same physical-chemical principles, we feel, depending on which nerve cells are currently active, e.g. pain, sorrow, joy, fear, panic, anger or desire. A physical world thus generates non-physical sensations. How this happens is not known and will probably remain a mystery forever. In all vertebrates, the information incoming from the sensory organs is processed in central sensory pathways. For example, there is a visual pathway, auditory pathway, taste pathway, and olfactory pathway. Sensory pathways consist of interconnected nuclei where sensory information is predominantly or even exclusively processed. In addition to the sensory pathways, brains contain motor pathways that originate in motor nuclei. These nuclei receive their input directly or indirectly from the sensory pathways, process the incoming sensory information, and as a result of their processing, send commands to the muscles with aid of motor neurons. The motor nuclei determine which muscles an animal contracts when, how quickly, how long, and with what intensity, i.e., whether or how an animal behaves in a given situation. Motor nuclei also control unconscious (involuntary) movements. These include breathing (gill cover movement in fish), heartbeat, and intestinal peristalsis. Some nuclei are responsible for processing emotional events. In addition to the aforementioned sensory and motor nuclei, the brains of all vertebrates (like those of many insects and other invertebrates) probably also have areas for spatial memory formation. This applies, for example, to the hippocampus, a nucleus in the forebrain of mammals and humans. However, modulatory nuclei are also of great importance for an animal’s survival. These include the dopaminergic, serotonergic, and noradrenergic systems (the chemical messengers of the nerve cells belonging to these systems are dopamine, serotonin, and norepinephrine). In mammals, the dopaminergic system is part of a reward system. When this system releases dopamine (e.g., during sexual intercourse), we feel extremely good. The dopaminergic system helps determine whether a person is more adventurous or more fearful. It also plays an important role in cognitive processes such as learning and memory and in movement control. The noradrenergic system, among other things, causes a person (a mammal) to focus its attention on a suddenly appearing aversive stimulus. This could be an animal that unexpectedly runs onto the road in front of our car, or a broken-down car blocking the road in a curve. In a fraction of a second, the noradrenergic system releases the neurotransmitter norepinephrine upon recognizing a suddenly appearing obstacle. We are instantly wide awake

114     H. Bleckmann

and can usually still avoid the danger. The serotonergic system influences, among other things, mood (anxiety), but also an animal’s (and a human’s) propensity for violence. I mention this in a book about fish because all the aforementioned modulatory systems have also been found in the brains of cartilaginous and bony fish. Therefore, we can assume that these systems perform a similar or even the same function in the fish brain as in the mammalian brain.

4.2 Evolution of the Brain When comparing the nuclei in the brains of different vertebrate species, the question arises as to whether or which nuclei are homologous. How this is determined will be explained using an example from comparative anatomy: The wings of all approximately 10,350 bird species still living today are homologous, i.e., they originate from a common ancestor. The wings of all insects are also homologous, they too originate from a common ancestor, but a different one than the wings of birds (the same applies to the wings of bats). Therefore, the wings of birds, bats, and insects are not homologous, but only analogous. The wings of birds, bats, and insects serve the same function (namely to enable flight), but do not originate from a common ancestor. They have each evolved independently during evolution. If one wants to find out whether a fossil animal could fly, one must first check whether it had wings. Similar considerations apply to the nuclei of central nervous systems. A nucleus involved in the analysis of potential dangers in mammals is the amygdala. The amygdala belongs to the limbic system. The amygdala is important for the generation of fear and anxiety. People with a damaged amygdala show no fear even in life-threatening situations. If one wants to find out whether fish feel fear, one should, in addition to behavioral experiments, also check whether there is a nucleus in their brain that is homologous to the amygdala of mammals. The above-discussed example of the wings of insects, bats, and birds was clear, because a wing is easily recognizable as such, even with different shapes and manifestations. In case of the nuclei of the brain, proving homology is significantly more difficult. However, with a certain probability, homologous nuclei can be identified by their location in the brain (e.g., in the midbrain or forebrain), their cell types (e.g., large or small, less or highly branched), and their input and output connections. If these are the same or similar, homology and thus functional equivalence is likely. Further criteria can be used to learn something

