The Equids: A Suite of Splendid Species (Fascinating Life Sciences) 3031271432, 9783031271434

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Fascinating Life Sciences

Herbert H. T. Prins Iain J. Gordon Editors

The Equids A Suite of Splendid Species

Fascinating Life Sciences

This interdisciplinary series brings together the most essential and captivating topics in the life sciences. They range from the plant sciences to zoology, from the microbiome to macrobiome, and from basic biology to biotechnology. The series not only highlights fascinating research; it also discusses major challenges associated with the life sciences and related disciplines and outlines future research directions. Individual volumes provide in-depth information, are richly illustrated with photographs, illustrations, and maps, and feature suggestions for further reading or glossaries where appropriate. Interested researchers in all areas of the life sciences, as well as biology enthusiasts, will find the series’ interdisciplinary focus and highly readable volumes especially appealing.

Herbert H. T. Prins . Iain J. Gordon Editors

The Equids A Suite of Splendid Species

Editors Herbert H. T. Prins Department of Animal Sciences Wageningen University Wageningen, The Netherlands

Iain J. Gordon Fenner School of Environment & Society Australian National University Canberra, Australia

ISSN 2509-6745 ISSN 2509-6753 (electronic) Fascinating Life Sciences ISBN 978-3-031-27143-4 ISBN 978-3-031-27144-1 (eBook) https://doi.org/10.1007/978-3-031-27144-1 © The Editor(s) (if applicable) and The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 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 Nature Switzerland AG The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

Hooves thunder Flying across the plains: Ever invincible

Foreword

As of this year (2023), seven species of wild equids grace Earth. Three are asses – two endangered. Three are zebras, two endangered; the sole wild horse is also endangered. This was not the case some 150-200 years ago. Stepping farther back, in the late Pleistocene, equids were far more widespread. And, they played ecologically relevant roles on the grasslands of five of six Earth’s continents – South America, North America, Asia, Europe, and Africa.

Humanity has been shaped by animals, influences that still mould us today. An array of species has satiated us and worked, as domestics, for us. Animals stir our imagination. Not only do constellations bear monikers of real and imagined species, but also artists draw and musicians sing about such beings. To claim that animals hold special reverence is mere truism. From the 45,000year-old painting of pigs in Sulawesi’s Leang Tedongnge site to the 38,000-year-old lion-man, carved from mammoth ivory and discovered in Germany eighty-five years ago, wild species catalyse spirits. The global intrigue has been deep and independent; on five of the six continents, petroglyphs thousands of years old were chiselled into rocks. Our fascination with ancient and existing beasts transcends art and culture. Consider hunting. No, not the ‘sport’ of today in pursuit of trophies or for meat. Moving deep into our past—some 400,000 years ago—eight wooden spears were found at what is now a German sedimentary rock site formed by compressed peat. Remains of about twenty Pleistocene horses were scattered about. A spear was implanted in a pelvis. Hunting by hominins has to have been the genesis of science through the practice of both inductive and deductive thought. This sort of reasoning is what the scientists of this volume bring forth in the quest to understand a very special group of mammals: The family Equidae has for more than a century been at the forefront of scholarly inquiry. For contributors of this work, myself included, the appeal of equids far exceeds a passing interest in utilitarian use or artful respect, as important as these pursuits are. A curiosity about this suite of splendid species goes to the heart of evolutionary and ecological understanding. This volume in particular—among the first academic vii

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treatises in nearly four decades—probes deeply to question past assertions and to bolster a multi-dimensional approach to better appreciate the Equidae. Herbert Prins and Iain Gordon have brought together experts who are profound in their explorations of nutrition and ecology, genetics, paleo-faunas, and evolutionary thought to frame zebras, horses, and asses as vibrant ecosystem constituents, both past and present. The authors pose questions and offer syntheses not previously available. The assessments are many—how have views of the Bell-Jarman Principle changed across half a century, will we ever approximate how many ‘real’ species of equids exist(ed), and what type(s) of selective forces have moulded speciation, hind-gut fermentation, and niche differentiation? With precision, authors tackle equid morphology and anti-predator defence, diseases and parasites, and why the radiations into hot and cold extremes from below sea level in the Danakil Depression of Somalia to plateaus above 5400 m in Tibet. Not least, however, is the penultimate chapter delving into equid relations with humans today including our marvellous dismantling of places where wild equids once ran freely. The final chapter, especially when contextualized with the first in the book—whether it’s true that equids are not evolutionary dead ends—will be provocative in the best of ways. Prins and Gordon posit that equids are finely tuned to the biomes they share with large herbivore ruminants, differentiated by their adaptations. While species like elephants or whales enthral the public at large, most people will never see a whale or elephant except in the digital media or perhaps in a zoological garden. By contrast, not only does nearly everyone know of horses, zebras, or asses but also far more people can relate because they’ve seen some form of their descendants. Across vast sections of humanity, equids have a place in our hearts and our souls. For scientists however, equids are a source of powerful query. Equids continue to be longstanding models to understand the biology of time as witnessed by changes in form and function, ecological role, and mystery. Our appreciation for how life on Earth unfolds has been shaped by fossils, and certainly, now in a more contemporary setting, by molecular discovery and behaviour. The Equids: a suite of splendid species envelopes this in a new story. Joel Berger, author of Wild Horses of the Great Basin Colorado State University, Fort Collins, CO, USA

Joel Berger

Contents

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Are Equids Evolutionary Dead Ends? . . . . . . . . . . . . . . . . . . . . . . . Herbert H. T. Prins and Iain J. Gordon

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Evolutionary Radiation of Equids . . . . . . . . . . . . . . . . . . . . . . . . . . Juan L. Cantalapiedra, Oscar Sanisidro, Enrique Cantero, Jose Luis Prado, and María Teresa Alberdi

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The Miocene Browsing Horses: Another Way to Be a Successful Large Equid . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Christine M. Janis, Edward Franklin, C. Nicholas Baird, and Joshua Tyler

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Why There Are No Modern Equids Living in Tropical Lowland Rainforests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Joost F. de Jong and Herbert H. T. Prins

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Evolution of Equid Body Size . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 113 Carmen Nacarino-Meneses

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Forage Consumption and Digestion in the Modern Equids . . . . . . . 143 Iain J. Gordon and Herbert H. T. Prins

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Revisiting the Jarman–Bell Principle . . . . . . . . . . . . . . . . . . . . . . . . 171 Arjun B. Potter and Robert M. Pringle

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Equid Adaptations to Cold Environments . . . . . . . . . . . . . . . . . . . . 209 Qing L. Cao, Budhan S. Pukazhenthi, Priya Bapodra, Samantha Lowe, and Yash Veer Bhatnagar

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Adaptations to Hot Environments . . . . . . . . . . . . . . . . . . . . . . . . . . 247 Jennifer Sneddon

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Diseases and the Distributions of Wild and Domestic Equids . . . . . 269 Susan J. Dennis, Ann E. Meyers, and Peter J. Mitchell ix

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How Equids Cope with Macroparasites . . . . . . . . . . . . . . . . . . . . . . 299 Kaia J. Tombak and Daniel I. Rubenstein

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Equids and Predators . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 323 Daniel I. Rubenstein

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Evolution of the Equid Limb . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 347 Mariëlle Kaashoek, Jamie A. MacLaren, Peter Aerts, and Sandra Nauwelaerts

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On Humanity and Equids: Ecologies, Trajectories, and Relationships . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 379 Robin Bendrey and Rebecca Oakes

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Conclusion: A New Story of the Modern Equids . . . . . . . . . . . . . . . 411 Iain J. Gordon and Herbert H. T. Prins

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 425

Chapter 1

Are Equids Evolutionary Dead Ends? Herbert H. T. Prins and Iain J. Gordon

If a student today asks, ‘how shall I study palaeontology’, we can do not better than direct him to the Versuch einer natürlichen Classification der fossilen Huftiere of Kowalevsky, out of date in some facts, thoroughly modern in its method of approach to ancient nature. This work is a model union of the detailed study of form and function with theory and the working hypothesis. It regards the fossil not as a petrified skeleton, but as having belonged to a moving and feeding animal; every joint and facet has a meaning, each cusp a certain significance. Rising to the philosophy of the matter, it brings the mechanical perfection and adaptiveness of different types into relation with environment, with changes of herbage, with the introduction of grasses. In this survey of competition it speculates upon the causes of the rise, spread, and extinction of each animal group. In other words, the fossil quadrupeds are treated biologically – so far as possible in the obscurity of the past. From such models and from our own experience we learn to feel free to abandon outworn traditions in the use of the tools of science . . . . H.F. Osborn [1874] (1910)

Abstract We posit that it is trite to compare equids with Pecora or ruminants and conclude that the equid lifestyle is less ‘successful’ because equids are hindgutfermenters and happen to be less speciose than ruminants. Indeed, ‘speciosity’ is a poorly supported attribute of ‘success’ which itself is poorly defined. Yet, it appears that the current number of equid species is smaller than it was when Equus, and its allied genera, still naturally occurred in the Americas in the Late Miocene and H. H. T. Prins (✉) Department of Animal Sciences, Wageningen University, Wageningen, The Netherlands e-mail: [email protected] I. J. Gordon Fenner School of Environment & Society, The Australian National University, Canberra, Australia e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 H. H. T. Prins, I. J. Gordon (eds.), The Equids, Fascinating Life Sciences, https://doi.org/10.1007/978-3-031-27144-1_1

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Pliocene. On the other hand, a much-needed revision of the genus, based on genetics, may show a number of ‘hidden species’ that are bundled within the kulans and the Burchell’s zebra. Besides speciosity, geographic extent of a species or a group of species is often also used to indicate ‘successfulness’. If that criterion is applied to the Modern genus, after it expanded into Eurasia and Africa (but before humans started hemming it in and competing for land), as compared to before it left the Americas behind, then the startling conclusion is that Equus became more ‘successful’. Many ‘theories’ and ‘hypotheses’ that have been formulated to ‘explain’ the morphological features of equids can safely be rejected based on new research that is presented here. And so can the notion that equids are somehow inferior to bovids and other Pecora: on the contrary, equids are marvellously well adapted.

Henry Fairfield Osborn’s (a famous fossil hunter, student of Cope and Huxley and long-time director of the American Museum of Natural History) quote from his famous book, The Age of Mammals in Europe, Asia and North America, encapsulates much what drives us in our endeavour to understand the evolution of the animals and their place in the modern world. The present book is about equids – not only about the living ones, but also about species that are long dead. Fossils represent once living animals, with their physiology, endocrinology, behaviour, and adaptations. One hardly ever knows, nor can know, why or how these fossil forms died out. However, because the dominant paradigm of our day is that all forms of life are subject to the forces of natural selection, which shape the evolutionary outcome (and thus the phenotypes with which species have to engage the world), the sheer fact of extinction leads to the belief that the extinct species were somehow less fit than the surviving forms. In a similar vein, it is the dominant way of thinking that diversity is superior to uniformity. This view leads to the thought that a speciose group of related organisms is somehow more successful than a species-poor group. Because the family Equidae encompasses numerous extinct genera and species (see https://en.wikipedia.org/wiki/Equidae), the thought may arise that the ‘horse Bauplan’ is an evolutionary failure in the present-day context. The Bovidae (the family of the antelopes, sheep and goats) (see https://en.wikipedia.org/wiki/ Bovidae) on the other hand, are positively framed in terms of the ‘explosive’ radiation of forms in the Middle Miocene (Allard et al., 1992; Bibi, 2013: 17 Mya), or perhaps at the end of the Miocene (Ropiquet & Hassanin, 2005: 11 Mya), or sometime in between (Hassanin & Douzery, 1999: 12–15 Mya), or a little bit later (Zurano et al., 2019: 13.5 Mya). The Cervidae seem to have a slightly later radiation at 12 Mya (Zurano et al., 2019). Because the Bovidae is thought to be ‘successful’, just as is the equally ‘successful’ Cervidae, it is then a simple leap of faith to think that because these two families form part of the suborder Ruminantia, the ruminant strategy must be superior to the hind-gut fermenting strategy of the equids. In the same vein, one can deduce that brachydont teeth (so, molars that are short) in contrast to hypsodont teeth (molars that are very long) are inferior because

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Fig. 1.1 The view of horse evolution around 2000, emphasizing the bushy branching nature of their history, as many more fossils have been found and new species named. However, the overall trends toward higher-crowned teeth (shown by the symbols for browsing leaves or grazing grasses), larger size, longer limbs, and reduction of side toes are still considered true. Source: MacFadden, 2005, with permission from AAAS

early equids had brachydont teeth, and Modern equids have hypsodont teeth. Pictures like Fig. 1.1 emphasize this image of a once tremendously successful group of horse-like animals that suddenly come to a halt and peter out to one ‘miserable’ remaining genus, the equids. If this image is then placed together with another ‘failing group of animals’ the camelids (Fig. 1.2), and contrasted with the

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Fig. 1.2 The family tree of camels, showing the great diversity of forms, from small primitive deerlike creatures to the gazelle-like stenomylines, the short-legged protolabines and miolabines, the long-legged long-necked “giraffe camels,” and the modern humpless South American camels (alpaca, llama, vicuña, guanaco), which are more typical of the whole family. The camel family, like the horse family, contained many species and genera in the past and few now. Source: Prothero, 2009, with kind permission from Springer Nature

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explosive radiation of the Pecora, then the conclusion must be that equids, like all Perissodactyla, represent a failing mode of life. The question, however, is whether these deductions and their invoked images of failure are correct. Hence, the authors in this book collectively investigate whether equids are a relic of the past and comprise lifeforms that are poorly adapted to the Modern era, or not.

Speciosity and Wide Distribution Hallmarks of Success? It is a widespread axioma in evolutionary studies that a group of taxa is considered ‘successful’ if that group has many species or much biological variation (e.g., Michaux et al., 2001; Wake & Hanken, 2004; Olivera et al., 2014; Verstraete et al., 2017; Peters et al., 2018; Sork et al., 2021). Another criterion that is used to describe a group of taxa as ‘successful’ is when they have a wide distribution (Michaux et al., 2001; Wake & Hanken, 2004). High speciosity and widespread distribution, however, do not necessarily correlate (see, for instance, the radiation of murine mice on the Solomon Islands: Aplin & Ford, 2014). Also, in the Artiodactyla, the characteristic ‘speciosity’ is used as a descriptor of ‘success’ (Clauss & Rössner, 2014; O’Brien, 2016), as is a wide distribution (Clauss & Rössner, 2014). Indeed, Claus and Rössner describe the present-day Tragulidae as species-poor with a narrow geographical distribution and compare them with the Pecora, pointing out that several million years ago the Tragulidae were speciose, and thus ‘successful’, and now are not anymore. But what is the definition of success in ordinary language? It is described as ‘the accomplishment of an aim or purpose’ (Oxford Languages) or ‘the correct or desired result of an attempt’ (Merriam-Webster). The Cambridge Dictionary describes ‘successful’ as ‘achieving the results wanted or hoped for’. In other words, the term ‘success’ can only be used if there is an a priori set goal. Because evolution is blind and has no purpose, the term ‘successful’ is thus, to put it mildly, strange. In behavioural ecology, however, the term ‘success’ has been used in conjunction with ‘reproductive success’. This term is defined as ‘the number of an individual’s biological offspring who survive to sexual maturity’ (see Clutton-Brock, 1988) and because this is linked to fitness, one may assume that natural selection ‘sees’ this as a goal function. It thus makes sense to use the concept ‘success’ in that field of ecology, but not so in association with diversity. In other words, we do not believe that it is valid to posit that equids are less successful than, say, Artiodactyls. Hence, it is not correct to claim that a hind-gut fermenter strategy is less ‘successful’ than a foregut fermenter strategy. But one could take this as a semantic argument and need biological arguments to reject this assertion as a false belief. There are also a number of purely biological reasons to treat speciosity as a measure of ‘success’ with apprehension. We mention the following reasons (inspired by the very insightful paper by Taylor et al. (2006):

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(a) In relying on the concept of morphological species recognition when comparing equids with bovids, one assumes that systematicists and palaeontologists recognize ‘species’ in these two families with equal acumen and perspicacity. First, equids, even though reasonably diverse, may have fewer morphological characters that are used for classification than do bovids. Second, equid morphology may be more difficult to assess than is bovid morphology because, for instance, soft tissues are possibly more important for equids. Third, the rate of change of morphological characters may be greater in bovids than it is in equids. This latter is perhaps possible if sexual selection on the shape and size of headgear (horns; like antlers in the cervids) is more powerful in bovids and cervids than it is in equids that do not have this headgear (cf. Wang et al., 2019). (b) While recent genetic analyses of bovids show an enormous speciosity (e.g., Hassanin & Douzery, 1999; Bibi, 2013; Chen et al., 2019), one must realize that the sampling of all that diversity was facilitated by the fact that so many specimens had been classified already and grouped into species. If one would suppose that there were many cryptic species hidden in the current apparent phenotypic homogeneity of, for instance, Burchell’s zebra (Equus burchellii a.k.a. Plains zebra, E. quagga), then it would be expected that a sampling programme for genetic research could have found them, but presently genetic research on wild equids is not as comprehensive as is that on bovids, even though it appears to be catching up fast (e.g., Steiner et al., 2012; Der Sarkissian et al., 2015; Heintzman et al., 2017; Librado & Orlando, 2021). Indeed, Librado and Orlando (2021) refer to ‘nine extant pockets of molecular diversity’ for Burchell’s zebra beside the extinct quagga, which is confirmed by Pedersen et al. (2018). (c) A third reason to treat speciosity as measure of success with apprehension is that the different (chrono-)species of Equus are possibly less permanent than are those in bovids and cervids because of ‘reticulate evolution’. In that case, phylogenetic species are not very well ‘maintained’, for instance due to hybridization. Some species groups appear to show a lot of reticulate evolution, including our own (Ackermann et al., 2016; Arnold & Kunte, 2017; Ottenburghs et al., 2017a, 2017b; Rogers et al., 2019). The morphological plasticity that has been reported from the genus Equus (Librado & Orlando, 2021) may point in this direction too. Indeed, Burchell’s zebra hybridize with both Grevy’s zebra (E. grevyii) and with Mountain zebra (E. zebra) (Gippoliti et al., 2018). The consequences of reticulate evolution for the theory of evolution are not yet very clear, but may be rocking many older assumptions (Gontier, 2020). We think the reality of reticulate evolution, and so widespread (but perhaps punctuated over time) introgression and hybridisation, can upset much of our thinking about phylogeny, speciosity and thus ‘success’ of particular species groups. Because Bovini also show hybridization to various extents (see, e.g., Prins et al., 2023), the verdict is still out in how this affects the comparison between hind-gut fermenters and foregut fermenters. (d) We also draw attention to the fact that genera are poorly defined in biology. Different modes of thinking, paradigms, impact on the construction, and

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Fig. 1.3 Visual representation of the geological span and geographical ranges of equids through the Cenozoic (from Matthew, 1926). Matthew, W.D. (1926). The evolution of the horse: a record and its interpretation” The Quarterly Review of Biology, 1, pp. 139–185

interpretation, of phylogenetic trees and on thinking about what a ‘genus’ is (see Box 1.1 and Figs. 1.3 and 1.4). So, again, if horse-systematicists or horsepalaeontologists have different paradigms, for whatever reason, than do students of Bovidae and Cervidae (Pecora) then their storylines will be difficult to compare. That is why in this book, we do not want to dwell too much on the

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Fig. 1.4 The number of genera one could discern in living and fossil horses depends on the analysis one performs. & used for explicit criteria (for details see the original publication) (a) phylogenetic gaps, (b), uniqueness of adaptive zone, (c), crown group definition, and (d) divergence time. They performed a phylogenetic analysis of derived Equini using a matrix of 32 morphological characters and 21 Equini taxa, namely, Astrohippus stocki, Boreohippidion galushai, Dinohippus leardi, D. leidyanus, D. interpolatus, D. mexicanus, Equus conversidens, E. ferus, E. hemionus, E. idahoensis, E. mexicanus, E. neogeus, E. occidentalis, E. quagga, E. simplicidens, E. stenonis, Haringtonhippus francisci, Hippidion saldiasi, Hi. principale and two outgroup taxa, Acritohippus stylodontus, and Pliohippus pernix. Source: Barrón-Ortiz et al., 2019, published under CC BY 4.0 (https://creativecommons.org/licenses/by/4.0/)

question of whether equids are less well adapted than Pecora, or whether the foregut fermenting strategy so much better than the hind-gut fermenting strategy. We are much more interested in investigating how well adapted equids are.

Box 1.1 What Is Equus? ‘The question “What is Equus”?’ is a philosophical one that ultimately relates to the evolutionary paradigm under which individual researchers are operating and the research questions that are being asked. In this sense, the question we pose . . . may have different answers depending on the paradigm under (continued)

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Box 1.1 (continued) consideration. What Equus is, under these varying paradigms, has implications for how we communicate knowledge about the evolutionary and taxonomic history of horses. Perhaps the more valuable question is not ‘What is Equus?’ but rather ‘How variable is the taxonomic content of Equus in a given phylogenetic tree, under very distinct paradigms for understanding higherlevel taxonomy?’ See also Fig. 1.4. Barrón-Ortiz et al. (2019)

Speciosity and Wide Distribution of Equids in the Past and at Present It cannot be denied that, in the past, there were many more species of equids than there are now. This statement is of course subject to the fact that ‘the past’ was much longer than the average time of existence of a given species. This refers to the concept of ‘chronospecies’ that palaeontologists use. A chronospecies is a whole series of forms over time (so a lineage of progenitors and descendants) for which it claimed that they morphologically belong to the same species. Alternatively stated, a chronospecies is a segment of an evolutionary lineage subjectively designated as a species (Stanley, 1978). Not only the fossil record but also the ability of the palaeontologists studying the fossil material to discern species in that material (cf. Lyman, 2019; Cucchi et al., 2017) thus plays a role in determining how old a species is determined to be. On average, a placental mammalian chronospecies lasts for about 1.5 million years, independent of continent or systematic group, while the rate of extinction is constant (Stanley, 1978; Alroy, 1996; Vrba, 2000; Bibi & Kiessling, 2015), and a genus much longer (Stanley, 1978). Among palaeontologists studying the fossil remains of equids there is no consensus about how to distinguish intraspecific variation between ecomorphs (adaptive or not) from a certain amount of morphological change that could be considered large enough to reflect speciation in equid lineages (Van Asperen, 2010; Boulbes & van Asperen, 2019). In other words, there is the risk that ecomorphs are mistakenly taken as species, or, alternatively, there is the risk that species reflect intraspecific variation. A good case in point of distinguishing ‘too many’ species is the South American Equus species: a few decades ago the fossils were reckoned to represent five species (E. andium, E. insulates, E. santaeelenae, E. neogeus and E. lasallei) - then three (E. neogeus, E. insulatus and E. andium), and now only one, namely, E. neogeus (Machado & Avilla, 2019). On the other hand, we think there is a fair chance that within E. hemionus a suite of species is hidden as it may be the case within in E. burchellii. The debate about the inclusion of E. hydruntinis (the European extinct Pleistocene wild ass) within E. hemionus, or not, (cf. Boulbes & Van Asperen, 2019) exemplifies this.

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So, is the present family of Equidae a pauperized reflection of what used to be a very diversified group of grazers and browsers? Here we run into difficulties about the species concept itself, and about the genus concept, and about what implicit and explicit criteria palaeontologists used when discerning past diversity (see Fig. 1.4). It is generally agreed that evolution led to new genera at times of great environmental transition (Stanley, 1978). The concept ‘period’ is used by people differently: if the radiation of the Bovidae and of the Cervidae is linked to an event, then this is a frightfully long period (namely between 12 Mya and 17 Mya and – see above). MacFadden and Hulbert (1988) discussing the radiation of equids cast their net even wider and refer to a period between 8 Mya and 15 Mya of the Miocene for equid radiation (Fig. 1.1) (this is about twice the duration of the Pleistocene; the figure also shows how arbitrary such boundary dates are). The point for our discussion about whether Modern equids are some sort of pauperised reflection of the past is that at the peak of their diversity, there was a minimum of 19 species of equids (MacFadden & Hulbert, 1988). Between approximately 15 Mya and 7 Mya, there were always approximately 18 species after which it fell down to a few species only) (Hulbert, 1993 - At present there are minimally seven [E. hemionus, E. kiang, E. ferus, E. grevyii, E. burchellii, E. zebra, E. asinus] but perhaps some cryptic species within E. burchellii and E. hemionus). Hence it appears probable that at present there is real reduction in the number of species (although Hulbert’s figures are a bit misleading because he only focussed on American Equinae and so the Pleistocene drop is obscuring the subsequent radiation of Equus in Eurasia and Africa). Box 1.2 Taxonomy, or the Art of Giving Names to Forms of Equus: E. burchellii or E. quagga? We have given careful consideration to the issue of nomenclature, especially of Equus burchellii versus E. quagga, E. burchellii quagga or E. quagga burchellii. Likewise, with Equus caballus versus E. ferus, E. przewalskii or E. ferus przewalskii. Three issues play a role here, namely, (1) the rule of precedence in name-giving and (2) the rule of preventing confusion. The International Committee on Bionomenclature (ICB) has agreed in article 19.1 that ‘For purposes of priority the date of a name is either the date attributed to it in an adopted List of Protected Names (Art. 20) or, for unlisted names established prior to the relevant starting date for mandatory registration (Art. 5.2), the date on which it was validly published or became available under the relevant Special Code, or the date on which it was established, on or after that same date, under the BioCode’. Under this article, it could be argued that E. quagga has priority over E. burchellii; however, recommendation 19A.1 states that ‘Authors should follow the principle of priority also when it is not mandatory, unless the result would be nomenclaturally disruptive and contrary to established tradition’. We as editors, in close consultation with the authors of the diverse chapters in the book, have decided to follow this (continued)

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Box 1.2 (continued) recommendation because the nomen ‘quagga’ is synonymous with an extinct species (as is ‘dodo’) in normal language, and ‘quagga’ is not known in East Africa where hundreds of thousands Burchell’s zebra live. Over and above this is (3) the rule of approved registration (Article 20) which normally in Zoological nomenclature follows a revision of a whole genus. See the Greuter et al. (2011) of the ICB (see: http://www.bionomenclature.net/index.html). Because the BioCode has not yet been accepted everywhere, the rules of the International Commission on Zoological Nomenclature should be followed for mammals. Article 23 of that code also follows the issue of priority. Yet, Article 23.2 states that ‘in accordance with the objects of the Code (see Preamble), the Principle of Priority is to be used to promote stability and it is not intended to be used to upset a long-accepted name in its accustomed meaning by the introduction of a name that is its senior synonym or homonym (for certain such cases see Article 23.9), or through an action taken following the discovery of a prior and hitherto unrecognized nomenclatural act (such as a prior type fixation; for such cases see Articles 70.2 and 75.6)’ (see: https://www.iczn. org/the-code/the-code-online/). We, as editors, in consultation with the authors and the series editor have maintained E. burchellii as the name for the animal that is known as Plains zebra or Burchell’s zebra. We have also rejected names such as Grant’s zebra or Chapman’s zebra. Cladistically, E. quagga is even more alike E. caballus than as E. burchellii (Bennett, 1980). The issue with Equus caballus vs. E. ferus is even more confusing, and that arose because of an eighteenth C. habit of giving different Latin binominals to domesticated forms of a species and their wild (“ferus”) progenitors. Treating the domestic horse as a subspecies of the wild horse, and naming it E. ferus caballus, hollows out the concept of subspecies beyond biological acceptability. We think it is best to not use systematic categories (Latin trinomials) for animals that became feral (like the mustangs or perhaps the tarpans), following others but a formal decision has not been taken by the Nomenclature Commission (see Grubb, 2005). Finally, given the absence of an authoritative recent revision of the whole genus Equus, also in the light of modern genetics, we cannot give a verdict on whether the Przewalski’s horse should be seen as a subspecies of Equus ferus or as a separate species E. przewalskii (cf. Orlando et al., 2009). Note that this book is about ecology and evolution of equids, not about how many angels can dance on head of a pin. Evolutionary science shows us the prevalence of reticulate speciation, hybridisation and gene flow between taxa, whatever taxonomists try to endeavour by classifying organisms into discrete units. We have three propositions to explain the drop in the number of Equine species: (1) The number of species at present is underestimated: in reality there are ‘many’

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cryptic species in Burchell’s zebra and a few in kulan too, and so the number of Equus is just as many as at their peak; (2) The number of species in the past are exaggerated because palaeontologists do not appreciate enough about intra-specific variability, and so the number of Equus species is about equal to what it has always been; and (3) The number of Equus species at the moment is really seven, and palaeontologists discerned the correct number of species in the past at maximally nineteen. In that case there a now fewer species than in the past. Of course, it is impossible to discriminate between these three options well. The ambiguity, however, is enough to dispel the simple idea that the hind-gut fermenting equids (or tapirs and rhinoceroses) are ‘living fossils’ that should take their marching orders towards the exit of evolution. Perhaps the real question to ask is why the plethora of non-equid Equines (alphabetically, for example, Astrohippus, Cormohipparion, Dinohippus, Hipparion, Hippidion, Merychippus, Nannippus, Neohipparion, Onohippidium Pliohippus, Pseudhipparion, except Equus) (Hulbert, 1993) went extinct: but that cannot answer the question whether Equidae would be somehow ‘Modern Misfits’ because Equus did not go extinct. We posit that they are not, and much in the present book will show how well adapted the Modern equids are. To make the concept of ‘successfulness’ or lack thereof, even more difficult to handle is that some species groups show a very wide distribution, also seem to be amazingly adaptable but do not show much variability (Ricci, 1987; Judson & Normark, 1996). But apart from that, the equids and their ancestors were a North American group of species from the Eocene until the Pleistocene. Only during that last Epoch, did they spread into the Old World, that is Asia, Europe, and Africa, and to South America. In North America, they had occupied some ten million km2 (see Broughton & Weitzel, 2018). The cause of their extinction is not fully clarified yet, and the safest bet is a mixture of climate effects and people (Broughton & Weitzel, 2018). In South America, they occupied maximally some three million km2 (Villavicencio et al., 2019), an area that they ‘lost’ when E. neogeus, Hippidion saldiasi, H. devillei and H. principale went extinct recently, again probably due to humans and changes in climate (Villavicencio et al., 2019). When Equus entered Eurasia, their distribution became vast. The Eurasian Steppe is some eight million km2, the region between the Red Sea and Bangladesh some other four million km2 and equids may even have lived in the tundras. This vast steppic area was occupied by E. hemionus mainly but also by E. kiang and E. ferus. Zebras went into Africa. The savanna region is some 21 million km2, and this became the land of Cape zebra, Mountain zebra, Grevy’s zebra, Burchell’s zebra and African wild ass. Again, much of that distribution was lost due to human activity but that is beside the point: Equus lost about 13 million km2 in the Americas and gained 31 million km2 in Eurasia and Africa. Indeed, if the extent of distribution is a hallmark of success, the equids became even more ‘successful’ after they left the Americas.