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about the possible function of a nucleus. For example, the neurotransmitter released by nerve cells are characteristic for a specific nucleus. The nerve cells of a nucleus referred to as the substantia nigra, for example, release dopamine. If these nerve cells stop producing dopamine, this leads to Parkinson’s disease and, in extreme cases, to complete immobility. Not only the mammalian brain, but also the fish brain contains dopaminergic cells. Another way to learn something about the suspected function of a nucleus is to surgically remove the nucleus or temporarily disable it by local cooling or anesthesia (at low temperatures, nerve cells show no activity). The behavior of the test animal (for example, fear behavior) is then compared before and after the operation. If the animal shows no fear at all after surgery, the deactivated nucleus was most likely involved in the generation of fear. New molecular genetic and developmental biological methods also allow conclusions about the origin and function of individual nuclei. However, these methods will not be discussed here. Similar to the wings of birds, bats, and insects, some nuclei are not homologous, but only analogous. In the course of evolution, a new nucleus has emerged in this case, or an existing nucleus has lost its original function and subsequently gained a new function. Using the methods mentioned, comparative neurobiologists have been able to show that fish brains, despite many species-specific peculiarities, are similarly structured in many areas to the brains of mammals (including the human brain). This is particularly true for the hindbrain, midbrain, and cerebellum. An exception is made, as already mentioned above, by the cerebral cortex), which is absent in fish.

4.3 Comparison Fish Brain—Mammalian Brain Mammalian researchers assume that only an exceptionally large cortex with its complex connections allows primates to perform higher cognitive functions. Conversely, this means that animals without a cortex have only lower cognitive abilities. To understand this argument, some information about the cerebral cortex of mammals is useful. The majority of the cerebral cortex in primates consists of six layers of pyramidal cells (the cell bodies of these cells look like small pyramids), this part of the cortex is also referred to as neocortex (or new cortex). In addition to the neocortex, there is also an  archicortex (old cortex) and the paleocortex (very old cortex). Unlike the neocortex, the archicortex and paleocortex consist of only three to four layers. Since differences in the evolutionary age of the different cortical areas

116     H. Bleckmann

are not proven, the neocortex is also referred to as isocortex and the rest of the cortex as allocortex. The neocortex is the seat of the highest integrative functions of the brain. Layer four of the neocortex receives input information from the sensory areas of the thalamus, a part of the diencephalon. Layer one receives input from adjacent cortical areas. The cells in layers two and three send their information to other cortical areas and the cells in layer five to areas outside the cortex. The cells of layer six project back to the sensory areas of the thalamus, thus being part of a feedback loop. Overall, the neocortex is characterized by numerous vertical and horizontal neuronal connections. The neocortex is particularly well developed in primates (including humans), in humans it covers 96% of the forebrain. Whales also have a large, highly folded cortex. This shows that during evolution there was no linear development of brains or brain areas. Because the evolution of whales began with the early even-toed ungulates (pigs, camels, ruminants) more than 50 million years ago in the Eocene, that of the great apes (chimpanzees, bonobos, gorillas, orangutans) began only about 15 million years ago. Although whales have a highly folded cerebral cortex, unlike the cerebral cortex of primates it consists of only five layers. In addition, the cerebral cortex of whales has significantly fewer cells per unit volume. I mention this only to point out that when assessing the performance of brains and brain areas, not only the size and external shape, but also the number, arrangement and connections of the nerve cells in these areas must be taken into account. Dolphins use their cerebral cortex primarily for emitting and processing ultrasonic sounds. In general, in the various vertebrate groups there is an independent, parallel increase in the complexity of the brains or individual brain areas. This also applies to the cerebellum of cartilaginous and bony fish. The fact that our knowledge about the complexity of certain brain areas can change quickly due to ongoing research is shown by the example of birds. Like fish, birds have a forebrain, which according to earlier studies should be much simpler than the forebrain of mammals. Recent studies show that this is not true and that many nerve cells in the forebrain of birds also have a vertical and horizontal arrangement. The resulting complex circuit diagrams in the forebrain could explain why many bird species have cognitive abilities similar to mammals. Whether some of the 33,000 living fish species also have complex cortex-like connections in the forebrain is conceivable, but has not yet been demonstrated. In science, there is consensus that consciousness in humans (and other mammals) requires a neocortex, a thalamus (part of the diencephalon),

4  The Central Nervous System of Fish     117

and connections between the thalamus and cortex. In mammals, with the exception of the olfactory system, all information coming from the sensory organs reaches specific sensory areas in the cerebral cortex via the thalamus. Scientists assume that human consciousness is linked to the cerebral cortex and neuronal connections within the cerebral cortex. Humans are only consciously aware of those sensory informations that reach the cerebral cortex. Fish do not have a cerebral cortex, but they do have a diencephalon with a thalamus. In fish, unlike in mammals, no (or at least very few) sensory information is transmitted from the thalamus to the forebrain. Therefore, according to the opinion of some researchers, fish lack the prerequisite for consciousness. The example of color vision has already shown that this argument is not conclusive. The forebrain of fish consists mainly of a subpallium and the much smaller pallium. Originally, both pallial areas were supposed to process only olfactory information. Their forebrain should therefore not allow fish to have higher cognitive abilities. Today we know that, similar to mammals, all sensory systems in both cartilaginous fish and bony fish send information to the forebrain. The forebrain of fish does not receive (or only a few) information from the thalamus, but from a core area of the diencephalon, which is referred to as the preglomerular complex. In addition, the forebrain of fish, like the cortex of mammals, is divided into a multitude of functional areas, all of which are interconnected. It therefore can not be excluded that some fish also have a certain form of consciousness. Another similarity with the mammalian brain should be mentioned. The forebrain of fish can be divided into a pallium and a subpallium (Box 9). The pallium of fish, in addition to inputs from all sensory systems, also receives modulatory inputs, including from nerve cells that release dopamine or serotonin. These neurotransmitters influence the motivation and emotional system (i.e., the sensations) of a human. This could mean that not only mammals, but also fish have a motivation and emotional system that is modulated by dopamine and serotonin. Box 9 Development of the brain. The fact that the embryonic development of an animal must also be taken into account when determining the homology of brain areas is exemplified by Fig. 4.5. The brain and spinal cord of all vertebrates develop from a tubular structure, the neural tube, during embryonic development. This structure can be divided into different sections from top to bottom (from the back to the belly side). In almost all vertebrates, including rays and

118     H. Bleckmann Evagination

Eversion

Pallium

Subpallium

Fig. 4.5  Cross-section through the neural tube during an early (bottom) and late stage of embryonic development (top). In cartilaginous fish (top left), the relative positions of the individual brain areas remain constant during development—as in almost all other vertebrates. In contrast, in ray-finned fishes (top right), all bony fish except lobe-finned fish, the originally centrally located brain areas move outward and downward through eversion (see positions of the stars). This must be taken into account when trying to determine which brain areas are homologous based on positional criteria.

sharks, the relative position of the individual sections of the neural tube does not change during embryonic development in the area of the later forebrain. In rayfinned fish, the upper sections of the neural tube (the centrally located upper section corresponds to the hippocampus of mammals) move outward and downward during embryonic development. Therefore, the brain area corresponding to the hippocampus (homologous) corresponds to the lateral part of the forebrain in ray-finned fish, and the centrally located part in cartilaginous fish.

4.4 Physiology of the Fish Brain 4.4.1 Neuronal Maps In the last 50 years, not only numerous works on the structure (fine structure), but also on the function (physiology) of the fish brain have been published. This book does not aim to report even remotely on the knowledge gained in this process. However, a few examples will show that fish brains often perform similar physiological functions to the brains of mammals.

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One example are neuronal maps. In the brains of mammals, numerous pieces of information are represented in the form of neuronal maps. For example, there are maps that represent the visual field (the visual space) in the visual cortex. This means that adjacent fields or excitation patterns in the retina of the eyes are represented in adjacent nerve cells in the visual cortex. Neuronal maps are also known from the auditory system of mammals. These maps systematically represent the frequency, amplitude, or origin of a sound event. The body surface is also represented in the brain of mammals in the form of neuronal maps. Important body parts, e.g. the hands, lips or wings of bats, are always overrepresented (examples see Fig. 4.6). The principle of representing information in neuronal maps is also realized in the brains of cartilaginous and bony fish. For example, a certain region in the midbrain roof (Tectum opticum) of fish each represents a certain area of the visual field. The distribution of electroreceptors in the skin of electric fish is also represented in neuronal maps. If a fish has several types of electroreceptors (this applies to all weakly electric fish), there is a separate neuronal map for each receptor type (Fig. 4.6). Further neuronal maps exist, for example, in the central auditory pathway and in the lateral line pathway of fish.