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The Equids: A Successful Suite of Species This book is not about why Late Pleistocene and Early Holocene wild equids (Equus, Hippidion) went extinct. It is an interesting topic about which much speculation is possible depending on the discourse of the day. One can think of advanced story telling along the lines of ‘superiority of competing species’, ‘dominance by man-the-hunter’, ‘eradication by reckless indigenous people’, ‘climate change’ and even ‘their time had come’. Many of these story lines are driven by discourses in society at large, but the origin of these discourses hardly lies in the natural sciences but much more in politics and socioeconomics. What we know for certain is that many Late Pleistocene species went extinct (Fig. 1.5). All wild horses were gone from the Americas before the Modern day. In Europe, the wild horse was still reported in the Roman Era. The records of two Roman Emperors explicitly refer

Fig. 1.5 A subfossil ostrich eggshell from Western Sahara with markings depicting an animal in the likeness of a Mountain zebra, with tail to the left and head vaguely visible to the right. Epipalaeolithic stone tools (bifacial arrow points; grinding stones) and pottery associated with the find yield an estimate date of the eggshell as 8000 BP when there was a climatic optimum over much of the present-day Sahara. From this area, the now-extinct Equus mauritanicus (Saharan zebra) is known to have existed, which went extinct around 4000 BP. It was as large as the extinct Cape zebra E. capensis, which had an approximate body mass of 400 kg. Provenance: surface collection and shallow excavation near Tarouma (26o54276 N, 13o28835 W), in a private collection of original collector. Photo credit Jan H. Koeman

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to wild horses but also to onagers. Of Gordian I it was said in the Scriptores Historiae Augustae (written about 300 CE) that ‘There also exists today a remarkable wild-beast hunt of [Gordian I] pictured in Gnaeus Pompey’s “House of the Beaks”. . . in [which] two hundred stags with antlers shapes like the palm of the hand, together with stag of Britain, thirty wild horses, a hundred wild sheep, ten elks [moose], a hundred Cyprian bulls, three hundred red Moorish ostriches, thirty wild asses, a hundred and fifty wild boars, two hundred chamois, and two hundred fallow deer. And all of these to be handed over to the people to be killed on the day of sixth exhibition he gave’ (Magie, 1924, p. 385; emphasis added). When Emperor Gordian III was killed “there were thirty-two elephants at Rome in the time of Gordian . . . ten elk, ten tigers, sixty tame lions, thirty tame leopards, ten . . . hyenas, a thousand pairs of imperial gladiators, six hippopotami, one rhinoceros, ten wild lions, ten giraffes, twenty wild asses, forty wild horses, and various other animals of this nature without number. All of these Philip presented or slew at the secular games [after Gordian III was killed]. Gordian intended to [use them] for a Persian triumph” (Magie, 1924, pp. 443–445; emphasis added). We think these were onagers – not African wild ass because they were mentioned in relation to the Persian campaign. Could they have been European wild asses, so E. hydruntinus? The archaeological record seems to lead to the conclusion that this species went extinct around 600 BCE (Crees & Turvey, 2014) but, intriguingly, in the 18th C the species was reported to occur in Siebenbürgen (then Hungary; now Transylvania, Rumania) (Busching, 1761, p. 1042). In 1800, a picture was published (Fig. 1.6). The animal was not the same as the Kulan of Central Asia, which Busching (1761, p. 700) describes as Tschigiati for Irkutsk Province of Russia, as does L.M.H. (1798, p. 8). Similarly, it is not clear when the wild horse went extinct in Europe but fossil material that was ascribed to wild horses disappears from the record c. 3000 BCE (Sommer et al., 2011), even though this may have been only c. 2000 BCE in the Carpathian Basin (Németh et al., 2017). The species survived further East where open landscapes maintained themselves. L.M.H. (1798, p. 7) describes them as Dsheren occurring in Siberia sin the eighteenth C. Intriguingly, the St. Galler Handschrift with an early version of the Niebelungenlied describes in verse 3753 ‘Darnach scluoch er [Siegfried] sciere einen wisent un einen elch starcher uore viere und einen grimmen Schelch’. It is not clear what a ‘Schelch’ was and three possible translations have been suggested, namely, the extinct Irish elk (Megaloceros giganteus) or a wild horse or a male Elk (Moose; Alces alces) (Anon., 1892). The gift of Emperor Otto I in 943 to the Bishop of Utrecht (Netherlands) of what is now the Province of Drenthe (Netherlands) states ‘Nemo sine venia Balderici Episcopi in pago forestensi Trentano cervos, ursos, capreas, apros bestias, quae teutonica lingua Elo aut Schelo appelantur venerari praesumat’ (‘no one is allowed without permission of Bishop Balderic, to hunt in the wild lands of Drenthe red deer, brown bear, roe deer, and especially not those animals that are called Elo [wild boar] and Schelo in the German language’) (Anon., 1892; Schelo and Schelch are considered to refer to the same animal species). Survival of Irish elk into the Middle Ages is to be considered unlikely based on the fossil material (cf. Lister & Stuart, 2019) but that was not believed in 1892 either (Anon., 1892).

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Fig. 1.6 Intriguingly, there may be a reasonably reliable picture of the European wild horse (1) and the European wild onager (3) published in 1800 by Friedrich Johann Justin Bertuch (1747–1822) before they went extinct. There is no doubt that the now-extinct Quagga (6) is depicted reliably, and so are the Kulan or onager (2), the Mule (4) and the working horse (5). This plate is based on Bertuch (1792) but was published in the Netherlands (c. 1800), plate 30). By courtesy Mr. Peter Cornelissen of Pictura Prints, Art & Books, Overasselt, Netherlands

E. Hahn, in that debate of 1892, put forward that ‘schelo’ referred to a wild stallion (and in passing refers to Wild horses still in Germany in 1537) but others at that scientific meeting maintained that it referred to a male Elk (Moose). Yet, in the

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Benedictiones ad Mensa (‘prayers and blessing during eating’) of the monastery of St. Gallen from about 1040 CE, we know that besides many other wild animals, also brown bear (Ursus arctos), aurochs (Bos primigenius), wisent (Bison bonasus) and wild horse graced the monks’ table (Bächler, 1910). They were thus not extinct yet in Western Europe in the Middle Ages. References to wild horses from Poland together with Aurochs in Mazovia (part of present-day Poland) and wisent in what was then Lithuania are known for the eighteenth century (Büschings, 1768, p. 301). Wild horses also persist till the eighteenth century in Ukraine (Busching, 1761, p. 808). Both the European wild ass (onager) as well as the European wild horse were eaten by people, and the model of their extinction seems to be ever-increasing forests after the end of the last glacial period, and human over-consumption (Crees & Turvey, 2014; Sommer et al., 2011). It is not unlikely that the ‘grim schelchs’ were wild black horses, because this coat colour became dominant during the Holocene when European horses may have adapted to an ever-increasing forest cover after the last glacial period (Sandoval-Castellanos et al., 2017). Anyhow, instead of going the way of the dodo (Raphus cucullatus), the horse morphed itself successfully into the domestic form that many of us enjoy riding or watching today.

Perspective for the Ideas Reported in this Book So, while this book is not about the patterns or explanations of extinction, it is about investigating how wonderfully adapted the animals classified in the different species of zebras, kulans, kiangs, wild asses, and wild horses are. An important paradigm that we wanted to investigate in the book is the concept of ‘adaptive zone’ (see Box 1.3) because this has been all-pervasive in scientific analyses of the evolution of the equids but also of their functioning in the present world. Indeed, they are seen to be mammals that are adapted to live in open, arid habitats and that can thrive on low-quality, high-fibre foods such as grasses and other coarse and tough vegetation. But are they? Much of the information in this book, shows that their adaptations are much more flexible, and that they can also deal with high-quality food very well, and that they do not just live in open arid environments only. We invite you to read that yourself, and hopefully reform many of the opinions that you may have had. Indeed, one of the strangest diets we came across was from the Gulf States, when these were still poor, was donkey feed consisting of dates and dried fish (A.H.J. Prins, pers. comm. 1964) but mules surviving on rhododendrons at five thousand metre altitude (pers. obs. 2022) also falls outside of the expected. Modern palaeontological research shows that if this concept of ‘adaptive zone’ were valid, then these traits should have evolved simultaneously. It is becoming very clear that they did not (Cantalapiedra et al., 2017; Parker et al., 2018; Barrón-Ortiz et al., 2019; Janis & Bernor, 2019). This strangely echoes the deductions by Osborn (1902) who showed that ‘practically all the adaptations known among mammals have arisen by combinations of divergence independently pursued in the limbs and teeth; for example, an herbivorous tooth type may combine with a terrestrial,

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arboreal, or volant limb type, according as the search for plant food is on the earth, in the trees, or in the air. Although every imaginable combination (c.g., aquatic limbs, myrmecophagous dentition) cannot be realized, yet these combinations have been multiplied almost ad finitum’ (cf. Gordon & Prins, 2019). Box 1.3 ‘Adaptive Zone’ of Equus ‘An adaptive zone is defined in the literature as a particular mode of life or a unique ecological situation. This criterion has been used in the definition of our own genus, Homo. Specializations in body size and shape, locomotor behavior, rate, and pattern of development, among other traits, are argued to have allowed Homo to play a unique ecological role relative to other hominins. Therefore, these traits have been considered important in the delimitation of the genus Homo by some . . . In this context, the unique mode of life of extant equids could be defined as that of ungulate mammals that are adapted to live in generally open, arid habitats and that can thrive on low-quality, high-fibre foods such as grasses and other coarse and tough vegetation. Potential morphological adaptations for this mode of life comprise modifications of the locomotory and digestive systems. . Possible locomotor adaptations to living in open habitats include the elongation of distal autopodial bones as well as the development of monodactyly and the reduction or loss of metapodials II and IV; however, we note that alternative explanations for digit reduction have been proposed. . The enhanced development of the stay-apparatus, which allows the individual to conserve energy while standing, is also potentially an adaptation to living in open habitats. . Potential adaptations of the digestive system, particularly the dentition, to feeding on low-quality, high-fibre vegetation in open environments include: – increased crown-height of cheek teeth and incisors), – increased enamel complexity; including increased implications of the occlusal enamel – elongation of the protocones of the upper molars and premolars, – increased separation of the metastylid and metaconid, and enlargement of the metastylid to the point of being equal or subequal in size to the metaconid in the lower molars’. . Large body size. Source: Barrón-Ortiz et al. (2019). References were removed; see the source.

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Anyhow, the book is about adaptation and leavened by thinking along lines of natural selection (see Box 1.4) but tries to do that from the perspective of the whole animal. We must disagree with papers that analyse the adaptiveness of a single trait (like monodactyly) without considering that the toe is part of a living animal (e.g., McHorse et al., 2019) as Osborn (1910) emphasised in our opening quote (above). Yet, the paper of McHorse et al. (2019) very nicely shows how many ‘theories’ and ‘hypotheses’ have been formulated to ‘explain’ the morphology of the Modern equids, which – one after the other – have been refuted by evidence. Many Chapters in the present book will do that too. We do not have much hope that evidence will weed out hypotheses and theories though (Prins & Gordon, 2014a, 2014b), but as scientists who were trained in a Popperian approach we express the hope that this will be achieved. Box 1.4 An Uneventful Day in London One-and-Half Century Ago “first July 1858 was a fine summer day in London. The temperature in Hyde Park at 9 in the morning was 21 °C. There was a drought and a water shortage. The Globe Theatre advertised a diorama of the Indian Mutiny. The clipper Lonchiel sailed for Sydney, with an estimated voyage of 79 days. Parliament debated the Universities Scottish Bill and what W. S. Gilbert called ‘that annual blister, marriage with deceased wife’s sister’. Good progress was reported in laying the Atlantic Cable. Queen Victoria and the Prince Consort attended a performance of It Trovatore by the Royal Italian Opera Company. And at the Oval the Gentlemen made 158 against the Players [during a threeday cricket match], who replied with 103 for 4, after a stand by Wisden and Lillywhite. But one event on that day passed unrecorded in The Times for the following morning. At a meeting of the Linnean Society, Alfred Russell Wallace and Charles Robert Darwin presented a joint paper entitled ‘On the tendency of species to form varieties, and on the perpetuation of varieties and species by natural means of selection’. The paper was calmly received, and few of those who heard it could have predicted its subsequent impact upon scientific thought”. F.H.T. Rhodes (1966). Few biologists would consider the genus Homo, with currently only one species but with a near-worldwide distribution, as representing a declining clade where there was once a thriving diversity of related genera (Fig. 1.7). By the same token, it is a valid viewpoint, we think, to consider Equus a very successful genus where its ‘Bauplan’ has shed all superfluous, evolutionary less well-honed earlier forms that evolved during the Miocene. A genus that took over nearly the whole world, and when it was re-introduced in the Americas found its niches everywhere again. Anyone who has stood in awe amidst tens of thousands Burchell’s zebras on their migration in Serengeti, or who has seen kulan groups congregating in their

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Fig. 1.7 Hominin evolutionary tree. The enormous Pleistocene diversity of human-like species and even genera disappeared, and only one species in one genus (Homo) remained. Yet, Homo is not considered some sort of living fossil or evolutionary dead end. Source: Parins-Fukuchi et al. (2019). Courtesy of Cambridge University Press

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thousands in Dzungaria, or admired kiangs at altitudes were few animals can live, like we have, recognises a group of animals that are amazingly well adapted and can prosper if people allow them space. We hope that ecologists who study large mammals will refocus their attention on physiology, endocrinology, endothermy, morphology, careful diet studies and work on food quality, and especially on experimental studies again instead of working on habitat suitability modelling or restating generalities about ‘hypsodonty’, ‘hindgut fermenting’, which were the rage 20-odd years ago. But which are not sufficient to understand the success (or failure) of this wonderful suite of species that are each unique. This must be done within the context of the whole animal, including its behaviour (Box 1.5); perhaps there will be attention then for the Baldwin Effect (an organism’s ability to learn new behaviours [e.g., to acclimatise to a new stressor]) as a force to reckon with. This book, we believe, will help in reinvigorating the science of plant – animal interactions and the study of large mammals of which the equids form a splendid suite of species. Dedication This paper is dedicated to the memory of Richard E.F. Leakey who was fearless in his striving for the conservation of large mammals, and who famously brought to the attention that biodiversity is under threat now because of land hunger and poaching: conservationists should fight for that instead of worrying about climate change. That was not to be denied, he stated, but was a ‘three-hundredyear-from-now problem’ while extinction happens under our eyes now. Richard passed away on the January 2, 2022. We are grateful for what he did for wildlife. Box 1.5 Traits Need to Be Seen in the Context of the Whole, Living Animal, Including its Behaviour ‘Behavioural ecology needs the perspective of evolutionary ecology to move beyond speculative accounts of what may have happened in the course of evolutionary history. Accounts that use current observations to reconstruct the past action of natural selection are always problematic. If anything, back then was different from the way things are now, as it must have been, then even if a trait could have been the same back then, its ecological context was different. When it comes to behavioural traits, we cannot even tell how the trait was different back then, except by using comparative phylogenetic methods. Until someone discovers a fossil record for behaviour, we can in practice investigate only what are the ecological consequences of a trait now—that is, the evolutionary ecology of behaviour. . . . .. If there are any local rules of engagement in ecological communities, they are rules about how engagement changes in response to conditions. Curiously, this insight, at which ecology arrived through decades of measuring variation and population dynamics, is natural to anyone who observes behaviour, even though the study of dynamics is not explicit in many studies of behaviour. Watching animals in the field, what you see is behaviour [with u] (continued)

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Box 1.5 (continued) that changes in response to changing conditions. The ecological rules of engagement often change because of behaviour. Context dependence in ecology is produced by behaviour. Ecological interactions are influenced by behaviour, and behaviour responds to changing conditions’. D.M. Gordon (2011).

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Vrba, E. S. (2000). Major features of Neogene mammalian evolution in Africa. In T. C. Partridge & R. R. Maud (Eds.), The Cenozoic of southern Africa (pp. 277–304). Oxford University Press. Wake, D. B., & Hanken, J. (2004). Direct development in the lungless salamanders: What are the consequences for developmental biology, evolution and phylogenesis? International Journal of Developmental Biology, 40, 859–869. Wang, Y., Zhang, C., Wang, N., Li, Z., Heller, R., Liu, R., Zhao, Y., Han, J., Pan, X., Zheng, Z., & Dai, X. (2019). Genetic basis of ruminant headgear and rapid antler regeneration. Science, 364, eaav6335. Zurano, J. P., Magalhães, F. M., Asato, A. E., Silva, G., Bidau, C. J., Mesquita, D. O., & Costa, G. C. (2019). Cetartiodactyla: Updating a time-calibrated molecular phylogeny. Molecular Phylogenetics and Evolution, 133, 256–262.

Chapter 2

Evolutionary Radiation of Equids Juan L. Cantalapiedra, Oscar Sanisidro, Enrique Cantero, Jose Luis Prado, and María Teresa Alberdi

Abstract Horses became ubiquitous elements of Cenozoic communities and reached high diversity in Neogene times. Most accounts of their diversification history have so far focused on the Early Miocene cladogenesis of the subfamily Equinae (the so-called “grazing horses”), interpreting raw diversity counts at face value. In this chapter, we reconstruct speciation and extinction in horses, while accounting for sampling biases, and interpret these trends in the context of the evolution of body size and relative tooth crown height (hypsodonty). We found that fast species proliferation (speciation rate) is a shared feature in anchitehres and equines, likely stemming from the more changeable environments of the Neogene. The fast early-phase radiation in the subfamily Equinae was likely the result of reduced extinction rates and higher lineage survival rather than a substantial acceleration in speciation. The evolution of body size and hypsodonty was not faster in regions of the phylogeny with faster diversification, suggesting a broad-scale decoupling of ecomorphological and taxonomic diversification. Our models show that major phenotypic trends were not caused by phyletic progression, derived from sustained, ubiquitous directional selection, but more likely was the outcome of differential lineage-level survival and multiplication (species sorting).

Supplementary Information The online version contains supplementary material available at https://doi.org/10.1007/978-3-031-27144-1_2. J. L. Cantalapiedra (✉) · O. Sanisidro Departamento Ciencias de la Vida, GloCEE Global Change Ecology and Evolution Research Group, Universidad de Alcalá, Madrid, Spain E. Cantero · M. T. Alberdi Departamento de Paleobiología, Museo Nacional de Ciencias Naturales (CSIC), Madrid, Spain J. L. Prado INCUAPA, CONICET-UNICEN, Universidad Nacional del Centro de la Provincia de Buenos Aires, Olavarría, Argentina © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 H. H. T. Prins, I. J. Gordon (eds.), The Equids, Fascinating Life Sciences, https://doi.org/10.1007/978-3-031-27144-1_2

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Introduction Living horses belong to the genus Equus, the only surviving branch of the horses’ evolutionary tree. The current diversity of horses, 7 species, is tiny in comparison to the more than 200 species that have been described in the fossil record. Despite their recent decline, horses were among the most abundant large mammals in Cenozoic assemblages (MacFadden, 1998). The abundance of North American horse findings through the nineteenth century inspired prominent scholars to erect the classic orthogenetic sequence of horse evolution: from the small-sized Eohippus through Mesohippus (and others) up to the living Equus (Marsh, 1879), a story still resounding in the social imagination, as well as in academic and education texts. This classic hypothesis involves a progressive increase in body mass, a gradual increasing slenderness of the limbs adapted to open habitats, and the development of more complex teeth to deal with abrasive grasses in the diet. The current knowledge of the family reveals a much more complex scenario characterized by consecutive evolutionary radiations. The family Equidae is one of the three surviving lineages of the Order Perissodactyla, or “odd”-toed ungulates. Perissodactyls are classically divided into two main groups: Ceratomorpha, comprising living tapirs and rhinos, and Hippomorpha (here regarded as equivalent to Equoidea), currently restricted to living horses (Fig. 2.1). The reconstructed split between ceratomorphs and hippomorphs took place at about 56 Ma, no later than the Paleocene-Eocene boundary (Bai et al., 2018), but the first perissodactyls could have arisen somewhat earlier, during the Paleocene times in Asia (Hooker, 2005). Equids have been classically clustered together with chalicotheres, brontotheres, and palaeotheres within the Hippomorpha (for a comprehensive review of perissodactyl classification see ref. McKenna et al., 1989). However, posterior assessments of the evolutionary relationships among perissodactyls have yielded conflicting results, and the current definition of Hippomorpha is now much more restrictive, not always including brontotheres or chalicotheres (Hooker & Dashzeveg, 2004; Bai et al., 2018). True horses, members of the family Equidae (or ‘equids’), arose in North America shortly after the Paleocene-Eocene boundary, at around 55.5 Ma (Froehlich, 2002). The earliest Equidae share many diagnostic traits (synapomorphies) with primitive representatives of other perissodactyl lineages (i.e., they are all small, have four-toed forefeet, and low-crowned dentition) but lack many of the highly derived characters of latter species, complicating the recognition of common traits to all Equidae (Hooker, 1989). The Late Eocene saw the evolution of a new type of horse featuring three toes and ectolophodont teeth (those with a dominant buccal cutting edge) devoid of cement (Fig. 2.1). These forms (Mesohippus and Miohippus) are the first representatives of the subfamily Anchitheriinae (here referred to as “anchitheres”) (MacFadden, 1998), which later were involved in the first relevant event of horse diversification in Miocene times (see below). Neogene anchitheres were the first known horses to venture outside of North America. Miocene anchitheres include two groups of species. The first group is the tribe

Evolutionary Radiation of Equids

Fig. 2.1 Phylogenetic position of horses among perissodactyls (Froehlich, 2002; Chimento & Agnolin, 2020) and main evolutionary relationships within the horse family (Equidae) (MacFadden, 1998; Froehlich, 2002; Janis & Bernor, 2019). Major phenotypic breakthroughs are highlighted. Vertical extension of gray triangles represents species diversity in subclades. Note how Anchitheriini, Equinae, and the clade defined by Equinae and the “stem equine anchitheres” (Archaeohippus, Desmatippus, and Parahippus) are monophyletic, whereas Anchitheriinae is paraphyletic. Relevant events (Damuth & Janis, 2011; Mihlbachler et al., 2011; Strömberg, 2011; Semprebon et al., 2016; Juan L Cantalapiedra et al., 2017) are shown with color bars on the temporal axis. Pli.: Pliocene, Pl.: Pleistocene, Ma: million years ago

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Anchitheriini (known as “Anchitheriinae sensu stricto,” or “anchitherines”), which forms a monophyletic group, this is, a set of lineages defined by an ancestor and all of its descendants. The second group of anchitheres is the “stem equine anchitheres.” These are not an evolutionary enclosed set of species like the Anchitheriini, but rather form a set of successive splits that eventually gave rise to the most specious subfamily of horses, the Equinae (Fig. 2.1). Since Equinae is not included in the Anchitheres, the “stem equine anchitheres” form a paraphyletic group, since it is defined as an ancestor and just some of its descendants (see Fig. 2.1). This is also true for the whole Anchitherinae subfamily (see Fig. 2.1). In some cases, the stem equine anchitheres already had grass-rich diets (Semprebon et al., 2016), and an increase in molar crown height (Semprebon et al., 2019), as well as the development of the more efficient “spring foot” that resulted from substantial modifications of the limbs (Janis & Bernor, 2019). During the late Early Miocene, between 19 and 16 Ma, the fossil record captures the radiation of the subfamily Equinae (here referred to as “equines”). The genus Merychippus, a primitive equine, already shows high-crowned, plagiolophodont cheek teeth (this is, columnar teeth with a flatten occlusal surface). From the Merychippus, three tribes evolved: Hipparionini, Protohippini, and Equini (here also called “hipparions” or “hipparionins,” “protohippins,” and “equins”). Hipparionini horses were a successful and diverse radiation of equids, dominating Miocene mid-size herbivore guilds for ten million years. In contrast to modern equine horses, all hipparionins have three functional digits. Monodactyly evolved in equines in the Late Miocene and Pliocene, in genera such as Pliohippus and Dinohippus (Parker et al., 2018) (the lineage that eventually led to the genus Equus), and in Hippidion (close relatives of Equus that dispersed into South America). The first hipparionin and equin horses, with features related to grass-dominated diets, such as fully hypsodont molars and an elongated rostrum (i.e., the longirostrine forms), occurred at the middle Miocene, between 15 and 14 Ma. While hipparionins mitigate tooth wear by increasing enamel complexity (Famoso & Davis, 2014), Equini overcame it by means of taller crowns (higher hypsodonty). Significantly, such an increase in hypsodonty is somehow delayed in relation to the expansion of grass-dominated landscapes in North America (Mihlbachler et al., 2011). Equini lineages differ from other members of the Equinae subfamily in the very highcrowned (hypsodont) teeth with simpler enamel patterns than that of hipparionin horses, but with cross-linked enamel ridges that allow for high wear resistance (Famoso & Davis, 2014). The fossil record of horses is dense and well-studied and has provided deep-time perspectives on the evolutionary and biogeographic history of this clade. Importantly, fossil horses have been inspirational in the development and testing of evolutionary theory related to phenotypic evolution and diversification. Examples include the testing of notions built around phyletic progression (Cope, 1886; Stirton, 1947), the role of adaptive zones in macroevolution (Simpson, 1944), the quantitative study of evolutionary radiations (MacFadden & Hulbert, 1988; Hulbert, 1993), as well as pioneering assessments of evolutionary rates, and the identification of macroevolutionary optima using phylogenetic data (MacFadden, 1985; MacFadden,

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1986; MacFadden, 1988; Hansen, 1997). Recent investigations, in a broad array of ecological and evolutionary venues, have, to a certain degree, reshaped what we knew about horses’ evolution from classic theory. These advances have drawn on expanded data availability, higher temporal resolution of the fossil record, and new quantitative methods, which have provided a new look at the paleobiology and macroevolution of the horse family regarding aspects such as diversification, phenotypic evolution, and dietary shifts (Mihlbachler et al., 2011; Shoemaker & Clauset, 2013; Tütken et al., 2013; Semprebon et al., 2016; Juan L Cantalapiedra et al., 2017; McHorse et al., 2017; Parker et al., 2018; McHorse et al., 2019), just to mention a few. The current Book focuses on the ecology and evolution of the living representatives of the horse family and in this Chapter, we will investigate the diversification and evolutionary processes that shaped the broader patterns of equid diversity. Although the multiplication of horse lineages is usually regarded as a remarkable feature of Cenozoic mammalian evolution, the truth is that quantitative accounts of their diversity and diversification trends are very scarce and have mainly focused on the subfamily Equinae (MacFadden & Hulbert, 1988; Hulbert, 1993; Juan L Cantalapiedra et al., 2017). Furthermore, thus far, no quantitative diversification assessment, that accounts for sampling biases, has been attempted in this group. In this Chapter, we assess the diversification dynamics (i.e., speciation and extinction rates over time) in this emblematic lineage using procedures that control for sampling biases. To frame the reconstructed diversification patterns in the context of phenotypic change, we also assess the mode of evolution in body size and hypsodonty index using phylogenetic methods.