4.4.2 Reafference Principle Great apes (including humans) can move their eyes in many directions through the targeted interaction of several muscles. With each eye movement, the image on the retina shifts with a speed and an amount that depend on the command the brain has sent to the eye muscles. Another cause for an image shift are active or passive head movements. A shift in the image on the retina can also be caused by the movement of an external object (e.g., a pedestrian walking by). As we know from experience, the environment does not move for us during active eye, head, or body movements. The reason for this is that the motor centers of our brain create a copy (efference copy) of each movement command (a sequence of nerve impulses sent to the muscles by the brain) at the same time. Each image shift on the retina is therefore first compared with an expected image shift calculated by the brain based on this efference copy. If both match, the brain reports no movement (we do not perceive any image shift). The described neuronal mechanism allows us to distinguish image shifts caused by our own movement from those caused by external events. This model of motion control was discovered in the mid-20th century by Erich von Holst and Horst Mittelstaedt during their study of the visual system of the housefly.

120     H. Bleckmann Midbrain

a

Cat

Hindbrain

b

Rhesus monkey

c

Weakly electric fish

P- and TReceptors Ampullary receptors

Fig. 4.6  Sensory mapping of the body surface in the diencephalon in domestic cats (a) and rhesus monkeys (b). In domestic cats, the forepaws and the snout region are most strongly represented, in rhesus monkeys the head and limbs. (Adapted from Hildebrand et al. 2021; with kind permission from Springer Verlag. All Rights Reserved) (c) Representation of the electroreceptors in the hindbrain and midbrain of the weakly electric fish Eigenmannia. For each type of electroreceptor, there is a separate map in both the hindbrain and the midbrain. As in cats and rhesus monkeys, skin areas with high receptor density are particularly large in the brain. (Adapted from Carr and Maler; with kind permission from John Wiley & Sons. All Rights Reserved)

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Sometimes our brain is also deceived. For example, one can touch the skin at the outer edge of the left eye with the index finger of one hand and then pull the skin and thus the eye slightly to the side. At the same time, one should close the right eye. Although the environment and our head have not moved, we now see an image shift to the right. Eye movements triggered by a hand do not normally occur, so there are no neuronal circuits in the brain that can compensate for the image shift on the retina caused by the hand movement. Another sensory illusion occurs when we sit on a train. It has probably happened to you that a train starting on the adjacent track gives the impression that your own train has started moving. Only when the end of the neighboring train passes our window do we realize that our train has not moved. A particularly memorable sensory illusion occurred to me many years ago during a visit to Disneyland in Los Angeles. In the open car of a tourist train, we drove into a brightly lit narrow tunnel. As we entered the tunnel, the walls of the tunnel began to rotate around the tunnel axis. Of course, I saw through this, but my brain could not prevent the overpowering impression that the train was tipping over. So I clung to my seat to prevent a seeming fall out of the train. The information reported by the eyes to the brain was so dominant that the position information conveyed by the inner ears was “overruled”. I finally stopped the extremely unpleasant feeling that the train was tipping over by closing my eyes. Many fish, like mammals, can rotate their eyes in almost any directions. Some fish can even move their eyes independently of each other. Whether the brain of these fish can distinguish the image shifts caused by this from environmental movements has not yet been investigated, but is very likely. However, the relationship between foreign and self-signals was investigated using the example of the electrosensory lateral line. As mentioned earlier, rays perceive weak electric fields with their electrosensory lateral line. Similar to the visual system, every self-movement of the ray causes the sensory organs of the electrosensory lateral line to be stimulated. Here too, it is not possible to distinguish self-generated from externally generated stimuli based on the information originating from the sensory cells. The brain of the fish solves this ambiguity problem in the same way as the brain of mammals. It creates an efference copy of each motor command. To breathe, rays must constantly move their gill covers. Each movement of the gill covers inevitably modulates the weak electric DC field that surrounds rays (and every other fish). The electroreceptors of the rays respond to each gill cover movement with several nerve impulses, but the responses are suppressed by an efference copy at the first processing station in the brain. The central

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nervous system of the rays thus avoids unnecessarily further processing predictable consequences of nerve impulses. Similar findings have also been shown for the mechanosensory lateral line of fish.