The Data Our analyses encompass all the species of the family Equidae. We gathered occurrence information from the New and Old World (NOW; https://nowdatabase.org) database and the Paleobiology Database (https://paleobiodb.org). The resulting dataset was revised for taxonomic consistency according to an exhaustive survey of the recent literature, yielding a total of 234 horse species, which is a conservative figure compared to that obtained from a literal reading of databases and publications. For each species, occurrences were evaluated to avoid duplicates coming from different sources of information. Given the impact of temporal – i.e., stratigraphic – precision of occurrences on the estimation of diversification rates, we further reviewed the paleontological and geological literature to increase the precision of temporal information. The resulting dataset contains 2975 occurrences. We used an occurrence-based method (Silvestro et al., 2019) to estimate speciation and extinction rates through time. This approach simultaneously estimates sampling rates, that is, the rate at which lineages (here species) produce occurrences that make it into our database (and are analyzed). Thus, our approach is robust with respect to temporal sampling heterogeneity and across-lineage sampling variation.

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We separately analyzed three major sets of species based on ecomorphological and taxonomical affinities. In the first set, here called “basal horses,” we include all species not included in Anchitheriinae and Equinae. Examples of genera included in this group are Arenahippus, Pliolophus, Xenicohippus, Eohippus, and Minippus. The resulting “basal horses” set includes 22 species spanning most of the Eocene. The subfamily Anchitheriinae (“anchitheres”) comprises 60 species (in genera such as Mesohippus, Miohippus, Desmatippus, Archaeohippus, Parahippus, Kalobatippus, Megahippus, Anchitherium, etc.), spanning from the Late Eocene to the latest Miocene, and making a second paraphyletic set of species (see Fig. 2.1). Finally, the subfamily Equinae (here referred to as “equines,” and including merychippines, hipparionins, protohippins, and equins), with 152 species spanning the last 19 million years, defines a third monophyletic set (see Introduction). Additionally, we analyzed stem equine anchitheres (Desmatippus, Archaeohippus, and Parahippus) together with Equinae, which also conform to a monophyletic set (Fig. 2.1). To assess the mode of evolution of body size and hypsodonty, we used an approach that combines trait information and phylogenetic trees. Body size and hypsodonty data were gathered from several published sources (MacFadden, 1986; MacFadden, 1998; Mihlbachler et al., 2011; Shoemaker & Clauset, 2013; Juan L Cantalapiedra et al., 2017) (see also references in (Juan L Cantalapiedra et al., 2017)), with additional measurements based on our own observations, as shown in Table S1. Body size was estimated using Damuth’s equation based on M1 area (Damuth & MacFadden, 1990). When M1 measurements were not available, we used m1 and its corresponding Damuth’s equation for body mass. Hypsodonty scores were obtained by measuring unworn teeth. Although our priority was to measure M1, information had to be obtained from M1, M2, and M3 in some instances (Table S1). Averages were used when more than one specimen was available. A complete tree for all 234 species of horses was assembled following an informal supertree approach that integrates current understanding of evolutionary relationships within the group (MacFadden, 1998; Juan L Cantalapiedra et al., 2017). The supertree was translated to topological constraints in MrBayes (Ronquist et al., 2012; J. L. Cantalapiedra et al., 2019), and tips were assigned the age of their oldest occurrence. This approach is flexible since it allows for multiple solutions in regions of the tree where the topological scaffold shows polytomies. The MrBayes analysis was run for 50 million generations and sampled every 10,000 generations. We discarded the first 20% iterations at the beginning of the Markov Chain Monte Carlo run to ensure a favorable starting point. From the resulting trees, we retained 100 topologies without zero-length branches to ensure proper fitting of maximum likelihood models.

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Early Diversification After a brief spike in speciation rates, the diversification of basal horses featured constant speciation and extinction. Both rates show highly overlapping values and 95% highest posterior densities (HPD) (Fig. 2.2), suggesting high volatility and species replacement. As a result, diversity in these lineages never really ramped up, showing an early peak in the Early Eocene (Fig. 2.2). The decline in diversity of these basal horses started around 45 Ma, around the beginning of the Middle Eocene, and was the result of decelerating speciation rates and not of peaks in extinction. This outcome suggests that environmental changes (imposed by the progressive global cooling and the new tectonic settings of the Eocene) hampered the ability of basal horses to produce new species, either because of the contraction of their adaptive landscape, or by the saturation of their niches by other small-to-middle-sized ungulates. Since the decline was taking place well before the Eocene diversification of the anchitheres around 40 Ma, it is plausible to assume that such competition would have come from lineages outside the horse family.

The Anchithere Radiation Anchitheres appeared during the Late Eocene, around 40 Ma. We identify two diversity peaks in this subfamily, the first of which was reached around 34 Ma (Fig. 2.2), because of early fast diversification in the group. From then on, diversity slightly decreased until the Oligocene-Miocene boundary. Neogene anchitheres represent a clear example of early-phase radiation: for eight million years they show sustained, high species proliferation (an average rate of 0.42 events per million species year, E/MSY, between 25 and 17 Ma), which is responsible for a maximal diversity peak of 16 species around 15.5 Ma. This remarkable finding shows that early-phase radiation is not a feature unique to equines (species in the Equinae subfamily), a classic example of evolutionary radiation within the horse family. The magnitude of early species proliferation in anchitheres is, however, lower than that estimated for the earliest radiation of Equinae lineages (average 0.73 E/MSY between 19 and 16 Ma; but see further discussion below). Nevertheless, the duration of this early-phase radiation event in anchitheres spans more than a third of their evolutionary history, revealing that anchitheres prospered in the conditions brought about by the new terrestrial regimes of the earliest Neogene (enhanced seasonality and habitat heterogeneity, among others) (Eronen et al., 2010), and were highly successful in terms of species production. From 15 Ma onward, anchitheres underwent a marked decline that featured reduced speciation and accelerating extinction (Fig. 2.2). Their x-shaped speciation and extinction trajectories over time observed in Neogene anchitheres (Fig. 2.2) represent a near-perfect example of the expected behavior of clades under a waxand-wane scenario, where extinction progressively increases as the environment

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Fig. 2.2 Diversification and diversity patterns in horses. The left column shows speciation and extinction rates over time. Note that the y-axis is log-scaled. Rates for alternative groupings of species are shown in dashed lines. The right column represents species diversity over time, after

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(extrinsic conditions, including biotic interactions) deteriorates over time (Quental & Marshall, 2013). Neogene anchitheres’ diversity over time follows a hump-shaped profile, which confirms that anchithere diversification trends perfectly fit a modellike scenario (Fig. 2.2).

A New Look at Early Equine Radiation As mentioned above, Equinae lineages show very high speciation and low extinction between 19 and 16 Ma. As a result, we reconstruct an averaged net diversification rate (r) of 0.58 E/MSY during this period for equine lineages. To put this in context, equine diversity doubled every 1.2 Myr (doubling time, t2 = log(2)/r) (Stanley, 1979), on average, during that diversification burst. From 16 Ma, speciation remained nearly constant (0.265 E/MSY) for the rest of the studied period. Changes in diversification in equines were thus determined by fluctuations in extinction rate (Hulbert, 1993). Extinction remained nearly constant until around 5.7 Ma, doubling as compared to Miocene values, thereafter. This increase in extinction rate marked the beginning of the equine decline since net species production (speciation minus extinction) has been negative ever since. This means that equine lineages underwent positive diversification between approximately 19 and 6 Ma, 70% of their history. Around 370 kya, extinction skyrocketed to unprecedented levels (2.84 E/MSY) (Fig. 2.2). The magnitude of the ongoing extinction event is maybe better put in this way: the average probability of surviving this brief regime (during the last 0.37 Myr) is just 35% for a given lineage. This sharp extinction pulse contrasts with the smoother waning of diversity of basal horses and anchitheres, emphasizing that, as for other mammalian lineages (Juan L. Cantalapiedra et al., 2015; Silvestro et al., 2015), the Middle to Late Pleistocene brought an unprecedented pace of diversity loss in horses. The age of this extinction shift predates the presence of modern human populations in all the continents except Africa, pointing to environmental perturbations brought about by the onset of the Late Quaternary fluctuating climate regimes as the most probable trigger of the last equine decline. With around 150 species, the subfamily Equinae triples the diversity of Neogene anchitheres (comprising 46 species). Most of the research conducted to explain the success of equines in terms of diversification and species diversity has focused on the sudden bloom of equine species during the Early Miocene, between 19 and 16 Ma. So much macroevolutionary relevance has been attributed to this event that other interesting features of equine diversification have been overlooked. Our analyses provide new perspectives into its macroevolutionary context and magnitude. > ⁄ Fig. 2.2 (continued) taking shifting sampling and occurrence age uncertainty into account. In all plots, shaded areas represent 95% highest posterior density (HPD). In the diversity profile of “stem equine anchitheres + Equinae,” a salmon-colored curve represents an exponential model (with intrinsic growth rate, r = 0.23) fitted to diversity values between 24 and 15.5 Ma

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We observe that rather than being an outstanding episode, the early equine radiation forms part of a continuous process. Quantifying diversification is a powerful tool in paleobiology because it can reveal simple mechanisms behind dramatic evolutionary events (Sepkoski, 1978). The study of macroevolution uses per-capita rates (events per lineage per unit of time, here E/MSY or events per million species years) to express the magnitude of the speciation and extinction process (birth-death process). It is important to note that a constant positive per-capita diversification rate translates into an accelerated total rate of diversification, as the number of lineages increases due to the multiplicative nature of the model (Sepkoski, 1978). Such processes result in the exponential patterns observed when diversity accumulates over time. Also, the model-based approach used here captures the randomness (stochasticity) inherent to diversification processes in natural systems (Silvestro et al., 2019). For example, simulating diversity trajectories under constant and identical diversification rates will yield very different outputs across simulations (Raup et al., 1973). Further, many factors obscure the underlying biological signal that we see in the fossil record. Changes in diversity are a result of changes in speciation and extinction but also changes in sampling rates. If changes in sampling are overlooked, these could distort diversity curves and diversification assessments. Finally, the age uncertainty typical of fossil sites must be accounted for. Our diversification modeling accounts for all these biases and allows for a fair assessment of the magnitude of the Early Miocene Equine radiation. When analyzed in isolation, the early radiation of equines shows the appearance of 5 lineages in a short period of time (Fig. 2.2) (Juan L Cantalapiedra et al., 2017), and thus requires a marked speciation peak to explain that diversity. However, when the diversification of Equinae is analyzed together with its stem taxa – the so-called “stem equine anchitheres” (Archaeohipppus, Desmatippus, and Parahippus) a set of anchitheres placed at the base of Equinae, also conforming a monophyletic group with equines (Janis & Bernor, 2019), we observe that the speciation rate of the resulting group remains at an average of 0.45 E/MSY between 24 and 16 Ma (Fig. 2.2, bottom of the left column). This is still an extraordinarily high speciation rate that was maintained over eight million years (net diversification 0.225 E/MSY; i.e., diversity is expected to double every 1.34 Myr). But the important point is that our model does not require a shift toward higher speciation between 19 and 16 Ma to explain the Early Miocene Equine radiation. To help the reader visualize this, we plotted the estimated diversity of this clade (Fig. 2.2, bottom of the right column) and fitted a simple exponential regression that models the reconstructed diversity between 24 and 15.5 Ma as a function of time: Nt = N0 e rt, where Nt is the number of species at time t, t is the spanned time in Myrs, N0 is the diversity at the beginning, and r is the intrinsic diversification rate, measured as the average net number of lineages produced by each lineage per unit of time. We also use the linear formulation: log Nt = log N0 rt (Sepkoski, 1978). Both formulations have only one parameter, r. The linear model yields a r of 0.220, and tightly tracks the diversity trend of the lineage (R2 = 0.989). The exponential formulation (run with the nlsLM function in the R library minpack.lm) yields a r of 0.230 (see Fig. 2.2). The averaged r (speciation minus extinction) under PyRate for that interval is 0.220 E/MSY. This

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does not mean that there was not an acceleration of diversification in basal equine lineages. Rather, it shows that the radiation event of the equine horses between 19 and 17 Ma falls within the expectation of a constant, more conservative diversification model, given the changes in sampling probability over time, the stochasticity implicit to birth/death processes, and its multiplicative nature. Part of the reason why this departure was identified as an event stems from a literal reading of the fossil record (e.g., using raw species counts for estimating rates) (MacFadden & Hulbert, 1988). But the critical period that we investigate (between 24 and 16 Ma) spans through time periods with different sampling potential. Our diversification model and diversity reconstruction were set so that they allowed sampling rates (ψ) to be different between time bins defined by North American Land Mammal Ages (NALMA stages). The sampling rate in the early Late Arikareean (before 19.5 Ma) was low (ψ -19.5 = 0.94 E/MSY), but it increased four times during the late Late Arikareean (between 19.5 and 18.8 Ma; ψ 19.5–18.8 = 3.83 E/MSY). The Early Hemingfordian (between 18.8 and 17.5 Ma) saw further increase in sampling rates (ψ 18.8–17.5 = 5.33 E/MSY). This means that one lineage of 1 Myr of duration is expected to have a probability of 0.61, 0.98, and 0.99 of being sampled once in each of these periods (a total 60% increase). Short-duration lineages would have seen an even higher multiplication of the odds of being sampled (for a 0.5 Myr lineage: 0.37, 0.85, 0.93; a total 150% increase). Thus, the exponential increase in species diversity of the clade, including stem equine anchitheres and equines, during this interval was coupled with increasing chance of lineages and ecosystems leaving a trace in the fossil record in the most recent beds, and a higher probability of paleontologists finding fossil horses in those beds and publishing about them. Together, these dynamics interwove and resulted in a disproportionated acceleration of diversification when the fossil record is read at face value. Although our arguments may have convinced the reader of the usefulness of accounting for sampling biases while acknowledging the nature of exponential trends, we still have not explained why the diversity of equines triples that of Neogene anchitheres. If we focus on the growth phase of anchitheres and equines (the interval when net diversification is positive), we can estimate average speciation and extinction for both groups. Neogene anchitheres show an average speciation of 0.41 E/MSY, whereas equines—even acknowledging their early speciation peak at 0.73 E/MSY—speciated at an average 0.37 E/MSY during their rise phase, a 10% slower rate. The extinction severity in anchitheres and equines during their rise phase, however, shows a crucial difference. Average extinction during this phase in anchitheres and equines was 0.26 and 0.18 E/MSY, respectively. This shows that anchithere diversity attrition was 43% faster than in equines, stressing the important role of differential species survival in macroevolutionary dynamics. However, we could follow a conservative approach and assume that equine speciation and extinction rates estimated between 19 and 16 Ma are over- and underestimated respectively (due to sampling and a truncated approach, as previously explained). But even if the net diversification of equines was more like that of anchitheres during the expansion phase, there are still differences among the two groups. First, equine diversification remained positive for longer (70% of their evolutionary history, until around 6 Ma).

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In anchitheres, on the other hand, diversification rates remained positive until 16 Ma, after 45% of their evolutionary history. Further, an inspection of the decline phase of the two subfamilies shows that net species loss was faster in anchitheres (-0.185 E/MSY) than in equines (-0.084 E/MSY; discarding the almost-catastrophic collapse in the Late Quaternary). Equine lineages underwent a longer expansion phase that allowed them to reach a global diversity of nearly 40 species around 7 Ma. Anchitheres, however, reached a maximum of around 20 species 16 Ma, and 10 Myr later they were all gone. The striking differences in diversity trends between coeval anchitheres and equines do not require an extraordinary early radiation event of the latter to be explained. Rather, the macroevolutionary success of equines arises from their capacity to keep extinction at bay for a longer period. A milder decline phase also ensured a longer duration of the clade (which provides further time for species production) (Raup, 1991), at least until their unexpected collapse in the Late Quaternary.

Body Mass and Hypsodonty Evolution in Horses The radiation of horses has been traditionally linked to phenotypic evolution. First, because under classic views speciation went hand in hand with phenotypic progression (Osborn, 1902; Stirton, 1947). Simpson’s ideas (Simpson, 1944) reframed this connection: phenotypic innovations allow lineages to enter previously unattainable adaptive zones. Entering new—sometimes unexploited—adaptive landscapes releases diversity limiters, for example by ameliorating competition and increasing the available resources (Marshall & Quental, 2016). An empty adaptive zone provides further opportunities for adaptation, enhancing phenotypic evolution while rendering a multiplication of lineages. Attaining the equine stage is considered a phenotypic milestone in horse evolution (Fig. 1.1). The Equinae family showed the evolution of plagiolophodont molars from the ectolophodont type that characterized anchitheres, as well as substantial modification of the foot in some lineages (see Fig. 1.1 for a representation of such evolutionary changes). The plagiolophodont tooth type allowed for a higher plasticity of the relative crown height (hypsodonty index), which is usually interpreted as an adaptation to harsher grass-dominated diets (and the increased intake of silica phytoliths associated to it), or other abrasive exogenous particles (Semprebon et al., 2019), because taller cheek teeth will last longer under severe attrition (Damuth & Janis, 2011). It also offers biomechanical advantages (Solounias et al., 2019). Early equines (e.g., Merychippus) already present relatively tall dentition in comparison to more ancestral forms, together with a modified pattern of mastication dominated by an anterior-posterior direction of movement (Rensberger et al., 1984). The spread of grasslands in North America during the Early Miocene would have provided the new adaptive arena that explains these adaptations, and the onset of the phenotypic

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breakthroughs brought by equine lineages would have fueled the equine adaptive radiation as a response to the new evolutionary opportunity. However, more recent findings that make use of updated datasets and quantitative methods have challenged the idea of an adaptive radiation at the base of Equinae around 18 Ma. First, it seems that grass-dominated habitats were already common in North America by 25 Ma, around seven million years before the onset of Equinae (Strömberg, 2011), or even earlier (Retallack et al., 2002). In fact, anchitheres show a wide variety of grass content in their diets even in the earliest Miocene, including many examples of pure grazing species (Semprebon et al., 2016), meaning that anchitheres were already in the new adaptive zone despite their short-crowned cheek teeth. Moreover, phenotypic evolution does not seem to fit the adaptive radiation scenario, which predicts accelerating phenotypic evolution during the early phase when lineages are multiplying faster, showing complex patterns instead, with factors such as biogeographic dispersals playing a key role (Juan L Cantalapiedra et al., 2017; McHorse et al., 2019; MacLaren, 2021). To give a phenotypic perspective to the diversification trends described in the previous section, we built models of phenotypic evolution using the phylogenetic tree of the horse family. In particular, we use a phylogenetic approach that allows us to simultaneously model the evolution of body size and hypsodonty, while accounting for their potential correlates (as implemented in the R package mvMORPH) (Clavel et al., 2015). Our analyses assess body mass and hypsodonty evolution as continuous variables. Here body size is log10- transformed, so that evolutionary rates reflect relative changes independent of the mass. This happens because the sum of the logarithms of two numbers is equal to the logarithm of the product of the two numbers. Let us imagine two species, with a mass of 10 and 1000 kg. If we do not log-transform the data and we estimate an evolutionary rate of 10 kg per million years (Myr-1), the expected change for the smaller species is huge (doubles or halves its size every Myr), whereas it only entails a 1% change for the larger species. In a log10-scaled analysis, these species will weigh 1 and 3 log10 units. Now, imagine that we estimate a rate of 0.0414 log10 units Myr -1. For the small species, 1 + 0.0414 in log10 scale means log10 (10) + log10 (1.1), which can be expressed as log10 (10 × 1.1). The same occurs to the 1000 kg species, since the rate would translate into a change of log10 (1000) + log10 (1.1), which is the same thing as log10 (1000 × 1.1). This means that summing/resting 0.0414 in log10 scale is the same as multiplying/dividing by 1.1, or to increase/decrease ~10%, independently of the size. Although body mass and hypsodonty represent just two of the many dimensions that define the ecomorphology of the horse family, we focus on them since they are available for a large proportion of species, and because many studies have stressed their evolutionary relevance (Simpson, 1944; MacFadden, 1986; Hulbert, 1993; Hansen, 1997; Mihlbachler et al., 2011; Juan L Cantalapiedra et al., 2017). We ran different models where different lineages of horses were able to evolve in different fashions (Table S2). Each model was run on 100 trees, and the different parameters were averaged across trees. The goodness of fit of the models (i.e., how good a model is at explaining the observed data) was assessed by their corrected Akaike

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Information Criteria (AICc) score, which penalizes the complexity of the model. Our models divide the tree in two or three partitions based on species sets defined above: Paleogene horses (now including Mesohippus and Miohippus), Neogene Anchitheriinae and Equinae. For comparison, we also built models where stem equine anchitheres and Equinae (called Pan-Equinae in Table S2) share the same mode of evolution. Other partition configurations included scenarios where lineages evolved differently in and outside of North America and other models where lineages evolved differently before and after 25 Ma (marking the onset of Neogene conditions in terrestrial ecosystems, including widespread grass-dominated landscapes). Once the different partition systems are defined, we can ask in which mode each of these regions of the horses’ tree evolve. A first family of models depicts scenarios where lineages evolve under unconstrained evolution (the so-called “brownian motion,” BM, where lineages are free to evolve across the ecological morphospace defined by body mass and hypsodonty index). Under our BM models, each partition can evolve at a different pace (i.e., has different evolutionary rates). A second family of models allows each partition to evolve at different rates but also under different selection pressures, this is, following a model where each set of lineages are “attracted” toward an optimal phenotype (Hansen, 1997; Benson et al., 2014) (the so-called “Ornstein–Uhlenbeck” models, OU). Within the OU models, a given selection regime could imply phenotypic stasis (lineages show constrained evolution and are unable to explore different regions of the bidimensional ecomorphological space), or that lineages are actively evolving toward a new region of the ecomorphological space (a phyletic trend stemming from sustained selection). The latter scenario could be equivalent to Simpsonian notions of lineages invading different adaptive regions (Simpson, 1944). A third family of models allows a given partition to follow an accelerating or decelerating evolutionary rate (ACDC models). We integrated different partition schemes with different combinations of BM, OU, and ACDC models to build a total of 21 models (Table S2). The best model recognizes three partitions, with differential rates of evolution in Paleogene horses, Neogene Anchitheriinae, and Equinae, and unconstrained evolution (the BM model). According to our best model parameters, body mass evolutionary rates were 0.021 log10(kg) per million years (Myr-1) for Paleogene horses, and close to 0.015 log10(kg) Myr-1 in Neogene Anchitheriinae and Equinae. Since our phylogenetic modeling was conducted on log10-transformed mass, these correspond to expected changes of 5% and 3.5% of the body mass per million years. This means that rates of body mass evolution were higher in the less diverse Paleogene lineages, and that body size evolved at a similar pace in anchitheres and equines. For hypsodonty, evolutionary rates in Paleogene horses, anchitheres, and equines are 0.011, 0.004, and 0.298 Myr-1, respectively. Changes in molar crown height were faster amongst basal lineages of the Paleogene than in Neogene anchitheres. Equinae lineages show a marked increase in the rate of hypsodonty evolution, likely resulting from the many craneo-dental changes (including the development of plagiolophodont teeth) that allowed the accommodation of diverse degrees of hypsodonty in different lineages.

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One interesting aspect revealed by our phylogenetic approach is that the three major lineages did not evolve toward adaptive peaks, that is, they were not under sustained selective pressures that drove them toward certain regions of the bidimensional morphospace. Models where widespread active phyletic trends are implemented show poor performance (the best OU model shows an AICc that is 145 units higher than the best model). This does not mean that directional selective pressures were not in place in smaller parts of the horses’ tree, but rather than treewide trends observed in body mass and hypsodonty can be explained without invoking constant and widespread phyletic directionality (resulting from pervasive selection pressures) among lineages within each of the three partitions examined. Thus, our results further reject the notion of Cope’s rule governing body mass evolution in horses (Shoemaker & Clauset, 2013; Juan L Cantalapiedra et al., 2017), since both increases and decreases in body size in horses are commonplace (Alberdi et al., 1995). Likewise, except for certain exceptions (e.g., certain lineages within American Hipparionini (Juan L Cantalapiedra et al., 2017)), we do not see sustained and ubiquitous increase in hypsodonty resulting from widespread natural selection along horse lineages. If sustained and ubiquitous selection pressures cannot explain the patterns observed in the fossil record of horses, what processes may have shaped major phenotypic trends in the horses’ family? We hypothesize that the answer lies in the differential survival and diversification of lineages, and not in the differential survival of individuals within populations (the driver of phyletic trends). The neutral diffusion model (BM models) implies that phenotypic change emerges randomly, without a preferential direction. As in other mammalian clades (Juan L. Cantalapiedra et al., 2021), the acquisition of certain phenotypic features would have increased the probability of populations surviving environmental disturbances and resource limitations. In scenarios of habitat fragmentation (e.g., during environmental fluctuations), when gene flow between populations diminishes, resources are scarcer, and population sizes decrease, certain features could render that some species and satellite populations become extinct, or that these populations survive in isolation. The latter case is the first step toward speciation (Vrba, 1980), the former is the precursor of lineage extinction. If two extremes of a phenotypic gradient show differential diversification rates (the so-called “macroevolutionary effect” (Vrba, 1984)), the clade is expected to advance toward the phenotypic extreme associated to higher diversification potential even in the absence of an active, parallel phyletic trend (Stanley, 1979; Alroy, 2000).

New Perspectives on Horses’ Diversification and Phenotypic Evolution The results described above yield a first general conclusion: there is little connection between rates of phenotypic evolution and rates of lineage diversification in horses. Paleogene horses show the fastest rates of body size evolution among horses, likely

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reflecting substantial evolution in various ecological niches, and yet they show the slowest speciation and net diversification rates of the three groups analyzed here. We have demonstrated that high diversification was a feature that characterized both stem equine anchitheres and early equines, in what seems to be a common trend (Fig. 2.2) likely triggered by the dawn of Neogene conditions (marked by seasonality and ecosystem heterogeneity (Badgley et al., 2016)). However, only Equinae lineages show high rates of hypsodonty evolution, an acceleration that postdates the onset of that diversification regime by six million years. Was this diversification event in stem equine anchitheres and early equines to any extent driven by fast evolution in the former? The second best-performing phylogenetic model yields some insights on equine evolution. It shows that phenotypic evolution in Equinae accelerated over time (an ACDC model with positive acceleration parameter; Table S2), opposite to the expectation under an adaptive radiation model: as diversification decreased and diversity in Equines plateaued (Fig. 2.2), phenotypic changes kept accelerating (Juan L Cantalapiedra et al., 2017). In summary, the fastest phase of species production did not require the fastest rate of phenotypic evolution, and likely started in stem equine anchitheres, slow-evolving lineages in terms of body size and hypsodonty. Further research should test the degree to which the acquisition of other phenotypic features, at the base of the equine anchitheres (e.g., limb modifications (Janis & Bernor, 2019; MacLaren, 2021)), is associated with the fast diversification of their lineage and that of the early equines. With the data at hand, however, it also seems plausible that extrinsic drivers promoted species origination in Neogene horses (by facilitating population fragmentation in both anchitheres and equines), and that such multiplication facilitated the emergence of phenotypic variation as a result of local selection pressures in small, isolated populations, rather than the other way around. This scenario is reinforced by the fact the anchitheres were already showing mixed and grass-dominated diets (Semprebon et al., 2016), which placed them in dynamic, heterogeneous, ecotonerich landscapes of the earliest Neogene that acted like a cocktail shaker for populations, enhancing opportunities for allopatric speciation and extinction. In turn, new phenotypic features could have reinforced the diversification process by favoring the survival of peripheral populations. Although the radiation of equines in the Early Miocene has become a paradigm of mammalian macroevolutionary success, in terms of species production (i.e., speciation rates), our analyses reveal that the key to the equine radiation may stem from a progressive suppression of extinction risk as we move from anchitheres toward equines, rather from an extraordinary capacity of species proliferation, which anchitheres already had. Acknowledgments We thank Judith Galking for her hospitality and for making our stay in the American Natural History Museum at New York so enjoyable. We also thank Marielle Kaashoek for her helpful insights and comments on the manuscript.

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Chapter 3

The Miocene Browsing Horses: Another Way to Be a Successful Large Equid Christine M. Janis, Edward Franklin, C. Nicholas Baird, and Joshua Tyler

Abstract Horse evolution is popularly known and portrayed as an “Eohippus to Equus” sequence, with the modern horse as the pinnacle of the sequence. This portrayal not only ignores the bushy and branching pattern of equid evolution that we now know took place, but in particular ignores the radiation of large browsing horses (the Anchitheriini) that occurred alongside the initial radiation of the grazing horses (Equinae) in the mid-Miocene, with the initial spread of grassland habitats. Here we show that the anchitheriins were not merely larger versions of earlier small browsers such as Mesohippus, but had their own specialized features of their skull, teeth, and feet, indicating unique adaptations to both diet and locomotion. Although they were less numerous as fossils (and probably as individuals) than their grazing relatives, they were nevertheless a successful radiation in both North America and Eurasia, and only became extinct with the climatic changes of the late Miocene.

Supplementary Information The online version contains supplementary material available at https://doi.org/10.1007/978-3-031-27144-1_3. C. M. Janis (✉) Bristol Palaeobiology Group, School of Earth Sciences, University of Bristol, Bristol, UK Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA e-mail: [email protected] E. Franklin Bristol Palaeobiology Group, School of Earth Sciences, University of Bristol, Bristol, UK C. N. Baird Department of Zoology, Museum für Naturkunde, Berlin, Germany Department of Vertebrate Paleontology, American Museum of Natural History, New York, NY, USA Lamont Doherty Earth Observatory, Columbia University, Palisades, NY, USA J. Tyler Milner Centre for Evolution, University of Bath, Bath, UK © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 H. H. T. Prins, I. J. Gordon (eds.), The Equids, Fascinating Life Sciences, https://doi.org/10.1007/978-3-031-27144-1_3

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Introduction The family Equidae (Perissodactyla, Eutheria, Mammalia) is divided into three subfamilies: the extant, monophyletic Equinae (early Miocene to Recent), and two extinct, paraphyletic subfamilies – Anchitheriinae (late Eocene to late Miocene) and Hyracotheriinae (early to late Eocene) (see MacFadden, 1992, for background on this and other matters relating to equid evolution). The Anchitheriinae has long been the neglected “middle child,” caught in between the dog-sized, forest-scampering hyracotheres and the larger savanna-grazing Equinae, to which the extant genus Equus belongs (c.f. Cantalapiedra et al., Chap. 2). The most basal anchithere, the late Eocene to early Oligocene Mesohippus, and the most derived anchithere (i.e., the one most closely related to the Equinae), the early to middle Miocene Parahippus, frequently appear in the orthogenetic diagrams of the “progression” of horse evolution. But in between those two endpoints was a distinct monophyletic side branch, first appearing in the latest Oligocene, radiating in the middle Miocene, and going extinct in the late Miocene – the “Anchitheriinae sensu stricto” (sensu MacFadden, 1992). We refer to this group here as the tribe Anchitheriini (informally anchitheriins, to match the Equinae (= equine) tribes Equini (= equins), Hipparionini (= hipparionins), and Protohippini (= protohippins)). Figure 3.1 shows an “anchitheriin-centric” phylogeny of the family Equidae and includes the range of body masses for the different taxa. Anchitheriins and early equines (subfamily Equinae) were contemporaries in the mid-Miocene (~17.5–10 Ma (millions of years ago)) woodland savanna habitats of North America, and in the early late Miocene (~ 11.0–9.5 Ma) in Eurasia. This was a new type of habitat, relating to changing climatic conditions over the Cenozoic. The hyracotheres (dog-sized browsers and fruit-eaters) lived in Eocene North American mid-latitude tropical-like forests (~55–37 Ma), which declined in the late Eocene with cooling global temperatures. The basal anchitheres (sheep-sized browsers) lived in the North American temperate woodlands of the late Eocene and Oligocene (~37–24 Ma). Grassland habitats first spread in North America at the start of the Miocene (~24 Ma) with renewed climatic warming, but the radiation of both equines (mixed feeders and grazers, see Hulbert & MacFadden, 1991), and anchitheriins (specialized browsers) did not really get underway until around 17.5 Ma, for reasons that are still not clear. By the late late Miocene (~9 Ma) the climate had cooled again, and conditions were more arid; the anchitheriins became extinct (as did many other contemporaneous browsers) and the diversity of the equines declined. (See MoralesGarcía et al., 2020, for a review of the North American savanna habitats.) Anchitheriins differed from all the other anchitheres in their larger body size, ranging from around 100 kg up to 600 kg, with most species being in the region of 150–250 kg (see Shoemaker & Clauset, 2014). This is a very similar range of body masses to the members of the tribe Equini (or even simply species of Equus). Some derived dental features unite the Anchitheriini in a clade, including an enlarged tooth crown area, and several details of the cheek teeth (e.g., welldeveloped cingulae, see MacFadden, 1992; O’Sullivan, 2008). Anchitheriins were

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Hyracotheres 8-10 kg

Basal anchitheres 25-60 kg

Stem-equine anchitheres 40-130* kg

Merychippus 65 kg

Hipparionini 40-400 kg

Protohippini 45-250 kg

Equini 100-600* kg

Equinae

Anchitherium 114-160 kg

Sinohippus 400 kg

?

Kalobatippus 75-160 kg

Hypohippus 230-600 kg

Anchitheriini

Megahippus 200-250 kg

Fig. 3.1 Phylogeny of the Equidae from an “anchitheriin-centric” viewpoint, based on MacFadden, 1992, with the separate identity and systematic position of the Protohippini following Kelly, 1995, 1998 and Pagnac (2006). Key: HYR (brown) = Hyracotheriinae; ANA (red) = Anchitheriini; ANB (orange) = basal Anchitheriinae; ANE (purple) = stem-equine Anchitheriinae; EQH (light blue) = Equinae – basal equines, Hipparionini, and Protohippini;

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“primitive” in as much as they retained certain characters of the more basal anchitheres, such as Mesohippus and Miohippus (late Eocene through earliest Miocene). In terms of craniodental features their cheek teeth were persistently brachydont, indicative of a browsing diet, a supposition supported by their dental wear (Mihlbachler et al., 2011; Semprebon et al., 2019). In contrast, the stem-equine anchitheres (Archaeohippus, Desmatippus, and Parahippus), first appearing in the latest Oligocene, had teeth that started to become somewhat higher-crowned, with dental wear evidence of the inclusion of some grass in the diet (Mihlbachler et al., 2011). Anchitheriins had tridactyl (three-toed) feet, likely with a tapir-like foot pad, but with longer metapodials and a more prominent central (third) toe than hyracotheres, quite unlike the monodactyl (single-toed) feet of a modern horse, with large single hooves and a system of supportive ligaments termed a “spring foot”. The evolution of equid feet is discussed later, in the section on foot anatomy. The anchitheriins were the first of the Equidae to reach the Old World. There is some debate as to whether any of the early Eocene Eurasian equoids (equid-like forms) were truly within the family Equidae, but the main radiation of Equidae was in North America. Their sister taxon, the somewhat equid-like Palaeotheriidae, was a Eurasian radiation of the Eocene and early Oligocene. Equid-like animals were then absent from the Old World until the immigration from North America of Anchitherium in the late early Miocene (at around 18 Ma). Anchitheriins had a moderate radiation in the mid-Miocene of Eurasia, including the larger (predominately Asian) late Miocene genus Sinohippus; however, unlike the later arriving hipparionins and equins, anchitheriins never reached Africa. They persisted until the end of the early late Miocene, around 9 Ma, overlapping for a short while with the hipparionin horses that migrated over to the Old World at around 11 Ma. The hipparionins persisted until around a million years ago (but at greatly reduced diversity to their Miocene presence), also having a radiation in Africa, while the first of the genus Equus migrated to the Old World from North America at around 2.5

Fig. 3.1 (continued) EQE (medium blue) = Equinae – Equini (less Equus); EQU (dark blue) = Equus. Body masses from Shoemaker & Clauset, 2014: a * indicates that this range excludes exceptional very large taxa: in the ANE, Parahippus nebraskensis (246 kg); in the EQE, Equus giganteus (1200 kg). Silhouettes (showing taxa approximately to scale) are all from phylopic.org, unless otherwise stated; horses facing to the left indicate taxa known from the Old World, the rest are all New World. Credits, from top to bottom: Eohippus angustidens by Scott Hartman; Mesohippus by Heinrich Harder, vectorized by T. Michael Keesey; Archaeohippus (Wikipedia); Merychippus insignis (this species not actually basal) (Wikipedia); Neohipparion affine by Bruce Robert Horsefall, vectorized by Zimices; Hippotherium primigenium by Zimices; Merychippus (standing in for Protohippus) by Mercedes Yrayzoz, vectorized by T. Michael Keesey; Pliohippus by Zimices; Equus scotti by Bruce Robert Horsefall, vectorized by Zimices; Anchitherium by Zimices; Kalobatippus (Wikipedia); Hypohippus (Wikipedia). Wikipedia images in the public domain. Phylopic images available for reuse under the Public Domain Dedication 1.0 license, or Creative Commons Attribution unported license http://creativecommons.org/licenses/ by/3.0/

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million years ago. The climatic changes previously described for North America also impacted Eurasia, but here the late Miocene aridity was not as profound (Eronen et al., 2012), and the decline in equid diversity occurred a few million years later (Janis, 2023). The radiation of the Anchitheriini was more prolific in North America than in Eurasia, and fossil localities frequently contain more than one (and up to four) anchitheriin species, whereas Eurasian localities almost never have more than a single species present (Janis, 2023). Their main diversity was in the middle Miocene, ~16–12 Ma, with the genera Hypohippus and Megahippus, but they also persisted into the early late Miocene with the last North American species (Hypohippus affinus) known from around 10 Ma. Anchitheriins were relatively common members of mid-Miocene (late early Miocene to early late Miocene, ~17.5–10 Ma) faunas on both continents, but they were not common as individuals in fossil deposits. The Eurasian anchitheriins are mainly known from teeth and some scraps of postcrania, and complete skulls are rare. The material from North America is a little better, including the complete skeleton of Hypohippus osborni mounted in the American Museum of Natural History. Although the larger size of anchitheriins is appreciated, and the relatively long neck of Hypohippus was featured (if a bit exaggerated) in the diorama for the American Museum of Natural History’s exhibition on horse evolution (https:// www.amnh.org/exhibitions/horse/the-evolution-of-horses), they remain relatively understudied, perceived as an evolutionary left-over when the ancestors of modern horses radiated on the Miocene savannas. Yet this is a viewpoint dominated by the specter of orthogenesis, and the old story of “horse evolution” leading to the genus Equus. A different way to look at the issue might be to consider that, by the start of the Miocene, there was a split in equid evolution: one lineage led to the more hypsodont, spring-footed stem-equine anchitheres and the Equinae, the other to the Anchitheriini. As we shall show in this Chapter, anchitheriins had a number of their own derived characteristics and were not simply Mesohippus writ large (contra Sondaar, 1968). Both equid lineages flourished and radiated in the mid-Miocene in the North American savannas (see Damuth & Janis, 2011). Anchitheriins only declined and eventually became extinct in the cooling temperatures and increased aridity of the later Miocene, a time when the Equinae were also reduced in abundance and diversity (see Fig. 10.5 in Janis, 2023). Below we describe various features of the anatomy of at least North American anchitheriins: some of this is general information, if not well known; we also present some original research, not published elsewhere (for this, details of the methodologies and the taxa studied are available in the online supplement). In this venture, we aim to compare and contrast anchitheriins with equins (i.e., members of the tribe Equini), especially with the genus Equus, and to show that there is more than one way to be a successful large equid.

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Anatomical Differences between Anchitheriins and Other Equids General Skeletal Form Figure 3.2 shows the skeleton of a representative anchitheriin (Hypohippus osborni) in comparison with two equines: a representative hipparionin (Neohipparion affine) and a representative equin (Equus scotti), all equids that would have been about the size of a large pony. The longer neck of Hypohippus is apparent: in other respects, the skeleton is quite similar to that of Neohipparion, with tridactyl feet (although the side toes are relatively longer than in Neohipparion), and relatively long metapodials. (Note that the metapodials in the anchitheriin Kalobatippus were extremely long: see MacFadden, 1992.) However, the proximal third phalanx is relatively short in Hypohippus (see also Fig. 3.7), reflecting the likely retention of a pad foot. Hypohippus also differs in retaining a complete, unfused distal ulna, in the other two equids this element is lost or fused with the radius. (A complete, although extremely slender, distal ulna is retained in the basal equine Merychippus primus (F: AM 1274490: CMJ pers. obs.)) Another relatively basal feature in Hypohippus (not visible in Fig. 3.2) is the form of the distal femur: the femoral articulatory surfaces at the knee for the tibia (condyles) are highly asymmetrical in Equinae such as Neohipparion and Equus, but much less so in Hypohippus (Janis et al., 2012). Hermanson and MacFadden (1996) originally noted this morphology in equine equids and attributed it to the knee-locking mechanism of horses and the development of a passive stay apparatus for the hind leg, in association with the habit of standing many hours per day while grazing. Although this morphology clearly does have this function, there are also broader implications: Janis et al. (2012) showed that in a wide diversity of ungulates asymmetric distal femora are associated both with larger size and a preference for open habitats for those taxa using an asymmetric gait such as a gallop (c.f., Kaashoek et al. Chap. 13). The lack of profound femoral asymmetry in Hypohippus probably relates to it being more closed-habitat in preference than the similarly sized contemporaneous equine equids. Hypohippus does appear to have the beginnings of an Equus-like stay apparatus in the shoulder, probably relating to its large size (see Kaashoek et al., Chap. 13). Equus differs from both other equids not only in being anatomically monodactyl but also in having somewhat shorter metapodials (see also Figs. 3.7 and 3.8). Equus also differs in the vertebral column: the neck is slightly longer than in Neohipparion (but not as long as in Hypohippus); in the thoracic region at the front of the trunk the neural arches (that project upwards from the vertebrae) are taller, indicating a larger area of attachment for the ligament for supporting the head (the nuchal ligament); in the posterior part of the trunk (lumbar and sacral regions) these arches are shorter, indicating a less flexible back. This lesser flexibility of the back was first apparent in the equin Pliohippus (see Janis & Bernor, 2019). Jones (2016) also showed that the equin genera Equus and Hippidion had a stiffer back than other equids, which she associated with a transition to horse-like gallop from a more bounding type of fast gait, but anchitheriins were not included in this study.

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Hypohippus osborni

Long neck

Complete distal ulna Long metapodials, robust side toes, foot pad likely present

Neohipparion affine

Elongated sacrum and high lumbar & sacral neural arches, back flexible

Distal ulna incomplete Metapodials long & lateral digits reduced but complete Longer proximal phalanx, evidence of “spring-foot”

Shorter sacrum & low lumbar and sacral neural arches, back stiff

Thoracic neural arches higher

Metapodials robust and shorter & lateral digits reduced to proximal splints

Fig. 3.2 Skeletons of equids, modified from photographs in the public domain (on Wikipedia) of mounted skeletons in the American Museum of Natural History (New York, USA), showing some distinguishing morphological features. Top to bottom: Hypohippus osborni (Anchtheriinae: Anchitheriini), Neohipparion affine (Equinae: Hipparionini), Equus scotti (Equinae: Equini). All equids shown to the same scale, about the size of a large pony

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Craniodental Anatomy Figure 3.3 shows the skull of a derived anchitheriin, Megahippus matthewi, in comparison with other equids. Note that both the skulls of Megahippus and Equus are derived in comparison with a more basal anchithere equid such as Mesohippus. The cheek teeth of Megahippus remain brachydont (low-crowned), but they are greatly enlarged, both in terms of the height of the crown above the level of the jaw (as seen here) and in the occlusal dimensions (i.e., the width times the length in occlusal view). The anchitheriin skulls appear to have been relatively flat (see also Fig. 3.S1: this is not simply an artifact of post-mortem crushing), and the postorbital bar (behind the eye) remains incomplete, as in the general mammalian condition, also seen in more basal equids such as Hyracotherium and Mesohippus. In comparison with Equus, the anterior jaw of Megahippus remains relatively short, the orbit has not been repositioned dorsally, and the face is not highly flexed on the basicranium (the base of the skull). (The dorsally placed orbit in Equus may be related to the presence of hypsodont cheek teeth and/or to the reorganization of cranial proportions with a long face and flexed basicranium.) However, the incisors of Megahippus are massive and protruding (other anchitheriins do not have incisors that are quite as prominent). The muzzle of Megahippus is fairly narrow, as befits a browser: this anatomy is similar to that of the more basal equids, but the muzzles of the equines, including Equus, are somewhat broader, and the incisor row is relatively straight with the lateral incisors as broad as the central ones, as see in general in grazers (Janis & Ehrhardt, 1988). These large incisors may reflect powerful prehension of vegetation, a notion that is supported by the large sagittal crest (in comparison with Equus) and the extended “sagittal flange,” which would have supported a larger temporalis muscle (one of the main jaw-closing muscles) than in other equids, especially than in Equus where this temporal area is reduced in size. The temporalis is the jaw adductor (closing) muscle better positioned to create or resist forces at the front of the jaw, while the masseter muscle is the one better positioned to generate forces at the cheek teeth during mastication of the food (Maynard Smith & Savage, 1959). The masseter originates from the zygomatic arch under the eye (= the “cheek bone” in humans) and inserts onto the angle of the mandible. Equine equids have an enlarged and reoriented masseter muscle, as shown by the extension of a masseteric ridge from the zygomatic arch, reflecting a more anterior origin of the masseter, and an enlarged angle of the mandible (see Fig. 3.4) (Turnbull, 1970). The zygomatic arch of Megahippus is massive, reflecting a relatively large-sized masseter muscle complex, but not with the particular specialties of Equus, and there is no masseteric ridge extension. In addition, Megahippus has not enlarged and changed the shape of the angle of the mandible as seen in Equus, although the main body of the jaw is robust. This change in mandibular shape is first apparent in basal equines such as Merychippus and is associated with a change in the size (larger) and positioning (more anterior) for the insertion of the deep portion of the masseter muscle, increasing its mechanical advantage (Turnbull, 1970, Fig. 4.8). The change in mandible shape in the Equinae,

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Fig. 3.3 Skulls of equids, including a ventral view of the front of the skull (anterior to the premolar row), i.e., the snout, to show face length and the shape of the muzzle and the incisor row. The lateral views of the skulls of Hyracotherium, Mesohippus, and Equus are modified from Radinsky, 1984; Megahippus is based on Megahippus matthewi (F:AM 60700). Note that the type of facial fossa seen in Megahippus was also common in the Equinae, and mainly lost only in Equus. A postorbital bar was first seen in stem-equine anchitheres Desmatippus/Parahippus. The snouts are from the following sources: Hyracotherium is based on AM 55986, with the incisors (but not the canine) modified from Miohippus obliquidens (F:AM 74076); Mesohippus is based on the related basal anchithere Miohippus obliquidens (F:AM 74076); Equus is the extant Greyvi’s zebra E. greyvi (ZMB_Mamm_70278) (photo taken by CNB); Megahippus is based on M. matthewi (F:AM 60700), but with the incisors taken from a drawing from the Florida Museum of Natural History (https://www.floridamuseum.ufl.edu/fossil-horses/gallery/megahippus/). Bar = 5 cm (for lateral

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Fig. 3.4 Skulls of Equus and Megahippus (see Fig. 3.3 for credits) with the positions of the major jaw adductor muscles (masseter and temporalis) imposed. Muscle positions taken from Turnbull, 1970; Megahippus conjectural but inferred by CMJ from cranial anatomy

and corresponding changes in the size and orientation of masseter musculature, may reflect different demands of chewing in the equine lineage that was now incorporating more grass in the diet. In summary, the skull, and teeth of both Megahippus and Equus are modified from the Mesohippus condition in ways that reflect different dietary specializations. The craniodental modifications of Megahippus reflect greater specializations for browsing: enlarged (but brachydont) cheek teeth, enlarged procumbent incisors, and modification of the temporal region indicative of a larger temporalis for exerting force at the incisors. In contrast, the modifications of Equus reflect specializations for grazing: hypsodont (high-crowned) cheek teeth, modifications of masseter musculature reflecting mastication of tougher food, a broad muzzle with incisors set in a straight line rather than an arc, and a long face flexed on the basicranium. Below we present some original research on the quantification of craniodental shape in equids (details of the specimens measured and the methodologies employed are in the supplementary online information). Figure 3.5 shows the general cranial shape of a diverse assortment of equids, as determined by two-dimensional geometric morphological analysis based on lateral images, shown as a Principal Components Analysis (PCA). Geometric morphometrics is a mathematical approach to understanding how geometric shape varies across a sample. Initially, Cartesian coordinates (landmarks) are collected for homologous points across images (2D) or scans/models (3D) from each sampled taxon. These are then translated, rotated, and scaled in order to minimize the differences in landmark position (Procrustes Alignment). This removes size effects from analysis and solely focuses

Fig. 3.3 (continued) skull views). AM American Museum of Natural History (New York, USA); F: AM Frick Collection, American Museum of Natural History; ZMB Museum für Naturkunde (Berlin, Germany)

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Fig. 3.5 Principle Components Analysis performed on the Procrustes coordinates from the 2D Geometric Morphometrics analysis on equid skulls (for details of the landmarks, see Fig. 3.S1 and Table 3.S2 in the online supplement). For information as to the numbered taxa, see the text in part and Table 3.S1 in the online supplement for the full listing. The identity of the anchitheriins is as follows: #7 = Sinohippus zitteli, #8 = Hypohippus affinus, #9 = Hypohippus sp., #10 = Megahippus matthewi, #11 = Megahippus mckennai

on shape. Morphospaces are then constructed using Principal Components Analysis. Table 3.S1 provides details of the taxa studied, and Fig. 3.S1 and Table 3.S2 show the placement of the landmarks in this study. This study included 51 individuals of 48 species: three hyracotheres, three basal anchitheres, five anchitheriins, two stem-equine anchitheres, and 38 equines. The equines included nine North American hipparionins and protohippins, ten Old World hipparionins, and 19 equins, including 11 species of Equus, seven of them extant. A few of these taxa had highly retracted nasals (the anchitheriin Sinohippus, the equin Hippidion, and three of the Old World hipparionins): in the analysis shown here this landmark was not included, so as to emphasize other features of craniodental anatomy on the second component. The first component, reflecting the main trend of morphological variation (35% of the variance), also reflects the equid phylogeny, plus the dietary trend of frugivorefolivore in hyracotheres (highly positive scores), browsing in anchitheres (somewhat positive scores), and mixed-feeding to grazing in equines (weakly positive to negative scores), with members of the genus Equus (the most specialized grazers) having the most negative scores. The differences in cranial shape along this axis are summarized in Table 3.1. The second component, explaining 14% of the variance, distinguishes the anchitheriins (with negative scores) from other non-equine equids (with scores

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Table 3.1 Cranial morphology trends along PC1 Cranial Anatomy Position of orbit Preorbital portion of skull Snout Distance between canine and first incisor Incisors Zygomatic arch

Postorbital portion of skull vault Occipital region

Flexion of face on basicranium Length from point of basicranial flexion to back of molar row.

High negative scores (equines) Moved posteriorly and dorsally Long Longer, anterior end of nasal incision more posterior Long Longer Long (extended by masseteric ridge), angled so lower anteriorly Shorter, slopes steeply ventrally from highest point to nuchal region Slopes anteriorly from nuchal crest to occipital condyles Highly flexed, shorter basicranium Long

High positive scores (hyracotheres) Over Center of molar row Short Shorter, anterior end of nasal incision more anterior Short Shorter Short (not extended by masseteric ridge), angled so slightly higher anteriorly Long, slopes only slightly ventrally Slopes only slightly anteriorly from nuchal crest to occipital condyles Little flexion, longer basicranium Short

ranging from around zero to positive scores) on the positive side of PC1, especially Megahippus mckennai (#11). However, a number of equines on the negative side of PC1 also have highly negative PC2 scores, including several Old World hipparionins and basal species of Equus such as E. scotti (#41) and E. stenosis (#42). In contrast, most of the extant species of Equus (#s 44–51) have highly positive scores. The difference in cranial shape along this axis is summarized in Table 3.2. This study unfortunately does not distinguish anchitheriins from all other equids by the features that are apparent in Fig. 3.3; however, it does show that they are distinct in the area of the morphospace (positive scores on PC1 > 0.05) that contains the non-equine equids. A statistical test (MANOVA) on the PC scores shows that anchitheriins are distinctly different from the other anchitheres (see Table 3.S3), and a separate linear discriminant analysis shows that the skull morphology of anchitheriins can be clearly distinguished as very different from that of other equids (see discussion in online supplement and Fig. 3.S2). Figure 3.6 illustrates the increased size of the cheek teeth in the derived anchitheriins. This study included 20 species: three hyracotheres, two basal anchitheres, four anchitheriins, two stem-equine anchitheres, and ten equines

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Table 3.2 Cranial morphology trends along PC2 Cranial Anatomy Position of orbit

High positive scores (inc. most Equus) Moved posteriorly and dorsally

Snout

Shorter, nasal incision more anterior, shorter distance between canine and incisors, first incisor more projecting Moderate

High negative scores(inc. anchitheriins) Above and slightly behind back of molar row Longer, nasal incision more posterior, longer distance between canine and incisors, first incisor more vertical Longer

More ventrally inclined Slightly shorter

More procumbent Slightly longer

Long

Long

Long, slight slope from highest point to nuchal region

Long, more pronouncedslope from highest point to nuchal region

Long, slopes markedly ventrally from nuchal region to occipital condyles Highly flexed

Short, slopes slightly ventrally from nuchal region to occipital condyles Less highly flexed

Distance between canine and first incisor Incisors Length of premolar row Masseteric ridge Postorbital portion of skull vault Occipital region Flexion of face on basicranium

(including three equins, one the extant Equus grevyii, Grevyi’s zebra) (see Table 3. S5). The volume of the cheek teeth (both molars and premolars) is calculated as the combination of occlusal length and width plus the height of the crown of the tooth above the jaw (not including the height of the tooth crown embedded in the jaw bones in the hypsodont taxa) measured for each tooth individually and then summed. The length of the molar row is taken as a proxy for body mass (see Janis, 1990). However, note that the anchitheriins, with their larger teeth in general, appear to have a proportionally longer molar row for their size: Megahippus matthewi (estimated mass of 265 kg, based on first molar length) appears be larger than Equus grevyii (average mass 350 kg), so the relative sizes of the cheek teeth shown here are actually underestimates. However, this graph provides a general picture. Among the Equinae, tooth volume increases slightly with increasing body size, but the Anchitheriini have proportionally much larger teeth for their size. This trend for increased cheek tooth size in larger, later Miocene anchitheriins was also noted for Old World anchitheriins (Forsten, 1991), who interpreted both increased body size and increased cheek tooth size as a response to a more fibrous diet in the less productive habitats of the later Miocene. Her conclusion echoes that of Janis et al. (1994), who also noted the increasing size of anchitheriins in the later middle to early late Miocene (around 14–10 Ma) of North America and attributed it

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Key

Hyracotheriinae

Anchitheriini

Equinae (non-Equini)

Equus (fossil)

Basal Anchitheriinae

Stem-equine Anchitheriinae

Equinae (Equini)

Equus (extant)

Volume of upper cheek teeth (log)

8

7

2.1

13

19 12

20 17 6

5

1.6

14 10 15 1.1

16 18

4 11 9

0.6

3

2 1 0.1 0 .4

0 .6

0 .8

1 .0

Molar row length (log)

Fig. 3.6 Bivariate plot of the molar row length (a proxy for body mass) against the volume of the upper cheek teeth (this equals the amount of the tooth visible above the jaw, and does not account for hypsodont tooth crowns). The regression line is drawn through the Equinae (slope of 3.2879, indicating slight positive allometry). A full listing of the taxa included is provided in the online supplement, Table 3.S5, but a few key taxa are identified here: #5 = “Anchitherium” clarencei, #6 = Sinohippus zitteli, #7 = Hypohippus affinus, #8 = Megahippus matthewi, #9 = Archaeohippus blackbergi, #10 = Parahippus cognatus

to inferred declining quality of available browse vegetation and competition with browsing ruminants.