4.4.3 Sensory Pathways Animals constantly receive information from their sensory organs. In mammals, this information is initially processed and forwarded in separate sensory pathways. These pathways include the visual, auditory, olfactory, and gustatory pathway. Within a sensory pathway, the various physical parameters of a stimulus are processed separately. In the visual pathway of mammals, this applies, for example, to the parameters color, movement (direction and speed), shape, and distance. Numerous examples of parallel information processing can also be found in the brains of cartilaginous and bony fish. All weakly electric fish possess, as already explained above, low-frequency ampullary and high-frequency tuberous electroreceptors. The information transmitted to the brain from these two receptor types is initially processed in separate pathways. Within the tuberous system, there is also a pathway for the stimulus amplitude and one for the stimulus shape (or stimulus phase). Mormyrids have tuberous organs (Knollenorgans) for intraspecific electrical communication. The information transmitted from the Knollenorgans is also processed in a separate sensory pathway. One last example: The mechanosensory lateral line of fish consists of free-standing neuromasts, which are sensitive to the velocity of water movements water movements on the fish surface, and canal neuromasts, which measure the pressure gradients along the head and trunk lateral line canals. The information from these two types of sensory organs is also processed in separate pathways at least up to the level of the midbrain. I have already shown above by example that fish use the information from several sensory systems for decision-making. This is referred to as multimodal information processing. Multimodal information processing reduces the probability of error. A simple example should illustrate this. Let’s assume we are hiking in Denali National Park in Alaska. Suddenly we hear a soft crackling in front of us in the bushes, probably caused by an animal. Since there are bears in this area, we stand still, take a closer look at the bushes and now believe to recognize the vague outline of a bear behind the bushes. As the wind is favorable, a strong smell that also indicates a bear reaches us at the same time. Now our brain is finally convinced that there is a bear in the bushes. To avoid any conflict, we carefully retreat. In the brains of mammals, the information from the various sensory systems is brought together in the association areas of the neocortex.

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Multimodal information processing takes place in these areas. This is also similar to fish, in whose forebrain information from all sensory systems also converges and is processed multimodally. Summary This chapter provides basic information about the central nervous system of fish. In addition to general information about the structure of the vertebrate brain, the chapter contains information about the development, anatomy, evolution, and physiology of the fish brain. It is shown that fish brains—with the exception of the forebrain—are similar to the brains of other vertebrates (including mammals and humans) in terms of their anatomy, complexity, physiology, and function, but undergo a strongly modified development during embryogenesis. Although the fish brain lacks a cerebral cortex, it performs cognitive functions in many areas that are tied to cortical circuits in mammals.

References Broglio, C., Rodríguez, F., & Salas, C. (2003). Spatial cognition and its neural basis in teleost fishes. Fish and Fisheries, 4, 247–255. Butler, A. B., & Hodos, W. (1996). Comparative vertebrate neuroanatomy. Evolution and adaptation. Wiley. Calvo, R., & Schluessel, V. (2021). Neural substrates involved in the cognitive information processing in teleost fish. Animal Cognition, 24, 923–946. https:// doi.org/10.1007/s10071-021-01514-3. Demski, L. S. (2013). The pallium and mind/behavior relationships in teleost fishes. Brain, Behavior and Evolution, 82, 31–44. Eaton, R. C., & Hackett, J. T. (1984). The role of the Mauthner cell in fast-starts involving escape in teleost fish. In R. C. Eaton (Ed.), Neural mechanisms of startle behavior (S. 213–266). Plenum. Hildebrand, J.-P., Bleckmann, H., & Homberg, U. (2021). Penzlin—Lehrbuch der Tierphysiologie. Springer. Nieuwenhuys, R., ten Donkelaar, H. J., & Nicholson, C. (1998). The central nevous system of vertebrates. Vol 1 and 2. Springer. Northcutt, R. G. (1984). Evolution of the vertebrate central nervous system: Patterns and processes. American Zoologist, 24, 701–716. Roth, G., & Wullimann, M. F. (1996). Evolution der Nervenssteme und der Sinnesorgane. In J. Dudel, R. Menzel, & R. F. Schmidt (Hrsg.), Neurowissenschaft. Vom Molekül zur Kognition (pp. 1–31). Springer. Striedter, G. F., & Northcutt, R. G. (2020). Brains through time. Oxford University Press.