Foot Anatomy We will first briefly review the evolution of equid feet: the following description is taken largely from Camp and Smith (1942), Sondaar (1968), and Thomason (1986). Basal equids (hyracotheres) had feet similar to those of modern tapirs and hyraxes, with four toes on the front feet (digits 2–5) and three on the hind (digits 2–4), although they had longer metapodials than hyraxes and tapirs (more similar to those seen in a dog). The central digit (the third) was the largest and most robust one, but the others (= the “side toes”) were only a little smaller (note that the term “side

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toes” should strictly refer only to the phalanges, not to their accompanying metapodials, but we use the term here to include the metapodials). The side toes were held somewhat behind the central one, with the array of digits forming an arch (see Wood et al., 2011; Solounias et al., 2018). As can be inferred from the bony anatomy, and comparison with related extant taxa (e.g., tapirs), the tips of the digits (ungual phalanges) were encased in little keratinous hooves, but there was also an extensive foot pad (a bit like those seen in cats and dogs), and the foot posture was “semi-unguligrade.” These equids did not stand completely on the tips of the digits (the “unguligrade” foot posture, like a ballerina en pointe) as in extant Equus, but with the pastern joint between the proximal and intermediate phalanges supported by the foot pad. The phalanges were orientated more horizontally with respect to the ground (but not completely horizontal as seen in the “digitigrade” foot posture of cats and dogs, which stand like a person walking on tiptoe). The limbs of the basal anchithere Mesohippus were more derived than those of the hyracotheres: the fifth digit was lost in the front foot, the side toes were somewhat reduced (being both shorter and slenderer than the central one), the position of the foot more upright, and the metapodials were more elongated (see MacFadden, 1998; Solounias et al., 2018). Their feet had side toes that were able to spread somewhat and would have been in contact with the ground during locomotion. In contrast, the stem-equine anchitheres (Archaeohippus, Desmatippus, and Parahippus) started to acquire the characteristic equine “spring foot,” with an elongated proximal phalanx, more uprightly inclined phalanges, and more reduced side toes where the metapodials were bound more tightly by ligaments to the central metapodial. The foot posture was now unguligrade. By the level of the subfamily Equinae, if not before, the side toes no longer contacted the ground during standing or even during most locomotory ventures (probably only during extreme fetlock flexion, as shown in fossil trackways, see Renders, 1984). The central (third) toe was more robust, and the original foot pad was lost (possibly retained as the digital cushion as seen in Equus). Most spring-footed equids were tridactyl; the loss of the side toes resulting in the condition of monodactyly was with one possible exception only seen within the tribe Equini (see Janis & Bernor, 2019). The type of large keratinous hoof seen in modern equids was probably present on the central toe of the tridactyl unguligrade equids, with smaller hooves on the side toes (but see Solounias et al., 2018). Figure 3.7 compares the forelimb (below the wrist) of Equus and Hypohippus. The most obvious difference is the monodactyl condition of Equus versus the tridactyl condition of Hypohippus. In Equus, the side toes have been reduced to remnants of the proximal metapodials, termed “splint bones.” In Hypohippus, the side toes are complete, although shorter and slenderer than the central third digit. Unlike the condition in more derived tridactyl equids (equines and stem-equine anchitheres) the side toes are relatively long and robust, but like these equids the side metapodials are closely appressed (and bound by ligaments) to the central metapodial (Camp & Smith, 1942; Sondaar, 1968).

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Fig. 3.7 Left manus (= hand, forelimb below the wrist, not including the wrist in this picture) of Equus burchelli (based on MCZ 5003) and Hypohippus equinus (based on an Alamy stock figure from Abel, 1919, with some modifications from photographs of Hypohippus specimens in the American Museum of Natural History taken by CMJ, volar view (underside of foot) based on AM 60545). Note in Equus the prominent distal sagittal metapodial keel extending onto the anterior surface, and the elongated proximal phalanx with a distally-extending V-scar (all indicative of the equine “spring foot” apparatus). On the volar illustrations of the phalanx, the proximal arrow marks the base of the ligament scars (the V-scar in Equus and the central ligament scar in Hypohippus) and the distal arrow marks the site of origin of the collateral ligaments. Note that while Hypohippus retains lateral digits, its bones are more gracile than those of Equus, and the metacarpal is longer. AM American Museum of Natural History (New York, USA); MCZ Harvard Museum of Comparative Zoology (Cambridge, USA)

There are other important differences: first of all, the proximal phalanx of Equus is proportionally longer than in Hypohippus, reflecting the acquisition of a functionally monodactyl and unguligrade “spring foot” with the loss of the foot pad (Sondaar, 1968; O’Sullivan, 2008; see also Kaashoek et al., Chap. 13). This change in phalangeal proportions was first seen in the most basal of the stem-equine

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anchitheres, Archaeohippus (O’Sullivan, 2008). The ungual (distal) phalanx of Equus is larger and broader than that of Hypohippus, reflecting its singular role in weight-bearing. The anterior (= cranial or dorsal) articulatory surface of the distal metapodial in Equus evidences a distinct extension of the metapodial keel, not apparent in Hypohippus. This keel is found on the volar (= underside, or posterior/plantar/ caudal) articulatory surface of the metapodial(s) of all equids (indeed of most mammals) but is only extended onto the anterior surface in cursorial ungulates such as pecoran ruminant artiodactyls (Janis & Scott, 1987) and derived equids (Thomason, 1986). This keel not only more firmly restricts the motion of the metapodial-phalangeal (fetlock) joint to allow near exclusively parasagittal motion (Kaashoek et al., 2019), but also allows for a greater stability during extension (= dorsi-flexion) at the joint, stretching the digital extensor tendons and providing the elastic energy storage that is the essential function of the “spring foot” (Thomason, 1986). The extension of the sagittal ridge onto the anterior metapodial surface is first apparent in Archaeohippus (MacLaren, 2021), accompanying the first appearance of the elongated proximal phalanx (O’Sullivan, 2008). The volar surface of the proximal phalanx in Equus shows a distinct, greatly elongated V-scar (see Fig. 3.7), which is typical of spring-footed forms, and in modern species of Equus the V-scar is particularly elongated (Camp & Smith, 1942). The V-scar marks the area of insertion of the oblique sesamoidean ligaments, which may be homologous with the outer layer of the proximal cruciate ligaments seen in the tapir (Camp & Smith, 1942). A distinct V-scar is associated with larger proximal sesamoids that support the more pronounced ligamentary suspensory apparatus for the fetlock (metapodial-phalangeal) joint, allowing for the greater rotation of the fetlock joint that maximizes elastic energy storage in the digital flexor tendons (see Janis & Bernor, 2019). In contrast, the proximal phalanx of Hypohippus shows a distinct proximal central scar, indicating a strong central sesamoid ligament, but there is no evidence of an attachment site for the oblique sesamoid ligaments (see Fig. 3.7) (Camp & Smith, 1942). Within the Equinae, the central scar progressively merges with the V-scar in the equines, but the V-scar and the central scar remain more separate in the hipparionins and protohippins (Camp & Smith, 1942). Finally, note that the foot of Hypohippus appears more gracile overall than that of the similarly sized Equus, and the metacarpal is longer. Even though Equus is hailed for its “evolutionary success” in attaining the derived condition of monodactyly, this genus actually has proportionally short metapodials in comparison with other equines (especially hipparionins and protohippins), and shorter than in the related equin Pliohippus (species of which either had extremely reduced side toes or were monodactyl; see Janis & Bernor, 2019). The following figures show the results of some research on the limb proportions of equids (see the online supplement for more details). Figure 3.8 shows a Principal Components Analysis of linear measurements of the third metatarsal (9 measurements) and proximal phalanx of the third hind digit (8 measurements) from 40 taxa of equids. Table 3.S6 details the taxa studied and Table 3.S7 describes the

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Key

Hyracotheriinae

Anchitheriini

Equinae (non-Equini)

Equus (fossil)

Basal Anchitheriinae

Stem-equine Anchitheriinae

Equinae (Equini)

Equus (extant)

Long metatarsal

33

28 0.9

PC3 (1.37%)

22

23

25

0.4

19

10

17

14

9

7

-0.1

-1.1

-2.6

-2.1

-1.6

15

39 40

12

More stabilized foot

37

35

13

2

34

32 30

16

3 -0.6

27 36

5

8

18 26

4

11

Broader fetlock articulation

38

24

21 6

29

20 31

1 -1.1

-0.6

-0.1

PC2 (4.64%)

0.4

0.9

1.4

“Spring foot”

Fig. 3.8 Principal Components Analysis of linear measurements of the hind third metatarsal and third proximal phalanx. A full listing of the taxa included is provided in Table 3.S6 and a description of the measurements taken in Table 3.S7 in the online supplement: #10 = a very large undescribed species of Hypohippus, estimated body mass of around 600 kg (see Janis et al., 1994); #29 = Nannippus peninsulatus, #32 = Calippus placidus, #33 = Protohippus simus, #38 = Dinohippus sp.

measurements taken. The analyses were performed on untransformed linear measurements, and so the first component (explaining 90.08% of the variance, not illustrated) largely reflects body size, with hyracotheres having the most negative scores and equins and anchitheriins the most positive. Note that a separate study (Franklin, 2021), which examined the metatarsal and the phalanx separately (including slightly more variables), and was thus able to include more taxa, showed that in the plots of PC1 against PC2 for each element the anchitheriins were also clearly separable from the other equids, as is the case here with the two elements combined in a single analysis. Figure 3.8 shows the plot of the second component (explaining 4.64% of the variance) against the third component (explaining 1.37% of the variance). This figure clearly shows that the anchitheriins have a pedal anatomy distinct both from that of basal equids (hyracotheres and basal anchitheres) and the equines (including the stem-equine anchitheres), reflecting the early Miocene split in the phylogeny discussed previously. Basal equids plot in the middle of PC2, with slightly negative scores, while the equines (plus stem-equine anchitheres) have positive scores and the anchitheriins have negative scores. The loadings of the variables (Table 3.S7) distinguish the equines as having a spring foot (long distal metapodial sagittal

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ridge, long proximal phalanx with a long V-scar) from the anchitheriins. The anchitheriins have their own set of derived morphologies, especially a wide (versus long) proximal phalanx and broad articulatory surfaces, an anatomy which may indicate a more stabilized foot (see further discussion in the online supplement). The length of the metatarsal is the predominant anatomical feature on PC3 with high positive loadings. The hipparionins and protohippins have high positive scores and Equus has high negative scores. Note also that the basal anchitheres and all but one of the anchitheriins (#12, Megahippus sp.) have higher scores on PC3 than the single specimen of Hyracotherium, reflecting their relatively longer metatarsals. Some of the variables with high positive loadings on PC3 reflect the spring foot morphology of the equines (the length of the distal metapodial sagittal ridge), plus perhaps also the unique feature of a deep (rather than wide) proximal phalanx (which may relate to the tridactyl condition of the hipparionins and protohippins, as also shown in the metapodial proportions in MacLaren, 2021). The stem-equine anchitheres and the non-Equus equins cluster with scores around zero on PC3 (although the equins have more positive scores on PC2); but the Equus species (#39, 40) have more highly negative scores on PC3, and more highly positive scores on PC2. The variables with negative loadings on PC3 reflect the longer V-scar in Equus than in other equines (see Camp & Smith, 1942), plus wider articulatory surfaces, which may reflect the Equus condition of monodactyly (see also MacLaren, 2021). These results are discussed in more detail in the online supplement. In summary, these results support the distinctive nature of the anchitheriin foot. Table 3.S8 shows that the anchitheriin foot is statistically different (using a MANOVA) from the other equids (based on the PC2 scores, but not on the PC3 scores). Although Sondaar (1968) considered that the anchitheriin foot was simply an allometrically scaled-up version of a basal anchithere foot, we consider this to be unlikely. In a diversity of plots, anchitheriins are always divergent from the other equids on PC2 (representing shape) and not on PC1 (representing size). We consider that anchitheriins show a pedal anatomy that had some unique specializations, divergent from that of the more basal equids, as well as being different from that of the Equinae. This anatomy was indicative of a greater degree of foot stabilization, perhaps associated with their habitat (see further discussion in online supplement). Figure 3.9 shows a PCA of the results of the 2D geometric morphometrics analysis of the proximal phalanx (which was landmarked in volar/plantar view so that the position of the ligament scars was apparent). Table 3.S9 details the taxa studied, and Fig. 3.S3 and Table 3.S10 show the position of the landmarks. The first component (66.31% of the variance) clearly separates out the equids with a spring foot morphology (positive scores) from those without (negative scores), based on relative robusticity of the phalanx and the position of the most distal ligament scars (see also Fig. 3.7). Note that the taxon with the most positive score is the hipparionin Nannippus peninsulatus (#19), whose foot anatomy is like that of derived equins to a large extent, including reduction or even loss of the lateral digits (see discussion in Janis & Bernor, 2019), but is divergent from equins in the morphology of the distal metapodial, which is more akin to other North American hipparionins (MacLaren, 2021).

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Key

Hyracotheriinae

Anchitheriini

Equinae (non-Equini)

Equus (extant)

Basal Anchitheriinae

Stem-equine Anchitheriinae

Equinae (Equini)

Tapiridae

12

0.06

24 5

PC3 (6.52%)

0.01

4

9

2

17

13

3

20 14 15

7 18

8

11

22

23 19

1 21

-0.04

16

10

6

-0.15

-0.05

-0.09 -0.25

0.05

0.15

0.25

PC1 (66.31%)

Fig. 3.9 Principal Components Analysis on the Procrustes coordinates from the 2D Geometric Morphometrics analysis of the hind left third proximal phalanx (volar/plantar view). A full listing of the taxa included is provided in Table 3.S9, and the position of the landmarks is described in Fig. 3. S3 and Table 3.S10. The wireframe diagrams show the morphology of the phalanx at the endpoints of the components: the black dot shows the position of the base of the ligament scars. #6 = Kalobatippus sp.1, #10 = very large species of Hypohippus, #14 = Parahippus cognatus, #19 = Nannippus peninsulatus, #22 = Pliohippus mirabilus

Of note is the position of the hyracotheriine Orohippus (#1), especially in relation to the tapir (#24). Tapirs are often thought of as being a good functional analog for early equoids (i.e., Equidae and their European sister taxa the Palaeotheriidae) in terms of their foot anatomy (see MacLaren & Nauwelaerts, 2020). In contrast, our study shows that, while both tapirs and basal anchitheres have short proximal phalanges, the proximal phalanges of hyracotheriines are more gracile. Hyracotheriines have relatively longer side toes than basal anchitheres (Sondaar, 1968), plus they (like tapirs) lack evidence of a central sesamoidean ligament (evidence for this first seen in Mesohippus). The presence of this ligament indicates greater support of the fetlock joint, which is necessary with the reduction of the foot pad in the basal anchitheres (Camp & Smith, 1942). Hyracotheres also have other features indicative of a less cursorial mode of locomotion than basal anchitheres (see Wood et al., 2011), and the short proximal phalanx (superficially tapir-like) of basal anchitheres (and anchitheriins) may be a derived condition within early equids. The second component (explaining 8.96% of the variance, not shown here) was based primarily on the position of the most distal sesamoid ligament scars,

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distinguishing the extant equid (Equus burchellii, #23) from all others, and did not distinguish between anchitheriins and basal anchitheres. Anchitheriins are separated from other equids on the third component (shown here, explaining 6.52% of the variance), with especially negative scores being seen in the large species of Hypohippus (#10) and a species of Kalobatippus (#6). However, the differences in morphology along this component are not easy to explain. There is little difference in phalangeal robusticity, and while the position of the ligament scars appears to play a role, in fact a similar result to this is seen on PC2 if this landmark is excluded (Franklin, 2021). Negative values indicate a somewhat broad midshaft, a less indented distal articulation, and somewhat less prominent attachment sites for the origin of the collateral ligaments binding the proximal phalanx to the intermediate one (landmarks 8 and 18, see Fig. 3.S3 and Fig. 3.7). The latter two features hint at a greater degree of movement between these phalanges in anchitheriins, possibly allowing for greater within-digit movement (see also the description of the proximal phalanx of Anchitherium by Sondaar, 1968). However, this analysis does show that the anchitheriin proximal phalanx can be distinguished from that of other equids, as shown by the analysis of the linear measurements.

New Insights on the Morphology of the Anchitheriin Equids Our results on the craniodental and pedal morphology of equids show that anchitheriins can clearly be distinguished from other equids and are not simply larger versions of the more basal anchitheres. Their craniodental anatomy is primitive in some respects – brachydont teeth, lack of a postorbital bar, relatively short face, and flat basicranium, but highly derived in other respects – greatly enlarged cheek teeth, protruding incisors, “sagittal flange” for the origin of the temporalis (Fig. 3.3). These features, in combination with the elongated neck (at least in Hypohippus (Fig. 3.2), the condition in other anchitheriin genera is not known) and the dental wear patterns, are indicative of a specialized browsing habit, possibly high-level browsing (although they lack the long jaws typical of ruminant high-level browsers (Mendoza & Palmqvist, 2008)). Anchitheriin feet show a divergence from the basal condition in the opposite direction from the spring-footed equines and stem-equine anchitheres, with the implication that their feet were more stabilized in their motion at the fetlock joint, rather than having the extensive capacity for extension (dorsiflexion) seen in the spring-footed forms. Note that Camp and Smith (1942) also considered anchitheriins to have had limited motion at the fetlock joint, based on a detailed study of the volar ligament scars. The point in the phylogeny where this foot morphology divergence occurs, just above the level of the basal anchithere Miohippus, also marks an interesting point in the evolution of equid body mass. Equids started out as relatively small animals (body mass estimates for “average-sized” hyracotheres = 8–10 kg (see Wood et al., 2011), although other estimations from craniodental measurements may be higher

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(see MacFadden, 1992)). Equid body size increased with the radiation of the anchitheres, with basal anchitheres being in the region of 25–60 kg (MacFadden, 1996; Shoemaker & Clauset, 2014). However, more derived equids (apart from secondarily dwarfed forms) tend to be larger than this: stem-equine anchitheres such as Parahippus and Desmatippus (Archaeohippus is a secondarily dwarfed form; MacFadden, 1992) and basal equines were mostly in the body mass region of 80–100 kg, whereas the anchitheriins were mostly over 100 kg (MacFadden, 1996; Shoemaker & Clauset, 2014; see also Cantalapiedra et al., Chap. 2; Narcarino-Meneses, Chap. 10). A body mass of around 50 kg turns out to be a bit of a “watershed” size in terms of locomotor biomechanics. The mechanical power demand on stance versus the mechanical work demand on each stride results in physiological constraints that cannot be adjusted via muscle gearing or limb posture (Usherwood & Gladman, 2020). Below around 50 kg animals are constrained in their speed by power demands during their stance phase, whereas above 50 kg they are constrained by the mechanical work demand of each step. This is the reason why the fastest mammals (e.g., Acinonyx jubatus (cheetah), Antilocapra americana (pronghorn)) are found at this “cross-over” point between the two constraints at a body mass of around 50 kg. These work versus power constraints may influence biomechanics and performance in other ways besides maximal speed, and it is of interest that this divergence in equid foot anatomy occurs at the point in equid evolution where this critical body mass appears to have been regularly exceeded. In any event, it is clear that equines (and related anchitheres) and anchitheriins show divergent pedal morphologies. It is not possible to be certain what the functional or adaptive advantage was of the anchitheriin foot. Likely a tapir-like foot pad was retained, and a larger body mass (for a variety of reasons) may have promoted a morphology with broader articulatory surfaces that resulted in a more stabilized foot. The anchitheriine foot was possibly more constrained in motion at the fetlock joint than in the basal equids, in contrast to the “spring foot” condition in equines where there is a greater degree of rotation possible at the fetlock joint, although motion is more restricted to the parasagittal plane. Evidence for both diet (craniodental adaptations, dental wear) and locomotor performance (e.g., distal femoral morphology), as previously discussed, lead to the inference that there was a difference in habitat preference in the mid-Miocene (~17.5–10 Ma): anchitheriins preferred more closed habitats and equines more open habitats (although both are still found in the same fossil deposits (see Janis et al., 2004), in an environment that would have been basically woodland to more open savanna (see Morales-García et al., 2020)). Anchitheriins, like large woodland or forest browsing ruminants today, were probably solitary animals, while the equines were likely social herd formers. Anchitheriins were not numerous as fossils, and so likely not individually numerous as living animals: but this is to be expected due to their evident browsing habit. In the African savannas today browsing ruminants are only about 20% as abundant as grazers of similar body mass (Owen-Smith, 2021, p. 192). Yet the browsers most certainly cannot be considered to be some sort of “evolutionary failure”; their presence is informative as to the nature of the habitat (i.e., woodland

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savanna, rather than prairie). Anchitheriins and equines are found in the same fossil deposits; the lower abundance of anchitheriins as fossil specimens most likely reflects their lower abundance in the ecosystem. If the climate of Africa were to become colder and drier, the habitat would change and browsing ruminants would likely disappear, while the grazers would likely survive. This is probably what happened to the anchitheriins versus the equines in the latest Miocene of North America, a time when many other browsing ungulates also became extinct (Janis et al., 2004). Anchitheriin decline and eventual extinction in the late Miocene should not detract from their obvious evolutionary success in the mid-Miocene. If we were to view equid evolution from the perspective of the mid-Miocene, we would certainly interpret equid phylogeny as having a fundamental split following the basal Anchitheriinae, with the Anchitheriini being a major evolutionary radiation rather than a forgotten side branch. Only time, and the subsequent radiation and success of the Equinae, has blurred our perception. The success of the anchitheriins demonstrates that there is more than one way to be a successful large equid, and that present-day Equus, however, successful in the Recent, is but one example of a “success story” in equid evolution. Acknowledgments For access to specimens in their care, we thank Judy Galkin and Jin Meng at the American Museum of Natural History (New York, NY, USA); Judy Chupasko, Mark Omura, and Jessica Cundiff at the Harvard Museum of Comparative Anatomy (Cambridge, MA, USA); and Thomas Schossleitner at the Museum für Naturkunde (Berlin, Germany). CMJ visits to North American museum collections have been supported by the Bushnell Foundation (Brown University). Thanks also to Padraic O’Driscoll for some early, preliminary analysis of the equid foot data, and to Nuria Melisa Morales-García (www.sciencegraphicdesign.com) for the patient and careful crafting of the figures. And finally, thanks to the editors, Herbert Prins and Iain Gordon for inviting this contribution and making many editorial comments on the MS, and especially to Jamie MacLaren for his heroic efforts in reviewing the MS.

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Chapter 4

Why There Are No Modern Equids Living in Tropical Lowland Rainforests Joost F. de Jong and Herbert H. T. Prins

Abstract Presently, the equid lineage occurs completely outside tropical rainforest environments, which is thought of as the cradle of Perissodactyls and early equid ancestors. The ancestral food of those early equids was based on seeds, fruits, foliage and C3-grasses. The CO2-content of the atmosphere was very high, and C4-grasses had not evolved yet. Zebras and horses are considered to be typical grazers often on C4-grasses, even though Asian equids (and the mountain zebra) have a high proportion of browse in their diet. In comparison to more open environments, present-day tropical forests represent marginal habitats for large ungulates in comparison to more open environments. The suite of traits of large ungulates is not very well adapted to this environment, but equids should not be considered the pinnacle of adaptation to open environments; they retain basal tropical forest traits and lack certain derived open environment traits. Also, equids should not be considered some “non-ruminating ruminant”: their physiology is very different from that of the artiodactyls with which they are often compared; in particular, they are much better at digesting starch and other soluble carbohydrates. We present four storylines on why extant equids may be absent from tropical rainforests: one centred on carbon dioxide, one on chemical plant defence, one on metabolism, and finally a parasitism storyline. Storylines are helpful to envisage how things could have evolved but, of course, do not provide proof.

J. F. de Jong (✉) Wildlife Ecology & Conservation Group, Wageningen University, Wageningen, The Netherlands e-mail: [email protected] H. H. T. Prins Department of Animal Sciences, Wageningen University, Wageningen, The Netherlands e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 H. H. T. Prins, I. J. Gordon (eds.), The Equids, Fascinating Life Sciences, https://doi.org/10.1007/978-3-031-27144-1_4

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Modern Equids Are Absent from Forests and Some Other Habitats Extant equids, of which the horse is seen as the textbook example of ungulate adaptation to grassland conditions (MacFadden, 1993; but see Janis et al., Chap. 3 and Kaashoek et al., Chap. 13), are conspicuously absent from extant tropical (lowland) rainforests (Fig. 4.1a). Yet these types of forests were the ‘cradle habitat’ of the Perissodactyla (see Solounias & Semprebon, 2002) (Fig. 4.1b, c). Presently, wild equids have a rather limited geographic range, namely, the savannas, grasslands and semi-deserts of southern and eastern Africa, southwest and Central Asia (Fig. 4.2a, b). Intriguingly, equids are absent from the WestAfrican savannas even though Equus mauritanicus occurred further north, and only recently became extinct (Faith, 2014). Wild equids are even absent from the modern American grasslands, where most of the evolutionary history of the equids took place (Librado & Orlando, 2021; Prothero & Schoch, 1989, 2002; NarcarinoMeneses, Chap. 5). Also, equids are completely absent from forests—whether

Fig. 4.1 (a) Rainforest floor in Gabon, Africa. Whereas rainforests of Gabon are home to large herbivores such as African elephants and bongo, zebras are absent (photo credit: Axel Rouvin under CC BY 2.0 (https://creativecommons.org/licenses/by/2.0/). (b) Propalaeotherium voigti belonged to a genus of ancestral horses that was native to both Europe and Asia during the early Eocene. It weighed about 10 kg and stood some 50 cm tall. This species foraged on seeds, fruits and foliage, and was found in the Messel Pit, Germany. ©Hessisches Landesmuseum Darmstadt, photo: Wolfgang Fuhrmannek, HLMD. Used with kind permission. (c) Artist impression of P. voigti on basis of a CT-scan of the fossil material by M. by A. Andikfar and J. Lauströer. ©Hessisches Landesmuseum Darmstadt, photo: Wolfgang Fuhrmannek, HLMD. Used with kind permission

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Fig. 4.2 (a) The kiang or Tibetan wild ass (Equus kiang), a modern representative of the Equidae lineage. Courtesy of Charudutt Mishra. (b) Equus kiang in typical Equid habitat. Has this modern equid lost (part of) the suite of basal traits that enabled ancestors to survive in tropical closed rainforests? Or possibly, do derived traits that enable existence in this open landscape preclude existence in tropical rainforests? Courtesy of Charudutt Mishra

temperate or tropical. Ostensibly, this range limitation matches the stereotypic image of the equid as the hypsodont and unguligrade pinnacle of evolutionary adaptation to open environments (for contrasting views see Cantalapiedra et al., Chap. 2; Janis & Bernor, 2019; Janis et al., Chap. 3). Yet, the question as how present-day adaptations of equids preclude their return to these forests—and particularly into their ancestral, basal environment of tropical lowland rainforests—has received little to no attention. The reader perhaps raises one or even two eyebrows with the image of a zebra in a closed tropical lowland rainforest; being a large-bodied cursorial grazer, a zebra in such a forest may appear to be like a fish out of water. Yet, a ‘tropical rainforest zebra’ is precisely the apparition that we, the authors, have in mind when writing this chapter. Organismal evolution can move, and has been moving, in unexpected and often surprising directions. For instance, fascinatingly, some land mammals took to the sea again after spending part of their evolutionary history on land (Cetacea—see Thewissen, 2014), but their adaptations to a marine life are based on existing ones from their time on land. Jumping to another wonder of the animal kingdom, we posit that if the speciose group of tree-kangaroos (Dendrolagus spp.) had not existed, no one in their right mind would have imagined a hopping, folivorous, canopy-dwelling mammal with padded feet (see Martin, 2005) (Fig. 4.3). We suspect that if treeclimbing, canopy-hopping, folivorous horses had existed, their existence would have been ‘explained’ away by evolutionary biologists (cf. Gould & Lewontin, 1979). In the same vein, if tropical forest equids had existed, many an ecologist would have taken this as a ‘logical’, and even ‘inevitable’ outcome of evolutionary history. With this in mind, we wondered: why are there no tropical rainforest zebras? Ultimately, we believe that contemplating this question can give new perspectives on equid adaptations and, more generally, ungulate ecology and evolution (cf. Markman & Wood, 2009). We focus on the question ‘Why equids do or did not reinvade these forests?’ and not on the question ‘Why equids did not survive in these forests?’. Our focus enables us to investigate the repercussions for forest life of the current suit of