5 Behavior

5.1 Evolution and Behavior How and why do animals behave the way they do? This is an exciting question that has interested me since I was a student. Behavior, like physical characteristics or physiological and molecular mechanisms, is subject to natural selection. Those who behave incorrectly and therefore have fewer or no offspring, and do not raise them, are missing in the next generation. Charles Darwin already pointed this out. An organism that is better adapted to its environment than its competitors produces more viable offspring and thus automatically prevails in evolution (the B.1.17 mutant of the coronavirus, which first appeared in England, has vividly demonstrated this to us). In terms of physical characteristics, “better” is usually easy to define. A pike that can strike faster catches more fish than its slower competitor. A fish that is better camouflaged remains undetected in danger, and a fish with sharper vision recognizes a food source from a greater distance than its food competitor. The proof that a certain behavior is optimal is much more difficult to provide, as the evolutionary advantage of a behavior is usually not immediately visible. According to behavioral ecologists, animals are optimally adapted when they behave at every point in their lives in such a way that the long-term evolutionary advantage achieved through their behavior is greater than the long-term evolutionary disadvantage. Advantage and disadvantage always refer to the number of viable offspring. Or in other words: All behaviors that lead to more viable offspring automatically prevail in evolution. © The Author(s), under exclusive license to Springer-Verlag GmbH, DE, part of Springer Nature 2024 H. Bleckmann, Stupid as a Fish?, https://doi.org/10.1007/978-3-662-68376-7_5

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Fish that follow this rule, like all other animals, have a selection advantage. Of course, animals (and humans) do not make conscious decisions regarding the evolutionary consequences of their behavior. They simply behave as if they were aware of the evolutionary consequences of their actions. A salmon that returns to the spawning grounds in the upper reaches of its home waters after several years at sea does not do this with the intention of reproducing, but simply follows the innate migratory drive that arises at a certain stage of life. It used to be believed that the behavior of fish was exclusively instinctdriven (innate). In contrast, learning processes and thus environmental influences should have a decisive impact on the behavior of higher mammals. Both assumptions have proven to be false, because in fish and mamals, both the environment, i.e., learning and memory, and the genes decide how an animal behaves in a certain situation. Whether, what and how much an animal can learn and retain depends only partially on its systematic position. If certain habitats and life circumstances require certain cognitive performances, these are also provided by the animals. Otherwise, they would not have been able to colonize these habitats or ecological niches at all. In other words: Similar ecological constraints often lead to similar adaptations and brain performances in very different animal groups. If the environmental conditions remain constant over a long period of time (e.g., the change between the seasons in Central Europe), innate (instinctive) behaviors are usually the most reliable (e.g., bird migration in the fall from Europe to Africa and in the spring from Africa back to Europe). Instinctive knowledge or behavior is always advantageous when a wrong reaction, e.g., at the first encounter with a source of danger, can be fatal. Fish that are attacked by a predator should evade an attacking predator in the right direction at the highest possible speed, even without experience. The fact that they can do this is ensured by two large cells, the Mauthner cells (Fig. 5.1a), located in their hindbrain. In case of danger, these cells, which receive input from acoustic, vestibular, optical, and lateral line nerve fibers, trigger an escape reflex within 5 to 25 milliseconds. With an angular speed of up to 3000 degrees per second, the Mauthner reflex catapults the attacked fish out of the source of danger at lightning speed (Fig. 5.1b, c). Only wanting to find out through learning whether a predator poses a danger would probably almost always be fatal for many fish. If environmental conditions and/or behaviors of conspecifics are unpredictable, the ability to learn provides a great advantage. Since fish of different species inhabit very different habitats and/or ecological niches, what they can learn, how quickly they learn, and how quickly they forget what they have learned is