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Fig. 4.3 Evolution can ‘hop’ into surprising and ostensibly ‘illogical’ directions: Ancestors of this tree kangaroo (Dendrolagus lumholtzi), photographed in Queensland, Australia, became tree dwelling not long after acquiring traits for more efficient locomotion on plains (photo credit: Eric Gropp (https://www.flickr.com/photos/egropp/36399405715/), licensed under CC BY 2.0 (https:// creativecommons.org/licenses/by/2.0/)

existing traits instead of speculating on traits that did not evolve, or which are not known. In this chapter, we integrate a study of the literature with a comparative approach, to probe which vanished primitive (in the sense of ‘ancient’) traits, and which acquired, derived traits, may prevent extant equids from inhabiting tropical forests (Fig. 4.4). Throughout this chapter we apply a broad approach in which we consider multiple basic needs of endotherms in the context of life in tropical lowland rainforests, viz., How to stay hydrated? How to stay warm? How to stay well-fed? How to stay safe? And: How to stay healthy (i.e., without too many parasites or pathogens)? We focus on megaherbivores (≥1000 kg) and large herbivores (100–

Why There Are No Modern Equids Living in Tropical Lowland Rainforests

Fig. 4.4 A conceptualization of organismal traits of ungulates, such as may be expected in tropical forests on the one hand (left) and open environments (grasslands and deserts) on the other hand (right). In most traits, equids are adapted towards the open environment, yet further specialization is possible. See main text for details and explanation

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⁄ Fig. 4.5 (continued) and fire. They are highly indigestible for terrestrial herbivores and can thus be considered as antifeedants. (b) Chemical structure of a part of cellulose. Cellulose, together with many other forms of carbohydrates, form the main part of the structure of leaves of plants. They can be digested by many terrestrial herbivores with the aid of microorganisms. Digestion takes much time. (c) Examples of the chemical structure of phenolics. Phenolics are antifeedants in many tropical rainforest plants (source: S. Kiokias and V. Oreopoulou, Molecules 2021, 26(17), 5405; https://doi.org/10.3390/molecules26175405; published under CC BY 4.0 (https:// creativecommons.org/licenses/by/4.0/)

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a

b

c

Fig. 4.6 (a) Bongo occur in African tropical rainforests. Bongo typically forage on grass in forest clearings and may be considered ‘hostage of the forest’. Photo Credit: Mathias Appel, CC0 1.0 Universal Public Domain Dedication. (b) Okapis in the Antwerp Zoo, Belgium. While this mother and offspring are members of a captive reservoir population, their wild conspecifics can be considered ‘hostages of the forest’ (photo credit: Alan Eng under CC BY 2.0 (https:// creativecommons.org/licenses/by/2.0/). (c) African forest buffalo (or dwarf buffalo) in Loango National Park, Gabon. Forest buffalo occur in African rainforests but forage along forest roads and in clearings. They are not ancestral to savanna buffalo and only recently invaded the rainforest environment (photo credit: Kurt Kundy under CC BY 3.0 (https://creativecommons.org/licenses/ by/3.0/)

well (Vanleeuwe & Gautier-Hion, 1998). Lions (Panthera leo) were rumoured to still exist a few decades ago in savanna patches deep in the rainforest zone of Gabon (pers. obs.), and recently a male encountered here proved to be related to Namibian

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or Angolan lions, and not to lions further to the north (Barnett et al., 2018). Even though rarely observed in large forest clearings, the okapi appears out of place in the rainforest: the okapi paces from (small-sized) tree fall gap to tree fall gap much as the giraffe (Giraffa camelopardalis) paces from freestanding acacia to freestanding acacia in the savanna. As asserted by Kingdon (1990, pp. 192–194) ‘... there are numerous species that have undoubted savanna origins that remain enmeshed [in the rainforest of Congo] today (a relatively humid period). [...] Of the larger savanna mammals that have been engulfed by the forest, the best known is the okapi [...]. It has been established from Pleistocene fossils that okapis and okapi-like giraffes once ranged widely through the African moist savannas’. Just as the relictual distribution of the gemsbok (Oryx gazella) and the East-African oryx (O. beisa) (a disjunct species pair) is indicative of a historic dry savanna connection (Kingdon, 1990, p. 17) the existence of the okapi may be a testimony of drier conditions (Kingdon, 1990, p. 194) or lower CO2-levels (cf. Schefuß et al., 2003) in the Congo basin in the recent past. If this portrayal of ‘prisoners of the rainforest’ is a valid one, then many a large ungulate that happens to live at present in a tropical rainforest should not be taken as standard for what would constitute a well-adapted large rainforest mammalian terrestrial herbivore. Nevertheless, through their existence and persistence, large tropical forest ungulates invalidate various traits as factors which limit for tropical rainforest existence. By considering relevant animal traits of ‘forest prisoners’, we can potentially obtain insight into what traits are not necessarily limiting the survival in tropical rainforests. While considering Asian elephants (Elephas maximus) in oriental forests, Wallace (2004) observed that ‘It seems arbitrary that mammoth-toothed Asian elephants survive by browsing in forests when mastodonts, whose cusped molars were adapted mainly to forest-browsing, are extinct’. Applying Popperian reasoning, this one observation by Wallace suffices to disprove the hypothesis that hypsodont teeth per se precludes existence in rainforests (see also Cantalapiedra et al., Chap. 2; Janis et al., Chap. 3). We can extend the same logical argument to the traits of okapi and other ‘forest prisoners’. It follows that toe reduction and limb lengthening, and cursoriality in general, do not preclude forest existence (c.f., Kaashoek et al., Chap. 13). Equally, large body size does not rule out a rainforest existence. Each of these traits may indeed hamper the return to the tropical rainforest, but not completely prevent it. Despite having the wrong ‘toolkit’, a species may be able ‘to muddle along’. The implication is that it is not because of their large size, their specialized legs or their hypsodont teeth that equids are not part of the scene in tropical forest clearings, let alone the forest interior itself. All of this indicates that the acquisition of advanced animal traits does not necessarily preclude the existence of advanced ungulates in rainforests. Various (sub)families with recent origins in (semi)open environments show that adaptation and/or acclimation back into tropical forests is possible, even by ungulates forms with strong grazing adaptations. These (sub)families include the Elephantidae, the Rhinocerotidae, the Giraffidae and the Bovini (wild cattle) and Tragelaphini (spiralhorned antelopes). When considering two pivotal traits, namely digestive strategy and life history, it appears that the hindgut fermenting Elephantidae and

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Rhinocerotidae have a slow life history (high longevity and slow reproduction), Giraffidae are ruminants with a slow life history, whereas Bovini and Tragelaphini are ruminants with a fast life history. The only large tropical ungulates that combine hindgut fermentation with a fast life history are the equids (see more below).

(iii) Traits of ‘True’ (Perissodactyl) Tropical Forest Ungulates We define true forest forms as species that have an ancestral line with a long (tens of millions of years) and uninterrupted existence in forests. Because forests are ‘old’ habitats (as opposed to the recently developed open environments), forest animals with such a long, interrupted existence likely represent the basal form, or at the very least retain primitive traits. It appears that these true forest forms still exist! As Geist (1978, pp. 179) noted, ‘[lineage] survival is associated with old, stable, productive habitats such as the tropics and subtropics’. Therefore, there are quite a lot of true extant forest herbivores. For mammals more broadly, Dasyproctidae (agoutis Dasyprocta spp.] (Fig. 4.7a) and achouchis [Myoprocta spp.]) (Fig. 4.7b) are possibly representative for small terrestrial herbivorous rainforest mammals. For Artiodactyla, the Tayassuidae (peccaries) and Suidae (pigs)—although having many non-forest species—could be considered basal. Within Pecora (the ruminant Artiodactyla), the Tragulidae (chevrotains) qualifies as true tropical forest form. Following the abovementioned criteria, duikers (Cephalophus) do not represent true archaic forest forms, as they form a secondary radiation. Putative advanced traits—associated with re-adaptation to rainforests—of duikers are, amongst others, large brain size and long gestation periods (Gentry, 1990: p. 225). Regarding the question as to why Artiodactyla, in the form of duikers, were able to adapt to tropical rainforests, Janis (2007) pointed out that ‘in contrast to Perissodactyls, Artiodactyls have had a significant radiation of medium- to large-sized omnivorous forms. This may relate to the fact that early artiodactyls retained a bunodont dentition, later

Fig. 4.7 (a) Central American agouti (Dasyprocta punctata) in Panama (photo credit: Geoff Gallice under CC BY 2.0 (https://creativecommons.org/licenses/by/2.0/). (b) An agouti foraging (photo credit: Brain Gratwicke under CC BY 2.0 (https://creativecommons.org/licenses/by/2.0/)

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Fig. 4.8 (a) An adult Tapirus pinchaque (photo credit: Patricio Pillajo. Location: Papallacta, Cayambe-CocaNational Park, Napo province, Ecuador; courtesy of Springer Nature). (b) This young Tapirus pinchaque in Equador illustrates how an Eocene ancestor of horses could have looked like (photo credit: Luis Gómez. Location: Cuyuja, Cayambe-Coca National Park, Napo province, Ecuador; courtesy of Springer Nature)

elaborated on in the more specialized larger omnivores. In contrast, the early radiation of perissodactyls consisted entirely of forms with more derived, lophed cheek teeth, adapted for a more folivorous diet. It may be the case that the morphology of lophed teeth cannot easily be reversed into a bunodont form, making a radiation of omnivorous perissodactyls unlikely’. Continuing our discussion of archaic forms, the Perissodactyla have true forest form representatives in the Tapiridae as well as one, arguably, in the Rhinocerotidae, namely the Sumatran rhinoceros (Dicerorhinus sumatrensis). Indeed, due to evolutionary change, all the aforementioned animals may differ somewhat from the true basal forest forms, yet we will focus on their many conserved, archaic traits—not their derived traits. Of all ‘archaic animals’, the tapir (Fig. 4.8) arguably represents the best stereotype of a large tropical forest ungulate. The tapir family persists in rainforests for tens of millions of years in largely unchanged form. Tapirs show several traits that hark back to a long-gone era. From a behavioural perspective, it is remarkable that tapir mothers lie down when the young suckle—which is uncommon in derived ungulates. It is a trait they share with pigs and peccaries. Also, as remarked upon by Janis (1984), ‘in laying down, tapirs first adopt a position of sitting on the haunches, a behaviour typical of primitive ungulates and rarely seen in equids or ruminant artiodactyls, which support themselves on the carpus when adopting this position’. Morphologically, basal traits are the tapir’s barrel-shaped body, with hindquarters higher than the shoulders, and the morphology of limbs (short) and foot (retaining of toes; four toes on each front foot, three on each back foot). Turning towards (behavioural) ecology, the tapir has a solitary lifestyle, a tendency to use water pools and mud baths putatively to cool down and to combat parasites, a selective foraging strategy of the few acceptable nutritious leaves available, a slow pace of life (and hence, probably a relative slow metabolism) leading to a relatively long lifespan and long gestation times (Medici et al., 2008).

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Fig. 4.9 Chemical structure of a hydrolyzable tannin (a) and of a condensed tannin (b). Note that tannins do not have fixed atomic mass and can form much longer chains than shown here. Tannins are good in binding proteins, making them not well digestible. From Lochab et al. (2014). Courtesy of RSC Publishing

Lastly, the tapir has a thick hide—because of which it originally was placed in the abolished taxon of Pachyderms—which perhaps is an explanation for the low predation rate by jaguars (Panthera onca) (Weckel et al., 2006). Relatively little is known about foraging behaviour and digestive physiology of true tropical forest ungulates. For tapirs, for example, little more is known than that their diets are broad (diverse and includes leaves of many plant species, as well as fruits and seeds). Yet tapirs are selective in the sense that they only pick particular leaves (Bodmer, 1989; Hibert et al., 2011; Salas & Fuller, 1996). For more specific nutritional considerations, we, therefore, must make inferences from related, not necessarily true, tropical forest ungulates. We could not find any mention of tapirs or rhinos digging for tubers or rhizomes that are rich in carbohydrates, even though rainforests and savannas can contain good food from subterranean sources (Bailey & Headland, 1991; Barton & Paz, 2007; Marlowe, 2002), which may explain their absence of hooves. The well-known habit of forest-living rhinoceroses and tapirs of visiting ‘salt licks’ (many of which are not salty but clayey only, pers. obs.) may be related to the ingestion of fine clay particles for binding nitrogen-based compounds (in particular, alkaloids and cyanogenic glycosides) that are present in many browse species (compare the composition of traditional ‘hunger food’ of pygmies in African rainforests) (Kreulen, 1985; Montenegro, 1998). This is a subject area of which many unexpected results can be found before a general pattern is distinguished (see Naude et al., 1997). Apart from visiting ‘salt licks’, how do tropical rainforest ungulates cope with plant secondary compounds? As discussed above, plants of tropical rainforests mainly invest in carbon-based secondary compounds (like phenols, tannins, resins, and oils) (see Figs. 4.5c and 4.9) rather than nitrogen-based ones. In artiodactyls, plant chemicals enter the rumen. Carbon-based secondary compounds disrupt

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digestive processes and prolong gut retention time (e.g., Van Soest, 1982, pp. 263 ff). Nitrogen-based secondary compounds, on the other hand, are degraded in the rumen, through which uptake of these compounds in the blood stream and subsequent toxic effects are prevented. Perissodactyls, in contrast, suffer more from the effects of nitrogen than from carbon-based secondary compounds; for want of a rumen, nitrogen-based compounds can easily enter the bloodstream (Guthrie, 1990, pp. 297). However, the disruptive digestive impact of carbon-based secondary compounds (like tannins, oils, and resins)—the dominant plant defence in tropical forests—can be lessened, to some extent in perissodactyls, by shunting the digestive food mass directly towards the colon thus bypassing the caecum (Guthrie, 1990: p. 267). This comes at the expense, of course, of gaining energy from digesting fibre in that caecum. Furthermore, we expect that tropical forest ungulates would have large livers to deal with nitrogen-based compounds, as well as well-developed saliva-binding capacities to neutralize nitrogen-based secondary compounds. Although being a savanna browser, the black rhinoceros (Diceros bicornis) may be representative of the strategy of tropical herbivores to deal with plant defences. Black rhinoceros appear to have a relatively large liver. Generally, the interspecific scaling of liver mass (kg) is 0.033 × M0.87 (M, body mass, in kg) (Daugirdas et al., 2008 based on Stahl, 1962; see Crile & Quiring, 1940). With 14.3 kg, the liver mass of a 763 kg black rhinoceros (the Table in op. cit.) is 35% heavier than expected. This liver was 1.9% of the rhino’s BM but those of the grazing adult horses were 1.2% (n = 11) like that of the African buffalo (n = 2); the African elephant of 6654 kg had a liver weighing 1.6% of its BM (ibid). Turning to carbon-based compounds, we expect that the black rhinoceros can cope well with tannins. Indeed, Loutit et al. (1987) did not find a relationship between tannin concentrations in plants and food choice in black rhinoceros. Apart from the caecal bypass (like all hindgut fermenters), this might be explained by the finding that the Black rhinoceros has a higher tannin-binding capacity of their saliva than does the grass-eating white rhinoceros (Ceratotherium simum) (as expected) (Clauss et al., 2005). In addition, the black rhinoceros can react by increasing the tannin binding capacity of the saliva to higher levels when the food has more tannins (Clauss et al., 2005). This contrasts with browsing ruminants where the tannin binding capacity of saliva is not induced by more tannins in the diet (Clauss et al., 2003, 2005). Note that the tannin-binding capacity of the saliva is considered to be an ancestral trait (McArthur et al., 1995). Also, the one-horned rhinoceros (Rhinoceros unicornis) has high tannin-binding capacity in its saliva (Clauss et al., 2005) even though they often forage on carbohydrate-rich basal areas of tall grasses (Fig. 4.10). So, on the basis of the knowledge of the diet of the most ancient equids, and because of the comparison with the extant Perissodactyla, we posit that the ancestral Equidae had saliva that was able to bind the tannins in their food.

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Fig. 4.10 (a) Grazing mother and calf one-horned rhinoceros in the lowlands of Nepal. They forage on Saccharum spec. (photo credit: Shyam Thapa). (b) Grazing one-horned rhinoceros bull in the lowlands of Nepal. Note that he forages on Saccharum spec. (the tall grass) and not on the short lawn grasses as a white rhino would do (photo credit: Umesh Paudel)

(iv) Equids: A Mixture of Basal Forest and Advanced Grassland Traits Apart from the often-mentioned traits of hypsodonty, unguligrade posture, and high mobility, what are equid traits that are associated with a non-tropical forest existence (Fig. 4.11)? It appears that equids have lost various primitive traits that may have been adaptive in tropical forests, yet less relevant or even maladaptive in open environments. Equids have moderately sized livers, compared to large livers in black rhinoceroses—possibly limiting detoxification of nitrogen-based compounds. Grazing adaptations appear to include a lower capacity to deal with plant secondary compounds. Because grasses have low levels of these compounds, the necessity to have adaptive traits to cope with these may have disappeared (Searle & Shipley, 2008). However, even though the traits associated with this may have become obsolete, it does not necessarily mean that these cannot be ‘hidden traits’ as exemplified by our experiments with Burchell’s zebra (Equus burchellii) and polyethylene glycol (PEG) (Fig. 4.12) in association with polyphenols and tannins in plants available to them. Horses and zebra, and presumably other equids, are not good at coping with tannins and phenols in their diet (although kulan [E. hemionis] also forages on shrubs and herbs: Wenxuan et al., 2009). First, the tannin-binding capacity of the saliva of zebras is low as compared to rhinoceroses (Ward et al., 2020). The production rate of saliva scales with body mass to the power 0.87, but the variation is not negligible between species (Virot et al., 2017). Second, in an experiment with free-ranging Common zebra in a sour veld in South Africa, where we gave Burchell’s zebra and other herbivores access to PEG feed blocks (Fig. 4.12), zebras changed their diet from about 0% browse to 30% in the dry season (Schroder, 2021). PEG is very efficient at binding tannins in the feed (see Mkhize et al., 2016,

Fig. 4.11 A visual overview of some of the adaptations of equids to open environments, such as hypothesized in this chapter. Boxes represent environmental or organismal characteristics, and arrows represent causal relationships. See main text for details and explanation

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90 Fig. 4.12 (a) The chemical structure of Polyethylene Glycol (PEG). The suffix ‘n’ denotes that the central part of this molecule can be repeated variably. PEG can bind tannins in plant material while a herbivore is masticating its food, thus preventing proteins from becoming immobilized. (b) Greater kudu (pictured in Welgevonden Game Reserve, South Africa) like most other herbivores readily take feed blocks also when enriched with polyethylene glycol (PEG) (photo credit: Thuto Ngongwane). (c) Burchell’s zebra in Welgevonden Game Reserve (South Africa) in a very dystrophic ‘savanna’. Foliage of woody species is very rich in astringent tannins. This is not a habitat that matches the textbook image of fleetfooted equids in a grassy plain, yet the zebra thrive here (Photo credit: Sam Davidson-Phillips). (d) Burchell’s zebra in Welgevonden Game Reserve (South Africa) started browsing after consuming feed blocks containing PEG (photo credit: Sam DavidsonPhillips)

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Fig. 4.13 In some vegetation types in the temperate zone, nettle (Urtica dioica) can become dominant in the understory. A large part of the winter diet of feral horses can be formed of their roots (photo credit: Ecopedia. https://www.ecopedia.be/natuurtypes/natuurtype-essen-elzenbosmet-grote-brandnetel)

2018). This demonstrates that Burchell’s zebra do not have an intrinsic avoidance of browse, but that they cannot cope with the browse tannins. It is often overlooked that horses are extremely good at digesting starch (with a maximum recommendation of 1–2% of their body mass as daily intake (Ellis et al., 2010; Geor, 2010; NRC, 1989); this is equal to about one-third to two-third of their food intake but that level should not be exceeded because of risk of cholic (Geor, 2010). Horses are also very good at digging for roots. For example, roots of Urtica can make up a large proportion of horses’ winter diet in the Netherlands (GrootBruinderink et al., 1999); Urtica roots and rhizomes can attain an underground mass of 3500 kg ha–1 (ibid) (Fig. 4.13). In the roots of a related nettle species in China, high sugar concentrations and some starch was found (Zhang et al., 2013). Equids are excellent diggers. For example, donkeys can dig wells much deeper than most other desert mammals. Horses can dig for wild carrot roots, celery roots, etc., and even dig up some wild garlic and onion species in Central Asia (pers. obs.), although these latter may be poisonous in large quantities (they contain N-propyl disulfide which is poisonous for horses but may function as an anthelminthic). Carrots (Daucus carota—also occurring in C. Asia), for example, have a high sugar concentration (Brøkner et al., 2012) and are an excellent food for horses (Nieschling, 1935). Feeds like carrot were found to be good for endurance racing of horses (Goachet et al., 2012). This brings to the fore that equids should not be considered some ‘non-ruminating ruminant’: their physiology is very different from that of the artiodactyls with which they are often compared, and that it is not merely about

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cellulose digestion that one should be concerned. Indeed, temperate Lolium perenne under sunny conditions with low temperature can contain up to 30% fructans (Geor, 2010). Fructans are 100% digestible (Van Soest, 1982: pp. 102) and yield fructose upon digestion (ibid, pp. 104). Tropical grasses do not store fructans. In other words, a grazing horse in the temperate zone can have an intake of some 5 kg of fructans per day (Geor, 2010) thus about half their daily DM intake. The resulting fructose is absorbed into the blood in the small intestine and fermented in the hindgut (Geor, 2010; Merediz et al., 2004). Fructose is rapidly converted into glucose in horses (Bullimore et al., 2000). Intriguingly, it appears that in horses the concentration of insulin is lower after consuming fructose than glucose (Bullimore et al., 2000; Merediz et al., 2004); high insulin levels may inhibit lipolysis (Bullimore et al., 2000): in other words, endurance may be augmented by consuming fructose as compared to glucose. A large number of temperate plant species with edible tubers and rhizomes may go unrecognized as food material by many herbivore ecologists (e.g., Turner et al., 2011), and that is why we believe that recognizing ‘tubering’ (as additional to ‘grazing’, ‘browsing’, etc.,) is important (see Box 4.1). Horses, of course, are very good at cratering in the snow, where sheep and cattle (ruminants) would perish (Anthony, 1994). Also, kulans are good at digging (Qing et al., Chap. 8), as are donkeys and horses (Lundgren et al., 2021). Box 4.1. Classifying Terrestrial Herbivores Since Reino Hofmann (e.g., Hofmann, 1989; Hofmann & Stewart, 1972) distinguished three main groups of terrestrial herbivores (namely, browsers, mixed feeders and grazers), Nikos Solounias played a pivotal role in finetuning this classification (e.g., Solounias & Moelleken, 1992). Where Hofmann focussed on the digestive system, Solounias studied meso- and microwear of the masticatory apparatus. This yields new insights because the richer taxonomy of feeding classes facilitates improved understanding of mammalian herbivores. One realizes that a classificatory system has to find an optimum between the number of categories (‘not too many’), and the number of species (‘very many’) (cf. Gordon & Prins, 2019). We posit that for classifying terrestrial herbivores, herbivore ecologists should broaden their classes to seven (based on Solounias & Semprebon, 2002; we changed their ‘rooters’ into ‘tuberers’) to better analyze different feeding strategies: (i) (ii) (iii) (iv) (v) (vi) (vii)

Fruit and seed browsers Bark, coarse stem, and leaf feeders Tuberers Seasonal switching mixed-feeders ‘Meal-by-meal’ mixed-feeders C3-grazers C4-grazers

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Moving on to parasitism, and based on responses to flies, it appears equids poorly deal with parasites. In many places where tsetse flies (Glossina spp.) occur there are no zebra at all, such as in the savannas of West Africa and parts of the tropical rain forest. We will deal with this further below (‘the parasitism story line’). Among the equid traits acquired in response to living in a non-forested environment is the capacity to sweat. Sweating is maladaptive in humid environments, and possibly equids cannot properly shed heat in the typically humid tropical forests. Another advanced trait is ‘speeding up’ of life history through a reduction in the gestation length, possibly to align reproduction with seasonality. The gestation period of equids is 11–13 months, compared to 13 months in the smaller-bodied tapir, and 15 months or longer in rhinos (Geist, 1998). In general, metabolism is relatively high in equids—which may be a consequence of their high mobility. Equids need to be mobile to travel from food patch to food patch, and, of course, to outrun pursuit predators (see also Rubenstein, Chap. 12). The high metabolism can be inferred from the high body temperature of equids, which averages between 37.5 and 38.5 °C - similar to (or close to) that of supraendotherms. In contrast, other Perissodactyls (rhinoceroses and probably tapirs too) appear to be baso- or mesoendotherms (Lovegrove, 2012a, 2012b, 2016). Similar to the pronghorn (Antilocapra americana), the supraendotherm pur sang, horses have a high muscle aerobic capacity (Withers et al., 2016: p. 158). To fuel high metabolism, equids have high intake requirements. It is well known that equids have a higher food intake (dry weight intake of approx. 3% of body mass: Ellis et al., 2010) than grazing ruminant Artiodactyls (dry weight intake of approx. 2% of body mass). On top of this, we expect that equids have a larger intake than other Perissodactyls do, to meet high their metabolic requirements. Even though empirical data are scant, Fig. 4.7a in Meyer et al. (2010) seems to indicate that wild equids have indeed a higher intake than sheep (Ovis aries) and cattle. Nevertheless, compared with other ungulates, equids are not ‘optimally’ adapted to open environments. Unlike Artiodactyla, equids cannot regulate their brain temperature through a carotid rete (Mitchell et al., 2002), or even use horns to cool their brain (Mitchell & Lust, 2008; Taylor, 1966). Moreover, partly due to the reliance on sweating during thermoregulation, water metabolism is rather inefficient (Cheeke & Dierenfeld, 2010). Reliance on water resources and the absence of a carotid rete are primitive traits that likely stem from tropical forest origins when they still were small-bodied and thus had a relatively large surface area. The fact that an effective brain cooling system did not evolve in equids does not show that there is no negative effect of such a lack of adaptation but highlights that natural selection could not lead to a better adaptation because there was no trait to be honed to perfection. The ‘equid Bauplan’ did not have it in store, as it were (cf. Janis, 2009)

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Equids in Tropical Forests: Storylines on Limiting Factors By comparing equid traits with the traits of ‘true’ tropical rainforest ungulates (see section iii), as well as with characteristics of tropical lowland rainforests, we have come up with several thoughts on what may, and may not, explain the absence of equids in these forests. Obviously, basal traits that have been retained over time, such as the reliance on water, are unlikely candidates (because in tropical lowland rainforests, surface water is at many places ubiquitous). Equally, unlikely candidate traits are those that are maladaptive in tropical forests yet can easily be acquired (or: restored—not to be confused with devolution). Examples of such traits may be coat colouration and patterning, as well as body morphology. Forest ungulates tend to have coats with a dark reddish colour, compared to black in woodland ungulates, and tan in treeless savanna and desert ungulates (Caro, 2005). Coat colour, however, appears to be easily modified, as strikingly shown by the blackish forest and reddish savanna subspecies of the African buffalo. That this may also apply to equids is illustrated by the rare though regular occurrence of ‘aberrant’, juvenile dotted coats reminiscent of young tapirs in zebra populations (Bard, 1981). Palaeogenetics shows that prior to its post-Pleistocene extinction, natural selection favoured black individuals in the European wild horse when forests expanded (Sandoval-Castellanos et al., 2017) (Fig. 4.14). Similarly, a shift in body conformation from pronounced

Fig. 4.14 Black koniks (‘tarpan’; feral European horses) in the Oostvaardersplassen Nature Reserve (the Netherlands). The genetic variants causing a black coat in the wild European horse spread through the population just before its extinction. Photo credit: ©Arndt Bronkhorst, Arnd Bronkhorst Fotografie ([email protected])

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forequarters suited for endurance (beneficial in open terrain) (Estes, 1991; see Kaashoek et al., Chap. 13) towards well-developed hindquarters that facilitate movement through the forest understorey, as well as explosive leaps, may ‘merely’ be a minor evolutionary transition—as evidenced by the eland antelope (Taurotragus oryx) and greater kudu (Tragelaphus strepsiceros) on one hand, and the bongo on the other (all members of the tribe Tragelaphini). Body conformation is, in fact, a selected trait in domestic horses, and substantial variation can be seen among breeds. As geneticists start understanding much more about gene silencing, and how that can be reverted (e.g., Deng & Ménard, 2020; Hurst et al. 2004; Preuss & Pikaard, 2007; Sutherland et al., 2000; Talon et al., 2019), it may be time to rethink Dollo’s Rule, just as Cope’s Rule was laid to rest (see Cantalapiedra et al., Chap. 2). Furthermore, there are equid traits that are potentially modified to function in open environments, and hence not optimal in tropical forests, but which nevertheless are not causing enough ‘disadvantage’ to preclude existence in tropical forests altogether. One such trait may be the equids’ tendency to wallow in combination with the acquisition of hooves. Whereas wallowing aids thermoregulation and parasite control—both of which are important capacities in tropical rainforest (see more below)—it may become a dangerous act for the one-hooved (rather than padded) equids if carried out in mud pools instead of on sand beds. Mortality due to getting stuck in mud pools is not uncommon in equids (e.g., Guthrie, 1990; Haynes, 1995; Vereshchagin, 1974; Weigelt, 1989). This illustrates another important point: traits interact. Likely, it is not one single trait that limits animal distributions but a combination of traits (see, for instance, Braz et al., 2021; Marderstein et al., 2021; Prokkola et al., 2018; Sutherland et al., 2019). Turning to factors that may explain the absence of equids in tropical forests, we would like to present four storylines, which we refer to as the carbon dioxide storyline, the chemical defence storyline, the metabolism storyline and the parasitism storyline.

The Carbon Dioxide Storyline This storyline links the abovementioned appetite of equids for starch with potential starch content changes in plant material, due to variation in carbon dioxide levels. During the Eocene, when the Perissodactyla arose, atmospheric carbon dioxide levels were much higher than they are today, at about 2000 ppm (Pearson & Palmer, 2000). What are the effects of elevated CO2-levels for the diet of equids, thereby considering that, as highlighted above (e.g., see Box 4.1), modern equids can well consume tubers, roots, and seeds? With elevated CO2-levels, total non-structural carbohydrates (i.e., sugars and starch) increase in leaves of C3 wild grasses, but not so in C4 wild grasses (Wand et al., 1999). Also, with elevated CO2-levels, N-content in leaves of C4 grasses does not change, but in C3-grasses it decreases (Wand et al., 1999). Under P-deficiency

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(often occurring in tropical grasslands and forests), the starch content increases in C3 grasses but appears to decrease in C4 grasses (Halsted & Lynch, 1996). An increased water deficit leads in Panicum maximum (a C4 grass) to elevated sugars; increased temperatures and irrigation leads to very low sugar contents and very low starch contents too in C4 grass (Habermann et al., 2019). Finally, nitrogen deficiency leads to elevated starch content and reduced N-levels and more or less level sugar concentrations in C3 plants (Stitt & Krapp, 1999). Due to earlier described intense competition and high growth rates, modern rainforests are generally N-deficient. The former has ramifications for understanding the effect of the emergence of C4-grasslands and the evolution of modern horses. If the ancestral niche of the medium-sized forest-dwelling horses was associated with a switch from fruit and browse eating towards more grass (so a bit like the modern okapi), they were doing that on a C3-grass diet (because C4-grasses had not evolved yet) in a tropical environment with higher temperatures and higher CO2 levels than today. In other words, we posit that the ancestral grass niche of these horses led to them feeding on grass with a much higher starch content and possibly higher sugar contents too, facilitating this switch from frugivory to graminivory. A ‘return to the ancestral tropical forest’ may thus be hampered by the present-day low global temperatures and low CO2-levels as compared to those in the Eocene. This may also explain why equids went extinct in their ancestral tropical rainforest. The ancestral diet of Eocene Perissodactyls was mainly C3-grasses and fruits (Solounias & Semprebon, 2002). However, the sparse occurrence of these C3-grasses in a modern tropical rain forest, and their low modern starch and sugar content would have precluded the survival of these ‘primitive’ animals, unless they had become much smaller (say, the size of a royal antelope [Neotragus pygmaeus] of some 2 kg only).

The Chemical Defence Storyline That equids can evolve into browsers is shown by the extinct Pleistocene hippidiforms of South America (Bernardes et al., 2013; Janis et al., Chap. 3). However, tropical forest leaves do not necessarily equal savanna leaves. For example, fine-leaved savannas, which typically have a much higher ungulate biomass than broad-leaved savannas, are typified by large investment in structural defence (thorns and spines) and high quality (Gambiza, 2001; Tomlinson et al., 2016). If nutritional aspects of browse are the limiting factor for the tropical forest existence of equids, then these are specific to the qualities of tropical forest leaves (and not browse in general). We posit that equids cope poorly with the carbon-based defence compounds that are so abundant in tropical forest leaves. Ruminants are generally better at coping with carbon-based compounds (cardenolides; they are also better at detoxifying N-based antifeedants such as alkaloids, glucosinolates and cyanogens) than are foregut fermenters, and equids also have a poor tannin-binding capacity of their saliva. In other words, we would expect equids, if they were living in tropical rain

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forests, to shun all dicot leaves and concentrate on the sparse graminoids. Our PEG experiments (referred to above; Fig. 4.12) point out that zebras are limited in their intake of tannin-rich food by the tannin-binding capacity of their saliva, so it would need quite some selection or mutations to enable equids to be as efficient as, e.g., black rhinoceroses, to deal again with the browse that is on offer in the tropical rainforest. Although nitrogen-based compounds are not the main defence strategy of tropical forest leaves, equids are sensitive to toxification due to the lack of a rumen and a putative loss in detoxication capacity of the liver.

The Metabolism Storyline This storyline builds on, and integrates the former storyline, and combines intake of energy and nutrients with expenditure thereof. As introduced above, equids have high metabolic rates with an associated active lifestyle and opportunistic life history (see above). In contrast, tapirs have low activity (Tucker et al., 2018), conservative life history (Kiltie, 1984) and—as speculated based on the low body temperature of rhinoceroses and the low cursoriality of tapirs—low metabolic rates (Lovegrove, 2012a, 2012b). We speculate that the high energy demands of the equids, which is likely a modification to the cursorial locomotion associated with open environments (Lovegrove, 2012a, 2012b), cannot be met by forage resources available in tropical forests. To satisfy requirements, equids have high food intake and show foraging behaviour during large parts of the day (whereas savanna ruminants are often crepuscular or diurnal, zebras are often active throughout day and night) (Veldhuis et al., 2020; see also Rubenstein, Chap. 12). This should not only be explained by the general higher intake rate of hindgut fermenters versus ruminants, or grazers versus browsers, but also by the supraendothermic body temperature and high metabolism of equids. Equids have adapted to become energetic herbivores with a high mobility, a capacity to outrun both ambush and pursuit predators, which partly may be explained by them keeping insulin levels low to continue mobilizing fat for energy release but also to cope with the enormous loss of body fluids (see above; cf. Antonia et al., 2021; Hess et al., 2007). They can forage on sugar-rich, starch-rich, and even fatty food, and are much less dependent on the slow energy release through cellulose digestion than are grass-eating ruminants. The high metabolism may have enabled a shortening of the gestation period, which may have been adaptive in the seasonal environment of savannas (in contrast to the stable tropical rainforest environment). Possibly, the energy expenditure of equids has become too high to allow for a tropical forest existence. The mortgage on an expensive mansion could serve as a metaphor, purchased during a period of high income—once such a mortgage is entered into, a person cannot afford a drop in salary. This principle applies to all endotherms, which, compared to ectotherms, have expensive, demanding lifestyles. Some endotherms, however, have an even more costly life than others. Indeed, this costly lifestyle does not apply so much to extant non-equid perissodactyls (tapirs and rhinoceroses), which have a low metabolism and conservative life history.

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Furthermore, it also does not apply to elephants and okapis, which also have a conservative life history, including long gestation periods. Finally, metabolism is not constraining for opportunistic bovids in tropical forests, such as the African buffalo, because rumination allows for a relatively low intake. An interesting, related observation is that Bos taurus indicus, as compared to Bos taurus taurus, is better able to cope with tropical conditions due to, amongst others, lower metabolic heat production (Withers et al., 2016: p. 319).

The Parasitism Storyline Although lacking (as yet) much empirical evidence, an opportunistic life history could be associated with a lower investment in the immune system (see for a comprehensive introduction, including consideration of innate vs. adaptive immunity, Valenzuela-Sánchez et al., 2021). An example may be the opportunistic elk (moose) (Alces alces), which has early sexual maturation, a tendency to give birth to twins and triplets, a high (though for deer not exceptional) milk fat and protein content, and fast development of young (see Geist, 1998). These traits possibly come at the expense of immune defence, given that the moose is notoriously susceptible to diseases (de Castro & Bolker, 2005; Geist, 1998: p. 228; Schmitz & Nudds, 1994). In the south, the range of the elk (moose) appears to be limited by the occurrence of the parasites carried by the white-tailed deer (Odocoileus virginianus) (Schmitz & Nudds, 1994). Similarly, there is circumstantial evidence that the immune system of equids is compromised, or at least, not able to cope with tropical disease load (or it is a strategy of high tolerance to parasites: Tombak & Rubenstein, Chap. 11). According to Osborn (1910, p. 507): ‘[...] the horse may have been swept out of existence by some epidemic disease or diseases. These diseases are carried by flies and are favoured by moist conditions occurring chiefly during or immediately after heavy rainfalls [...] The tsetse fly of Africa renders thousands of square miles unhabitable by horses . . . ticks, even when non-infection bearing, form absolute effective barriers to the introduction of quadrupeds into certain regions. [...] in certain regions of Africa ticks are practically fatal to horses. [...] thousands of ticks would sometimes gather on a horse as the result of a single night’s grazing. The mane especially serves to collect these pests’. Indeed, Law (1976) stated that: ‘[...] there were serious constraints upon the effective use of cavalry forces in West Africa. Tsetse are a problem in almost all areas of West Africa, except the extreme north, especially during the rainy season, and they made it virtually impossible to breed horses in the southern area. [. . .] The most southerly of the West African cavalry states, such as Gonja and Dagomba in northern Ghana and Nupe and the Yoruba Kingdom of Oyo in Nigeria, were, therefore, almost wholly dependent upon imports of horses from further north’. Furthermore, during the Iain Smith rule in Rhodesia (now Zimbabwe), the Burchell’s zebra was exported to the coastal savanna of Gabon (to the Wonga Wongué Presidential Reserve) in exchange for oil, but they did not survive

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(Blom et al., 1990). The fact that zebra did not persist, but also did not penetrate the Guinea Savanna west of Central African Republic, may point at range limitation by diseases (see Dennis et al., Chap. 10). In fact, in eastern and southern Africa, the distribution of zebra is the inverse of the occurrence of the tsetse fly. The stripes of the zebra have been tickling the inquisitiveness of ecologists though, resulting so far in 18 different ‘hypotheses’ (Horváth et al., 2018; Ireland & Ruxton, 2017) so the verdict about their functional meaning lies in the future. However, the distribution of some tsetse fly species closely follows the drought corridor, that bridges dry East-African and dry Southern African savannas. On this drought corridor, the stripe pattern is strongest (Caro et al., 2014). Stripes have been shown to deter flies effectively (Caro et al., 2019). The relaxation of stripes in the quagga (Equus quagga quagga) may thus perhaps be a response to lower insect harassment. This idea is contested though (Gibson & Young, 1991; Gibson, 1992; Hughes et al., 2015; Larison et al., 2015), but there is the possibility that zebra, and equids in general, have an elevated level of activity and (re)production, at the expense of investments in their immune system (see for more on this issue Tombak & Rubenstein, Chap. 11). Another perspective is that given that recent ancestors of extant equids lived at high latitudes, extant equids have adapted to other disease pressures than those in the tropics. Box 4.2. Browse Versus Grass, and Browsers Versus Grazers In science, one may need to simplify to conceptualize, but the simple contrast of browsers versus grazers is causing confusion (see also Gordon & Prins, 2019). First, the diet of herbivores comprises more than the leaves of trees and grasses. Herbaceous plants (herbs) other than grasses, in particular forbs, are a significant component as well. The same applies to tubers and seeds. We believe that one reason why diets of equids are poorly understood (as argued in the main text) is that many scholars perceive nutritional ecology of herbivores purely from the grazer versus browser dichotomy. On a similar note, the contrast browse versus grass may give the wrong impression that habitat types can be viewed as binary too, as closed woodland (or forest) versus grassland, as so often stated in palaeontological literature. Yet there are many habitats (e.g., miombo, thickets, marsh, broad-leaved vs. fine-leaved savannas, bushland, wooded grasslands, deserts) that lay in between closed forests and treeless open environments, and these habitats and their herbivore assemblages have characteristics and traits that can hardly be placed at this putative simplified binary classification. The habitats formed by the different vegetation types are all qualitatively different, such that the transition from forest versus open environments is neither gradual nor linear. The horse evolution storyline may, therefore, give the wrong impression that the evolutionary ‘path’ from forest to open grasslands is a continuous and direct trajectory. (continued)

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Box 4.2 (continued) Indeed, too much simplicity may lead to simplism, thus missing the subtility of the forces of natural selection that may lead to adaptation and evolution. Also, the characterization of browsers as selective foragers and grazers as unselective foragers is an oversimplification. There, simply, are unselective browsers (e.g., elephants: Pretorius et al. 2016) and selective grazers (e.g., the hartebeest family) (Gosling & Kingdon, 2013). Even more, the characterization of browse and grass as high- and low-quality forage is inaccurate. Browse may indeed have relatively high nitrogen levels but is typically well defended chemically (Searle & Shipley, 2008; Venter et al., 2019). In the growing season, nitrogen levels in grass approach those of browse, while being generally poorly defended by secondary compounds or by thorns and spines (even though silica bodies may cause much harm) (Prins, 1996: pp. 29 ff; Searle & Shipley, 2008; Tomlinson et al., 2016). Furthermore, grass is often available in large, fairly homogeneous volume. Lastly, most grass seeds are very nutritious (e.g., NRC, 1989). The characterization of grass as low quality forage only applies off season, and even then, some herbivores have specialized on this type of forage, turning vast quantities of cellulose content of dead grass material in a valuable resource (that is, the so-named ‘bulk and roughage grazers’ such as African buffalo). The perception of browse as high quality is an ignoration of the importance of chemical deterrents. The former may lead to the realization that the Jarman-Bell principle is fundamentally flawed (as already argued by Clauss et al., 2013; Clauss & Hummel, 2005; Prins, 1996 pp. 261 ff; see Potter & Pringle, Chap. 7). Small herbivores commonly forage on fruits and selected leaves (which is typically perceived as, in herbivore terms, a ‘high quality diet’) (Hempson et al., 2015). The low proportion of fruits and tender leaves in the diet of large herbivores is one of the reasons that led to the label of ‘poor quality diet’. The reason why large herbivores hardly have fruits, and only selected plant leaves, as important component of their diet is simply because neither fruits nor tender leaves are available in large enough quantities year-round (see also Ritchie & Olff, 1999). Never mind the relative efficiency of large herbivores (relatively less heat loss, and higher digestive efficiency), the absolute requirements are much, much larger than those of small herbivores, and cannot be met by the availability of fruit resources. In other words, being dependent on fruits and tender leaves is only a valuable foraging strategy for small animals, that because of their low absolute requirements do not need much of it (and then, even small animals must make ends meet at times of the year that fruit is not available). Hence, large ungulates hardly have fruits in their diet because of physiological but ecological limitations (Clauss et al., 2013).

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Implications for Ungulate Evolution and Ecology We have raised questions about frequently held assumptions or persistent, possibly false, paradigms. We not only proffer a better understanding of the evolution of ecology of equids and ungulates in general, but also a deeper understanding of the marginality of the tropical forests as habitat from a large ungulate perspective. The high botanical diversity of tropical forests does not imply that tropical forest leaves are of high nutritional quality, or that large forest ungulates are abundant. In fact, many perceived large tropical forest ungulates are woodland- or savanna-adapted large mammals surviving in grassy glades and gaps inside the tropical rainforest which they hardly use. Indeed, perhaps large tropical forest ungulates should be considered ‘prisoners’ that await better times when tropical rain forest would retreat again if conditions would become drier again or CO2-levels drop again (see Saltzman et al., 1999). As we argue below, there are limitations and flaws in the widely held assumptions relating to the continuum browser versus grazer, and we call for a more critical attitude towards the competitive exclusion principle as a driving force in species distribution and coexistence. Indeed, there is very limited empirical evidence for competitive exclusion in ungulates (Prins, 2016; Schieltz & Rubenstein, 2016) even though many studies show diet overlap or lack thereof. Equids do not represent the pinnacle of adaptation to open environments. As discussed above, equids still have many traits that can be considered a legacy of their ancestral adaptations to an earlier existence as species adapted to tropical lowland rainforests. With those vestiges of earlier adaptations, their present traits are not honed to cope with the spatiotemporal variation in conditions and resources that is so typical for open grassy environments (contrasting with the much more constant supply of resources and unfluctuating conditions of tropical lowland rainforests). In particular, equids are constrained in large- and small-scale distribution by having only a moderately evolved water-saving metabolism (Cheeke & Dierenfeld, 2010: p. 257). Also, in contrast to heat-adapted Bovidae, they have no particular adaptations to cool their brains and cannot let their core temperature rise to very high temperatures. Equids are not even the cursorial, open-plains animal that they are renowned for. We have frequently marveled by the terrain choice of the Burchell’s or ‘Plains’ zebra. In a mosaic landscape of flat grasslands and rugged, extremely rocky terrain, these zebras do not shy from using the whole landscape. Our GPS analyses show that when encountering Lions on the grassy plains, rather than sticking to these plains (the strategy preferred by a true plains animal, the blue wildebeest [Connochaetes taurinus]), Burchell’s zebra prefer to run up rock-piled slopes, possibly heading for rocky plateaus (unpublished M.Sc. thesis). An often overlooked, yet important, component of the diet of equids is grass seeds (see Boxes 4.2 and 4.3). By not shying away from the ingestion of stemmy material, equids can exploit seeds. According to Guthrie (1990) ‘grass seeds [...] are usually isolated high on an undigestible coarse stem of mature plants. This coarse

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stem is avoided by most ruminants because it clogs the rumen with relatively undigestible fibre. Horses [and other equids] take advantage of the seeds’ placement on the stems; they are able to pass the stem quickly through the gastrointestinal tract in relatively undigested form. At the same time, the horse can ingest, masticate, and digest the seeds which are high in nutrient quality and easily assimilated’. If one observes Burchell’s zebra in the Serengeti, one sees them snapping off the panicles instead of grazing the grass. McNaughton (1985) measured this, and the zebra energy budget can only be understood if one takes seed consumption into account (McNaughton, 1985). Yet in ruminants, the addition of grains to the diet leads to a lowered digestion of NDF and DM because of reduced cellulose digestion (Robbins, 1993: pp. 303; Van Soest, 1982: pp 108). As a matter of fact, this fundamental understanding of the difference between ruminants and non-ruminants, and the importance of starch, fat and sugars for these horse-like zebras appears to have been forgotten (e.g., Hopcraft et al., 2012). Indeed, the oft-cited publication of Bell that lays at the basis of the so-named Bell-Jarman Principle, describes Burchell’s zebra moving in advance of blue wildebeest, but in that story, only cell wall digestibility stands central (Bell, 1971) and not the cropping of the haulms of the tall grasslands with their seeds (cf. Potter & Pringle, Chap. 7). Box 4.3. The Importance of Digestibility and Predation There is much more to ungulate evolution and ecology than avoidance of predators and breakage of plant cell walls. First, digestion is more than digestibility only. As Guthrie (1990) observed: ‘Herbivores do not generally select plants on the basic gradient of nutrient quality, but rather, the primary emphasis in selection is to avoid secondary plant constituents’. Perhaps even more important than its digestive function, the rumen functions as a detoxifier. Arguably, the evolution of Artiodactyla is driven more by the detoxification function of the rumen (Lapierre & Lobley, 2001) than by digestive capacity. Another potential key trait of the rumen (other than enhancing digestibility) is the high nitrogen efficiency of ruminants due to their urea recycling mechanism (Lapierre & Lobley, 2001; Reynolds & Kristensen, 2008; Tan & Murphy, 2004). Second, there is more than digestion and predation. Thermoregulation, disease tolerance and life history may be important determinants of abundance and distribution of herbivores. In this chapter, we show that the occurrence of species is complex and potentially determined by many factors. The storylines presented by us, whether plausible or functioning as red herrings, bring to the fore that there are many physical and biotic pressures (i.e., natural selection forces) acting on organisms. We are of the opinion that, in comparison to diet (in)digestibility, many of these other selective pressures receive too little attention: e.g., thermal conditions (‘climatic stressors’), resource stress (continued)

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Box 4.3 (continued) independent of the presence of a competitor, and the effects of parasites and other disease agents. Moreover, we argue that the first explanations to consider for limitations in species distribution are those that directly relate the environment to the animal, without considering the effects of a second species. Oftentimes, the competitive exclusion principle (which integrates a second species) is postulated by both ecologists and palaeontologists alike. However, there is very limited empirical evidence for competitive exclusion in ungulates (Prins, 2016; Schieltz & Rubenstein, 2016). In addition, there are many other, arguably simpler, explanations. The introduction of a new species to a new but already occupied area may indeed affect resident species negatively, yet not necessarily through a higher resource use efficiency. For example, a newcomer may introduce new diseases and parasites, which residents cannot cope with. Also, resource competition with newcomers may not necessarily act through depletion, but through instigating novel adaptive responses of the prey item. Artiodactyls possibly instigated the development of thorns and spines in shrubs and trees (Charles-Dominique et al., 2016). These thorns and spines severely reduce bite size—which is a major compromise for hindgut fermenters, which need high intake. If this inference matches history (which is largely unknown), then Artiodactyls may have indeed caused the demise of Perissodactyls, yet not through depletion of resources, but through triggering modification of resources! Although still not featuring prominent in herbivore ecology, parasites are an important determinant of abundance, and perhaps also, distribution of open environment ungulates (Ostfeld et al., 2008). Around 1900, rinderpest wiped out millions of African game (Cleaveland et al., 2008; Prins, 1996). The Serengeti Burchell’s zebra and blue wildebeest migration only could take immense populations when rinderpest was erased through a vaccination programme of livestock (Sinclair, 1979). Recently, large proportions of the Saiga antelope (Saiga tatarica) population were found dead (Fereidouni et al., 2019). The formation of large, dense aggregations is probably the most important determinant for the heavy impact of diseases on open plains herbivores. However, another factor may be higher disease susceptibility. As illustrated by the moose, herbivores of seasonal environment may invest in (re)production as the expense of lower investment in the immune system. Whereas obvious and conspicuous, life histories of ungulates are generally overlooked by ecologists. As put forward by Kiltie (1984) and Geist (1987), it is probable that life history is a major determinant for the distribution and success of extant large herbivores. For example, the Cervidae appear to have a strategy of fast development (fast growth of embryos and juveniles, early sexual maturity, short lifespan), which may well explain their Holocene (continued)

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Box 4.3 (continued) success at higher latitudes, whereas many other herbivores succumbed (Geist, 1987). Yet, while being a potentially strong explanatory variable, few herbivore ecologists and palaeontologists consider life history.

Closing Remarks As can be inferred from the term ‘storyline’, we recognize that much of the above rests on weak evidence. However, we do believe that all these storylines are worthy of consideration and further investigation because they are relatively understudied. Instead, time and again ecological studies on ungulates focus on potential body size effects, in relation to the Jarman-Bell Principle and the Competitive Exclusion Principle. Although decades of research have raised little to no evidence (Prins, 2016; Schieltz & Rubenstein, 2016), ungulate ecologists resume their narrow focus on exploitation competition. We think that it is about time that species coexistence should not be taken as proof for niche differentiation, but instead—more factually and simply—as a consequence of the fact that free-ranging ungulates are not protozoa in a petri dish. Also, even if the storylines presented by us were false, we believe that raising the question ‘Why are there no modern equids living in tropical lowland rainforest?’ has merit by itself. How species traits limit species ranges is a basic question that an inquisitive child could raise—and yet, we ecologists are unable to answer the question satisfactorily. Palaeontologists have the capacity to infer much about ecology based on the limited information that can be derived from a few teeth, jaws, and bones. Based on hard tissues, one can hardly deduce metabolic, thermoregulatory and immune responses. For ecologists, however, there is no excuse for a narrow focus that excludes important components of an organism and its ecology. The tendency to reduce perspectives to body size, foregut vs. hindgut fermenting, and predator avoidance strategy is too simplistic and unnecessarily limiting. Perhaps none of the storylines we outline above on why tropical forests equids do not exist are valid; however, we believe that by integrating a wide variety of organismal traits and environmental characteristics we increase our chance of ‘finding the truth’—that is, to grasp the perplexing patterns of animal abundance and distribution. There is more to equids, and vertebrates in general, than their teeth—and much more to ecology than the Jarman-Bell Principle and the Competitive Exclusion Principle.

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Turner, N. J., Łuczaj, Ł. J., Migliorini, P., Pieroni, A., Dreon, A. L., Sacchetti, L. E., & Paoletti, M. G. (2011). Edible and tended wild plants, traditional ecological knowledge and agroecology. Critical Reviews in Plant Sciences, 30, 198–225. Valenzuela-Sánchez, A., Wilber, M. Q., Canessa, S., Bacigalupe, L. D., Muths, E., Schmidt, B. R., Cunningham, A. A., Ozgul, A., Johnson, P. T. J., & Cayuela, H. (2021). Why disease ecology needs life-history theory: a host perspective. Ecology Letters, 24, 876–890. Van der Zon, A. P. (1992). Graminées du Cameroun. Ph.D. thesis, University of Wageningen. Vanleeuwe, H., & Gautier-Hion, A. (1998). Forest elephant paths and movements at the Odzala National Park, Congo: the role of clearings and Marantaceae forests. African Journal of Ecology, 36, 174–182. Van Soest, P. J. (1982). Nutritional Ecology of the Ruminant: ruminant metabolism, nutritional strategies, the cellulolytic fermentation and the chemistry of forages and plant fibers. O & B Books. Veldhuis, M. P., Hofmeester, T. R., Balme, G., Druce, D. J., Pitman, R. T., & Cromsigt, J. P. G. M. (2020). Predation risk constrains herbivores’ adaptive capacity to warming. Nature Ecology & Evolution, 4(8), 1069–1074. Venter, J. A., Vermeulen, M. M., & Brooke, C. F. (2019). Feeding ecology of large browsing and grazing herbivores. In I. J. Gordon & H. H. T. Prins (Eds.), The ecology of browsing and grazing II. Ecological studies (Vol. 239, pp. 127–153). Springer. Vereshchagin, N. K. (1974). The mammoth “cemeteries” of north-east Siberia. Polar Record, 17, 3–12. Vilà-Cabrera, A., Premoli, A. C., & Jump, A. S. (2019). Refining predictions of population decline at species’ rear edges. Global Change Biology, 25, 1549–1560. Virot, E., Ma, G., Clanet, C., & Jung, S. (2017). Physics of chewing in terrestrial mammals. Scientific Reports, 7, 43967. Wallace, D. R. (2004). Beasts of Eden: walking whales, dawn horses, and other enigmas of mammal evolution. University of California Press. Walton, D. N. (1988). Burden of proof. Argumentation, 2, 233–254. Walton, D. N. (2001). Abductive, presumptive and plausible arguments. Informal Logic, 21, 141–169. Wand, S. J., Midgley, G. F., Jones, M. H., & Curtis, P. S. (1999). Responses of wild C4 and C3 grass (Poaceae) species to elevated atmospheric CO2 concentration: a meta-analytic test of current theories and perceptions. Global Change Biology, 5, 723–741. Ward, D., Schmitt, M. H., & Shrader, A. M. (2020). Are there phylogenetic differences in salivary tannin-binding proteins between browsers and grazers, and ruminants and hindgut fermenters? Ecology and Evolution, 10, 10426–10439. Weckel, M., Giuliano, W., & Silver, S. (2006). Jaguar (Panthera onca) feeding ecology: distribution of predator and prey through time and space. Journal of Zoology, 270(1), 25–30. Weigelt, J. (1989). Modes of death. In J. Weigelt (Ed.), Recent vertebrate carcasses and their paleobiological implications (pp. 27–78). University of Chicago Press. Wenxuan, X. U., Weikang, Y. A. N. G., & Jianfang, Q. I. A. O. (2009). Food habits of Kulan (Equus hemionus hemionus) in Kalamaili mountain nature reserve, Xinjiang, China. Acta Theriologica Sinica, 29, 427–431. Withers, P. C., Cooper, C. E., Maloney, S. K., Bozinovic, F., & Cruz-Neto, A. P. (2016). Ecological and environmental physiology of mammals. Oxford University Press. Zhang, H., Yan, X., Zhao, Z., & Ji, L. (2013). Analysis of the polysaccharides from Urtica angustifolia and their anti-fatigue activity. African Journal of Pharmacy and Pharmacology, 7, 1438–1447.