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a

0,5 20 ms

X 100 ms

Angular speed (degrees/s)

4000

2000 1000 0 –1000 –2000

1,0 b

3000

Y

c

–20

0 20 40 60 Time after start (ms)

80

Fig. 5.1  a–c. a Mauthner cell in the hindbrain of the paddlefish (Polydon spatula) (photo M. Hofmann). b Mauthner cell reflex of the goldfish Carassius auratus. The black dot shows the position of the tip of the snout 20 and 100 ms after the start of the escape reaction. c Average angular speed of the longitudinal axis of the fish’s head during twenty escape movements within the first 100 ms after the start of the escape. (Adapted from Eaton and Hackett 1984; with kind permission from Plenum Press)

species-specific. However, there is no clear contrast between innate and learned behavior. Konrad Lorenz has already pointed out that there is only a gradual difference between innate (genetically determined or acquired in phylogenetic history) knowledge and individually learned knowledge, as the

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physiological and molecular mechanisms that enable learning and memory are also subject to genetic control, i.e., they are innate. An example of an innate predisposition to learning is the imprinting of following in gray geese. Gray goose chicks must first learn what their mother looks like. Therefore, after hatching, they approach the first object that moves and makes sounds (in extreme cases, this can be a sound-making football). After a short time near this object, they follow it unconditionally. Under natural conditions, the first object a gray goose chick sees is always the mother, as she incubates the eggs. It is very likely that epigenetic phenomena (caused, for example, by stress or fear) also influence behavior in fish. Epigenetic mechanisms can even pass on experiences to the next generation.

5.1.1 Group Selection Konrad Lorenz mistakenly assumed that natural selection primarily serves the preservation of species, a view he extensively justified in his 1963 book “On Aggression”. The basic idea was that groups of animals of one species, consisting only of altruists, have a greater chance of survival than groups of pure egoists. In social sciences, altruists are understood as people who restrict their consumption to increase the consumption of others (e.g., through monetary donations). The recipient of the aid can be fellow human beings in need, but also animals (e.g., with a donation for animal or nature conservation). In contrast, an egoist is a person whose actions are solely aimed at their own material advantage. In evolutionary biology and evolutionary psychology, the terms altruist and egoist are much more sharply defined. An altruist is a creature that consciously or unconsciously renounces its own chances of reproduction for the benefit of conspecifics. An egoist, on the other hand, is an animal that is solely aimed at optimizing its own reproductive success in its actions. The idea of group selection was first expressed by Charles Darwin, picked up in 1962 by the British zoologist Vero Wynne-Edwards, and extensively justified in the book “Animal Dispersion in Relation to Social Behaviour”. The concept of group selection assumes that not the individual, but the group (for example, a school of fish) is the unit of natural selection. According to the theory of group selection, it is advantageous for each individual in a school to behave altruistically (i.e., at their own expense for the benefit of the other school members). Fish (or other animals and humans) should, for example, keep the number of their offspring low to preserve limited available food resources for the other group members (the fact that this

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is not the case is already shown by the still largely unchecked population growth of humans in developing and emerging countries). Against the theory of group selection is the fact that individual selection proceeds much faster than group selection. If an egoist arises in a group of pure altruists due to random changes in the genetic material (mutation), this egoist has a selection advantage and will therefore spread within the group at the expense of all other group members. Evolutionary biologist William D. Hamilton was the first to recognize that in the evolutionary assessment of whether a behavior is egoistic or altruistic, one must consider not only the number of one’s own offspring (= individual fitness) but also the number of offspring of all relatives, weighted by degree of kinship (= inclusive fitness). Which individual (phenotype or appearance = set of all external characteristics of an organism) develops from a fertilized egg is largely determined by the genetic makeup and thus the genes. Genes determine in mammals, for example, the sex, eye color, body size, and behavior (e.g., brave or fearful). The gene for blue eye color differs from the genes for green, yellow, or brown eye colors. Therefore, the genes responsible for eye color are not all the same, so they are referred to as alleles that compete for the same gene location. When looking at the level of alleles in the evolution of egoists and altruists, this means that “selfish” alleles spread within a group at the expense of “altruistic” alleles. However, this only applies to a certain extent, because sooner or later egoists almost only encounter egoists and then experience a selection disadvantage (e.g., because the egoists injure or even kill themselves in the attempt to achieve a goal by force). For this reason, a balance between egoists and altruists will establish itself in a natural population. A second example: In bluegill sunfish (Lepomis macrochirus), the males build a nest during the mating season, court females, and fertilize the eggs immediately after the female spawns. The clutch and eventually the brood are then guarded by the male. However, there are also males who save themselves the work of nest building. These males (“parasites”) invade the nest of a foreign male shortly after egg laying and fertilize the freshly laid eggs themselves. Stabilizing selection maintains a certain ratio between nest builders and parasites. Because if no male builds a nest anymore, the parasite can no longer reproduce. The mating of the bluegill sunfish is determined by genetically conditioned behavioral strategies, with the frequency distribution remaining stable. In this case, we speak of an evolutionarily stable strategy (ESS), i.e., a strategy that cannot be changed by any mutation. A second argument speaks against group selection. A group of altruists can hardly avoid being infiltrated by egoists from a neighboring group.

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These egoists would then spread within the new group of altruists at the expense of all other group members. Whether group selection is not important under certain conditions cannot yet be completely ruled out and is currently being hotly debated by scientists. As already mentioned above, Konrad Lorenz transferred the principle of group selection to the species. As proof, he cited, among other things, that animals almost never kill a conspecific, but—to preserve the species—they settle their disputes exclusively in the form of ritual fights. Today we know that in many animal species—apart from diseases and parasites—most individuals are killed by conspecifics. Humans, as a glance at crime statistics and the number of annual war deaths shows, are unfortunately no exception. Infanticide is widespread in the animal kingdom. For example, when a new male lion takes over a pride, it kills all the cubs that are still so small that their mother cannot ovulate for the next 2 to 3 months. Since lionesses can become pregnant again immediately after their young have been killed, the new leader ensures that he can sire his own offspring immediately after taking over a pride. Infanticide has now also been detected in many primate species, but also in other mammals and birds, and was originally common in human societies (if abortions are counted as infanticide, child killing is still common today). Infanticide is also found in fish. In many fish species, the males take on the task of brood care. These fish include the blenny Rhabdoblennius nitidus. After a male blenny has enticed a female to lay eggs through courtship, he fertilizes the eggs. The male then guards the clutch until the young fish hatch. Occasionally, a male gives up guarding and eats his own clutch or the freshly hatched young fish. Initially, it was thought that this happened due to a lack of food. However, Japanese researchers have observed that even well-fed males sometimes eat their clutch or remove individual eggs from the clutch one by one. These behaviors were particularly common with small clutches. Studies have shown that a significant factor for the males’ seemingly strange brood care behavior is a hormone level altered by the presence of the clutch. In the presence of a fertilized clutch, the testosterone level of the males drops to a lower level. This ensures that the males do not court any more females, but devote themselves exclusively to brood care. After the destruction of the clutch, the testosterone level rises, the males can now mate again and possibly with greater success with another female. In sand tiger, mako, herring, and white sharks, intrauterine cannibalism occurs. In these sharks, the young hatch from the eggs in the womb and initially feed

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on the yolk supply. As soon as this is used up and the first teeth have developed, the young start to eat each other while still in the womb.

5.1.2 The King Selection Apparently altruistic behaviors also seem to be widespread among fish, as many fish show brood care behavior. They do this because their offspring carry 50% of their alleles (50% from the male and 50% from the female). Often, one can observe that in addition to the parents, another fish is involved in the brood care. This helper obviously forgoes his own reproductive chances while helping, so at a superficial glance, he has a selection disadvantage. As genetic studies show, helpers are almost always young fish from a previous brood. These young fish thus share (provided the eggs were fertilized by the same male) 50% of their genes with the fish they are helping to raise. If a helper has not found a partner for his own reproduction, his seemingly altruistic behavior at the level of alleles or genes is selfish behavior (Box 11). Kin selection is one of the evolutionary engines that produces seemingly altruistic behaviors in fish (and other animals). Box 11 Spread of altruistic alleles. According to the English evolutionary biologist William D. Hamilton, “altruistic” alleles (alleles that promote altruistic behavior) spread in a group (or population) when the following applies:

C