Chapter 5

Evolution of Equid Body Size Carmen Nacarino-Meneses

Abstract Body size plays a central role in the biology, physiology, and ecology of organisms. It further represents a main characteristic of the evolutionary history of horses, as these animals experienced multiple changes in body size since their first appearance in the Eocene. The traditional view considering equids as a paradigm of body size increase over time (i.e., Cope’s rule) is now demonstrated to be out of date, as both dwarfing and gigantism processes have been shown in multiple lineages. The only extant genus of horses, the genus Equus, itself experienced significant variations in body size during the Pleistocene. Generally, extinct true horses and zebralike equids decreased in size during their evolution in Eurasia and Africa while they increased in body size in North America. Equid body size trends have been related to changes in climate, habitat and resources and, more recently, to variations in key life history traits. Extant wild Equus have a mass of between 200 and 400 kg and do not generally show much sexual dimorphism in body mass. Domesticated equids also present a wide range of sizes that, in the case of horse breeds, result from mutations in only a few genes.

Introduction Body size is one of the most important features of an animal (Peters, 1983). It correlates with a variety of physiological characteristics (McNab, 1990), including metabolic rate (Schmidt-Nielsen, 1984). Body size also co-varies with ecological variables such as life history traits, population density, home range size, community structure, or behaviour (Peters, 1983). Body size can be used as a predictor of the extinction risk of a species (i.e., its vulnerability to extinction) (Chichorro et al., 2019), and constitutes a great source of biological information for already extinct

C. Nacarino-Meneses (✉) Department of Biological Sciences, University of Cape Town, Cape Town, South Africa Evolutionary Paleobiology Research Group, Institut Català de Paleontologia Miquel Crusafont, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 H. H. T. Prins, I. J. Gordon (eds.), The Equids, Fascinating Life Sciences, https://doi.org/10.1007/978-3-031-27144-1_5

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animals (Damuth & MacFadden, 1990). Consequently, the study of body size, and its variation among organisms and species, is the focus of research for many evolutionary biologists, ecologists, and palaeontologists. Body size changes are a key feature of equid evolution (MacFadden, 1992). Furthermore, extant domestic horses present one of the widest ranges of sizes known for a single species (Brooks et al., 2010). Hence, the study of body size in these iconic mammals has drawn the attention of many researchers over many decades (Alberdi et al., 1995, 1998; Cantalapiedra et al., 2017; Forsten, 1991a, 1991b, 1993; MacFadden, 1986; Nacarino-Meneses & Orlandi-Oliveras, 2021; Orlandi-Oliveras et al., 2018; Saarinen et al., 2021). In this chapter, I will review the most important changes in body size that horses experienced along their evolutionary history, placing a special emphasis on the only extant genus of horses, i.e., the genus Equus. I will also examine which were the selection pressures that likely drove equid body size variation. I will further analyze the body size differences in extant wild horses, zebras, and asses with a special focus on the lack of sexual dimorphism in terms of body mass in most species of living equids. Finally, I will assess the genetic foundations for body size variation in domesticated horses and donkeys, highlighting some biological and developmental differences between different-sized breeds. Box 5.1. Estimation of Equid Body Mass from Fossil Bones and Teeth Body size of living horses is usually represented by their body mass (weight) and/or their height at the withers. These parameters, however, cannot be directly measured in extinct species. Hence, palaeontologists often use linear dimensions such as limb bones lengths and widths, teeth occlusal diameters or skull basilar lengths as proxies of body size (e.g., Alberdi et al., 1995). Nevertheless, body mass can be estimated from fossil remains using allometric models (Damuth & MacFadden, 1990). These are represented by the power function: y = axb (Damuth & MacFadden, 1990), which can be log-transformed to obtain a linear relationship: lny = lna + blnx (Peters, 1983). In both equations, y is the dependent variable (i.e., body mass), x is the independent variable (i.e., measurement taken on the fossil remain), a is a constant and b is the allometric coefficient measured within or across species (Alberdi et al., 1995). Generally, limb bones provide more accurate body mass estimations as compared to teeth (Damuth & MacFadden, 1990; Saarinen et al., 2021). Therefore, body mass equations for extinct horses usually involve the measure of different anatomical regions of metapodia (Alberdi et al., 1995; Saarinen et al., 2021). See, as an example, the equations developed by Alberdi et al. (1995) for extinct Equus. Teeth, however, are more abundant and taxonomically diagnostic than other skeletal elements (MacFadden, 1986). Therefore, several researchers have used teeth instead of bones to estimate the body mass of fossil horses (MacFadden, 1986; Shoemaker & Clauset, 2014).

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Evolution of Body Size Within the family Equidae: A Highly Complex and Non-linear Journey The first members of the family Equidae, the hyracotherines (Eocene, 55 Ma), were small-sized animals that only had a mass of around 10–20 kg (MacFadden, 1986; Secord et al., 2012; Shoemaker & Clauset, 2014) (Fig. 5.1). Subsequent Eocene and Oligocene horses’ relatives, such as Mesohippus (40–30 Ma) and Miohippus (35–20 Ma), were slightly larger, but still the size of a small to medium-sized mammal, between 10 and 60 kg (MacFadden, 1986; Shoemaker & Clauset, 2014) (Fig. 5.1). Conversely, in the Miocene epoch there was a great diversification in equid body size (MacFadden, 1986) (Fig. 5.1). During that time, some taxa achieved a body mass of 500–600 kg (e.g., Hypohippus cf. MacFadden, 1986; Shoemaker & Clauset, 2014), while others only had a mass of 40 kg (e.g., Cremohipparion periafricanum cf. Cantalapiedra et al., 2017) (Fig. 5.1). All possible body sizes in between these weights were found among Miocene horses (Cantalapiedra et al., 2017; Shoemaker & Clauset, 2014) (Fig. 5.1). The Pliocene, and especially the Pleistocene epochs, were dominated by the genus Equus (MacFadden, 1992). Some extinct members of this group, such as the Villafranquian (3.5–1 Ma) Equus major (700 kg cf. Saarinen et al., 2021) from Europe, were among the largest of all known horses (Fig. 5.1). If one analyzes the body size changes observed in equids from the most ancient tiny horses (e.g., Sifrhippus sandrae, Eocene, 5 kg cf. Secord et al., 2012) to the most recent huge ones (e.g., Equus major, Pleistocene, 700 kg cf. Saarinen et al., 2021), a general pattern towards an increase in body size can be identified (Fig. 5.1). For this reason, the family Equidae has traditionally been considered a poster child of Cope’s rule (Stanley, 1973)—i.e., the tendency to increase body size along evolutionary lineages through time (Purvis & Orme, 2005)—found in multiple textbooks and museum exhibitions. This gradualist view, however, is completely erroneous, as it represents an oversimplification of the body size changes that horses experienced during their evolutionary history (Gould & MacFadden, 2004; MacFadden, 1986). Over recent decades, numerous investigations have revealed that body size evolution in equids did not follow a single trend, but that both dwarfing and gigantism occurred in several lineages and at several times (Gould & MacFadden, 2004; MacFadden, 1986) (Fig. 5.1). Miocene anchiterines, South American hippidiforms and North American Equus, for instance, likely experienced phylogenetic increases in body size (Alberdi et al., 1995; Gould & MacFadden, 2004; MacFadden, 1986) (Fig. 5.1). Conversely, size decrease has been reported in at least four clades: the North American genera Calippus, Nannippus and Pseudohipparion, and the so-called “Old World hipparionines” (Gould & MacFadden, 2004; Ortiz-Jaureguizar & Alberdi, 2003) (Fig. 5.1). Therefore, the traditional view of the family Equidae as a model to explain deep-time linear trends in body size should be abandoned, and the complexity of body size evolution within the group has to be acknowledged. This idea was already anticipated by Simpson in his Major Features in Evolution (Simpson, 1953), and Cope’s rule has now been proved to be wrong for the horse

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Fig. 5.1 Evolution of body size in the family Equidae. Simplified red cladogram based on MacFadden (1992). Equid silhouettes were obtained from phylopic.org, where they were published under the Public Domain licence. Data on body mass obtained from Alberdi et al. (1995), Nowak (1999), Eisenmann (2000), Ernest (2003), Shoemaker and Clauset (2014), Cantalapiedra et al. (2017), Zedda et al. (2020), Nacarino-Meneses and Orlandi-Oliveras (2021) and Saarinen et al. (2021). Body mass of Equus sivalensis was estimated using the data published in Bernor et al. (2019) and the equations provided by Alberdi et al. (1995)

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family by several authors (Shoemaker & Clauset, 2014; Cantalapiedra et al., 2017, see also Chap. 2 in this volume).

Body Size Variation in Extinct Equus: Pleistocene Trends Around the World All extant species and subspecies of zebras, asses and horses (wild and domesticated) belong to a single genus: Equus (Groves, 2002). This group originated 4–4.5 Ma in North America and derived from the Miocene monodactyl equid Dinohippus (Cirilli et al., 2021; MacFadden & Carranza-Castañeda, 2002; Orlando et al., 2013). Nowadays, Equus is only represented by a few wild species, patchily distributed along Africa and Eurasia (Moehlman, 2002). Equus horses, however, were much more diverse during the Pleistocene, when they lived in all continents except for Oceania and Antarctica (MacFadden, 1992). Interestingly, this genus experienced a large variation in body size during that period, although these changes did not follow the same pattern all around the world (Alberdi et al., 1995) (Fig. 5.2). Moreover, taxonomy and phylogeny of most extinct Equus species is still under discussion (e.g., Barrón-Ortiz et al., 2019; Cirilli et al., 2021), so it is not possible to know yet if the body size variation observed in Pleistocene equids represents a phyletic trend or just a chronological cline. These unresolved questions further hamper us knowing whether these trends/clines occurred in the context of phyletic evolution (i.e., gradual evolution along a single or a few branches) or through cladogenesis (i.e, the size trends could result from smaller or larger species going extinct and being substituted by emerging ones), and only future studies will shed some light on this issue.

North America From Mexico to Canada, the numerous fossil equid remains found in multiple palaeontological sites indicate that horses were common elements of the North American fauna during the Pliocene and the Pleistocene (MacFadden, 1992). However, phylogenetic and taxonomic relationships within this group are still not well understood, and, therefore, the analysis of body size trends remains problematic. Traditionally, all Pliocene and Pleistocene monodactyl equids from North America were grouped under the genus Equus (MacFadden, 1992). This classification, however, has recently been challenged by molecular and morphological studies; for example, recent ancient DNA investigations revealed that the Pleistocene stiltlegged horse, traditionally known as Equus francisci, should instead be included in a new genus (i.e., Haringtonhippus), and consequently named Haringtonhippus francisci (Heintzman et al., 2017). Yet, morphology-based phylogeny still grouped

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Fig. 5.2 Body size variation in extant and extinct Equus. On each graph, abscissa axis (x) indicates body mass (kg) and ordinate axis ( y) represents time (Ma). Data on body mass obtained from Alberdi et al. (1995), Nowak (1999), Eisenmann (2000), Ernest (2003), Shoemaker and Clauset (2014), Cantalapiedra et al. (2017), Zedda et al. (2020), Nacarino-Meneses and Orlandi-Oliveras (2021) and Saarinen et al. (2021). Body mass of Equus sivalensis was estimated using the data published in Bernor et al. (2019) and the equations provided by Alberdi et al. (1995). Black colour depicts extinct taxa, while grey colour indicates extant species. Triangles denote plesippine and stenonid horses, while circles represent caballoid equids. Filled triangles indicate zebra-like stenonids and unfilled symbols depict ass-like stenonids. Continent silhouettes were obtained from thenounproject.org, where they were published under Public Domain licence. Red arrows represent the size trends described in the text. (a) North America. (b) South America. (c) Asia. (d) Europe. (e) Africa

this taxon under the genus Equus (Barrón-Ortiz et al., 2019). The most recent phylogeny of North American monodactyl equids further proposes that earlier plesippine taxa should be considered a new genus (i.e., Plesippus), although this idea is not supported by the divergence time criterion (Barrón-Ortiz et al., 2019). New phylogenetic studies involving Eurasian and African species do not recognize

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Plesippus at the generic level either (Cirilli et al., 2021). Here, until further studies clarify their phylogenetic relationships, I will consider North American plesippines as part of the genus Equus and H. francisci as belonging to a distinct genus. Box 5.2. Plesippine, Stenonoid, Caballoid and Stilt-Legged Horses: Grouping Equus Based on Morphological Characters . Plesippine: usually applied to North American fossil species, this term indicates a primitive zebra-like anatomy. Plesippine Equus are characterized by showing V-shaped linguaflexids (i.e., enamel fold between the metaconid and the metastylid that faces the inner side of the mouth) and molar ectoflexids (i.e., enamel fold between the protoconid and the hypoconid that faces the outer side of the mouth) that penetrate the isthmus of their lower molars (Scott, 2006). . Stenonid (also stenonine, stenonian, stenonoid, non-caballine): named after Equus stenonis, this term also indicates a primitive morphology. It is usually employed to group the most primitive extinct Equus of Eurasia and Africa (Alberdi et al., 1998; Forsten, 1988) and all extant species of zebras and asses (Forsten, 1988). As in plesippines, lower molars of stenonoids also present a V-shaped linguaflexid (Forsten, 1988). The ectoflexid of the lower molar is deep in zebras but shallow in asses. . Caballoid (also caballine): named after Equus caballus, this term indicates derived anatomical features. Specifically, caballoid teeth present a U-shaped linguaflexid and short ectoflexids (Forsten, 1988; Scott, 2006). Caballoid equids comprise all feral and domestic living horses, as well as some Middle/Late Pleistocene and Holocene extinct Equus. . Stilt-legged horses: subdivision of North American Pleistocene horses that includes hemione-like caballoids with elongated and gracile metapodia (Heintzman et al., 2017). Conversely, caballoid horses with short and robust metapodia are classified as stout-legged horses (Heintzman et al., 2017).

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North American Equus are usually clustered in two distinct groups: plesippine and caballine horses. The plesippine Equus simplicidens, also known as the Hagerman horse or the American zebra (Scott, 2006), likely represents the earliest common ancestor of Equus (Rook et al., 2019), and had a mass of around 375 kg (Alberdi et al., 1995) (Fig. 5.2a). The more derived plesippine Equus idahoensis (Scott, 2005) was larger, as it exceeded 500 kg in mass (Shoemaker & Clauset, 2014) (Fig. 5.2a). Caballine horses appeared in North America during the Early Pleistocene (Irvingtonian I NALMA, 1.9–1.7 Ma, Rook et al., 2019). By that time, the largesized Equus scotti (500 kg cf. Cantalapiedra et al., 2017; Fig. 5.2a), and the smallsized Equus conversidens (300 kg cf. Alberdi et al., 1995; Fig. 5.2a) and Equus alaskae (370 kg cf. Cantalapiedra et al., 2017; Fig. 5.2a), were common taxa. These species also persisted during the Middle and Late Pleistocene (Irvingtonian II, III and Rancholabrean, 850–11 Kyr, Rook et al., 2019), when they shared the continent with two other caballine equids: the large Equus occidentalis (570 kg cf. Alberdi et al., 1995; Fig. 5.2a), and the smaller Equus mexicanus (400 kg cf. Cantalapiedra et al., 2017, Fig. 5.2a). According to Alberdi et al. (1995), the evolution of North American equids was generally accompanied by a slight increase over time in body size, which can be distinguished in both plesippine and caballine horses (Fig. 5.2a). Interestingly, trends of decreasing size have also been described in horses on this continent. This is the case of the last caballine equids that inhabited Alaska during the end of the Late Pleistocene (12.5 Kyr), which experienced a size decline (metacarpal’s length varied from about 230 to 190 mm), just before their extinction at the beginning of the Holocene (Guthrie, 2003).

South America Equus arrived in South America through the Isthmus of Panama during the third pulse of the Great American Biotic Interchange (GABI 3, 1.0–0.8 Ma) (MacFadden, 2013). These equids rapidly dispersed in the continent, achieving a widespread distribution (Machado & Avilla, 2019), and ultimately becoming extinct at the end of the Late Pleistocene (Prado & Alberdi, 2017). South American Equus lived in woodlands and grasslands (Prado & Alberdi, 2017), highlands (up to 3000 m) and lowlands (less than 50 m), in all areas except the Amazon region, north of latitude 40°S (Machado & Avilla, 2019). The exact drivers of their extinction are still unknown, although some studies suggest a synergistic effect between environmental change and human activity (Barnosky & Lindsey, 2010; Villavicencio et al., 2019). Until recently, scientists recognized three different species of South American Equus, i.e., Equus andium, Equus insulatus and Equus neogeus (Prado & Alberdi, 2017). E. insulatus is considered a large-sized horse (350 kg cf. Prado & Alberdi, 2017; Fig. 5.2b) that lived in the Andean region during the Middle and Late Pleistocene (Prado & Alberdi, 2017). According to Prado and Alberdi (2017), E. insulatus gave rise to the two species that also inhabited South America during

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the Late Pleistocene: the small E. andium (220 kg cf. Prado & Alberdi, 2017, Fig. 5.2b) of the Andean region, and the larger E. neogeus (380 kg cf. Prado & Alberdi, 2017, Fig. 5.2b) of the South American Plains. Hence, no specific trend in body size can be recognized during the evolution of Equus in South America (Fig. 5.2b). Interestingly, recent publications have questioned the taxonomic validity of South American Equus species, as these were only described by considering differences in size and proportions between them (Machado & Avilla, 2019; Machado et al., 2018). Several researchers believe that these characters alone are not diagnostic enough, and propose that all South American Equus belong to the single species E. neogeus (Machado & Avilla, 2019; Machado et al., 2018). For these authors, E. insulatus and E. andium just represent different morphotypes within a smooth size cline, which was probably driven by the topography of the continent (Machado & Avilla, 2019; Machado et al., 2018).

Asia Equus migrated from North America to Eurasia through the Bering Strait 2.5 Ma (Lindsay et al., 1980). By that time, at least six species of large stenonoid horses that likely derived from the North American Equus simplicidens dwelled in the steppes of China (Sun & Deng, 2019): Equus stenonis (420 kg cf. Cantalapiedra et al., 2017; Fig. 5.2c), Equus sanmeniensis (430 kg cf. Cantalapiedra et al., 2017; Fig. 5.2c), Equus huanghoenensis (340 kg cf. Cantalapiedra et al., 2017; Fig. 5.2c), Equus qingyangensis (360 kg cf. Cantalapiedra et al., 2017; Fig. 5.2c), Equus yunnanensis (300 kg, Cantalapiedra et al., 2017; Fig. 5.2c), and Equus eisenmannae (unknown body mass, basal skull length over 590 mm cf. Wang & Deng, 2011). Other primitive taxa such as the large Equus wangi (425 kg cf. Cantalapiedra et al., 2017; Fig. 5.2c), and the small Equus teilhardi (280 kg cf. Cantalapiedra et al., 2017; Fig. 5.2c), also lived during the Early Pleistocene of China (Sun & Deng, 2019). The high diversity of Chinese stenonoids was substantially reduced during the following middle and late Pleistocene, as only E. sanmeniensis and E. yunnanensis respectively survived these epochs (Deng & Xue, 1999). The diversity decline of stenonoids was probably related to the arrival of caballoid horses at the end of the Middle Pleistocene (0.2 Ma), when the large Equus beijingensis (600 kg cf. Cantalapiedra et al., 2017; Fig. 5.2c) appeared in China (Deng & Xue, 1999). During the late Pleistocene, two other Chinese caballoids were common: the large Equus dalianensis (550 kg cf. Cantalapiedra et al., 2017; Fig. 5.2c) and the smaller Equus ferus przewalskii (200–300 kg cf. Nowak, 1999; Fig. 5.2c). Only the latter has survived to the present, when it shares the continent with the smaller asses E. hemionus (230 kg cf. Ernest, 2003; Fig. 5.2c) and E. kiang (275 kg cf. Ernest, 2003; Fig. 5.2c) (see later sections for further information on the body size of extant Equus).

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The distribution of stenonoid and caballoid horses during the Pleistocene of Asia was not restricted to China. In the Indian subcontinent, the large stenonoid Equus sivalensis (400 kg, own estimation based on data from Bernor et al., 2019; Fig. 5.2d) from the Siwalik hills (India) was a common taxon in the Early Pleistocene (2.6–0.6 Ma) (Bernor et al., 2019). By that time, a small stenonoid equid (Bernor et al., 2019), sometimes referred as Equus sivalensis minor (Gaur & Chopra, 1984) (unknown mass, antero-posterior diameter of the distal end of the third metacarpal over 25 mm cf. Gaur & Chopra, 1984), also inhabited the north of India and Pakistan (Bernor et al., 2019). Caballine horses in the Indian peninsula, on the other hand, are represented by the large Equus namadicus (600 kg cf. Zedda et al., 2020; Fig. 5.2d), which has been found in Middle and Late Pleistocene sites (Chauhan, 2008). Generally, both stenonoid and caballoid Equus in Asia experienced a decrease in body size from the early Pleistocene to the late Pleistocene and current times (Fig. 5.2d).

Europe Equus first appeared in Europe during the Early Pleistocene, ca. 2.6 Ma (Bernor et al., 2018). Earliest stenonine horses in this continent are represented by Equus livenzovensis, a large (560 kg cf. Alberdi et al., 1995; Fig. 5.2d) monodactyl equid closely related to E. simplicidens from North America and E. eisenmannae from China (Bernor et al., 2018). E. livenzovensis was quickly replaced by the slightly smaller Equus stenonis (420 kg cf. Cantalapiedra et al., 2017; Fig. 5.2d), which was the most common horse throughout the early Pleistocene of Europe (Boulbes & van Asperen, 2019). During that epoch, stenonoid European horses were rather diverse in body size (Boulbes & van Asperen, 2019), as both small- (e.g., Equus stehlini, 320 kg cf. Alberdi et al., 1995; Fig. 5.2d) and large-sized species (e.g., Equus major, 700 kg cf. Saarinen et al., 2016; Fig. 5.2d) have been found across the continent. By the end of the early Pleistocene, two other stenonoids appeared in Europe: the small Equus altidens (300 kg cf. Cantalapiedra et al., 2017; Fig. 5.2d), and the large Equus suessenbornensis (570 kg cf. Saarinen et al., 2021; Fig. 5.2d). These sympatric taxa survived until the beginning of the middle Pleistocene (0.8 Ma) (Boulbes & van Asperen, 2019). The last stenonoid found in Europe is the small-sized European wild ass (Equus hydruntinus), which had a mass of around 215 kg (Cantalapiedra et al., 2017) (Fig. 5.2d) and lived during the Late Pleistocene and the Holocene. Most European stenonoids were replaced by caballine equids during the Middle Pleistocene (Forsten, 1988). The first true horse described in Europe was the largesized Equus mosbachensis (610 kg cf. Nacarino-Meneses & Orlandi-Oliveras, 2021; Fig. 5.2d), which probably survived until the end of the Middle Pleistocene (0.1 Ma) (Boulbes & van Asperen, 2019). Other Middle Pleistocene caballoids include the slightly smaller Equus taubachensis (580 kg cf. Cantalapiedra et al., 2017; Fig. 5.2d) and Equus steinhemensis (470 kg cf. Nacarino-Meneses & Orlandi-Oliveras, 2021; Fig. 5.2d). Recent investigations, however, suggest that these equids should be

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considered subspecies of Equus ferus instead of separate taxa (Boulbes & van Asperen, 2019). E. ferus was the most common caballine horse found in the Late Pleistocene deposits of Europe (Boulbes & van Asperen, 2019). During that time, different subspecies, such as Equus ferus germanicus (470 kg cf. Alberdi et al., 1995; Fig. 5.2d) and Equus ferus arcelini (470 kg cf. Alberdi et al., 1995; Fig. 5.2d), were common in the European continent. As in Asia, both stenonoid and caballoid horses show a tendency towards a decrease in body size during their evolution in Europe (Alberdi et al., 1995, 1998; Forsten, 1991a). As shown in Fig. 5.2c, earlier species from both equid lineages are larger than later ones.

Africa Equus first appearance in Africa is dated 2.3 Ma, when the zebra-like equid Equus oldowayensis (Bernor et al., 2019) is first recorded in the Omo Valley (Ethiopia) (Bernor et al., 2010). With an estimated body mass of 330 kg (Cantalapiedra et al., 2017; Fig. 5.2e), this species was the most widespread Equus in the east of Africa during the Early Pleistocene (Bernor et al., 2010). During that epoch, it shared north eastern Africa with the slightly larger Equus koobiforensis (425 kg cf. Cantalapiedra et al., 2017; Fig. 5.2e) (Bernor et al., 2010). Equus numidicus (475 kg cf. Cantalapiedra et al., 2017; Fig. 5.2e) and Equus capensis (400 kg cf. Eisenmann, 2000; Fig. 5.2e) were large prehistoric zebras that also inhabited Africa in the Early Pleistocene (Bernor et al., 2010). Their distribution, however, was restricted to the northern and southern parts of this continent, respectively (Bernor et al., 2010). Only Equus capensis persisted throughout the Pleistocene, as it became extinct at the beginning of the Holocene (11 Kyr) (Bernor et al., 2010). Living zebras (Equus zebra, Equus quagga and Equus grevyi) (Groves, 2002; Nowak, 1999), which appeared during the Middle and Late Pleistocene (Bernor et al., 2010), are smaller than any of these extinct species (250–380 kg cf. Ernest, 2003) (see later sections for further information on the body size of extant Equus). The Early Pleistocene species Equus tabeti likely was the earliest African ass (Bernor et al., 2010; Groves, 2002; Nowak, 1999). It lived in the north (e.g., Algeria) and east (e.g., Kenya) of Africa (Bernor et al., 2010; Sam, 2020) and had a mass of around 270 kg (cf. Cantalapiedra et al., 2017; Fig. 5.2e). Late Pleistocene asses in the continent are grouped under the species Equus melkiensis (Bernor et al., 2010), which was very similar in size to earlier taxa (i.e., E. tabeti). This small equid had a mass of 275 kg (cf. Cantalapiedra et al., 2017; Fig. 5.2e) and was endemic to the Maghreb region (Sam, 2020). The extant African wild ass Equus africanus (250 kg cf. Ernest, 2003; Fig. 5.2e), which first appeared in the fossil record at the end of the early Pleistocene, or the beginning of the middle Pleistocene (Bernor et al., 2010), is slightly smaller than both E. tabeti and E. melkiensis. E. africanus currently occurs in some areas of Eritrea and Ethiopia so, for now, there are no records of asses in West, Central or Southern Africa.

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Generally, both zebras and asses experience a slight decrease in body size during their evolution in Africa (Alberdi et al., 1995), from larger early Pleistocene forms to smaller extant taxa (Fig. 5.2e). This size variation, however, was much less marked as compared to the mass changes observed in other continents, such as Europe.

What Drove Body Size Changes in Extinct Equids? Different Frameworks to Study a Singular Phenomenon Body size variation in vertebrates has traditionally been explained as occurring as the consequence of selective pressures (e.g., resource variation) acting directly on this key biological trait (e.g., Alberdi et al., 1995). However, some researchers have proposed that selective forces may instead act on key life history traits to which adult body size is sensitive (e.g., growth rate, age at maturity), and, therefore, that variations in body size are just a by-product of natural selection on another trait (Palkovacs, 2003). Changes in body size, during the evolutionary history of Equidae, have been studied and analyzed under both kinds of analytical frameworks.

Variation in Climate, Habitat, and Resources: Traditional Explanations for Body Size Changes in Extinct Equids Climatic variation and associated changes in the quality and availability of resources are the most widespread explanations for the body size differences observed in extinct equids (Alberdi et al., 1995, 1998; Boulbes & van Asperen, 2019; Cantalapiedra et al., 2017; Forsten, 1991a, 1991b, 1993; Ortiz-Jaureguizar & Alberdi, 2003; Saarinen et al., 2021). In some clades of horses, for instance, body size changes seem to conform to Bergmann’s (Alberdi et al., 1995; Secord et al., 2012) and/or Allen’s rule (Van Asperen, 2010). The former of these ecogeographical principles aims to explain the tendency for endothermic animals to be larger at high, cold latitudes than they are nearer the warm equator (Purvis & Orme, 2005). It is based on the notion that larger animals have a thermoregulatory advantage in preventing heat loss in colder climates due to their lower surface-to-volume ratio (Blackburn et al., 1999). The size trends experienced by Equus in specific parts of the world during the Pleistocene might be interpreted in the light of this rule, as the presence of small- and large-sized taxa generally correlates with warm and cold climates, respectively (Alberdi et al., 1995). When analyzed at a finer scale, however, Bergmann’s rule does not seem to apply, as it happens in many other taxa (Blackburn et al., 1999). Glacial Middle Pleistocene caballine horses from Europe, for example, are generally smaller than inter-glacial ones (Van Asperen, 2010) although opposite results would be expected from Bergmann’s rule. Nevertheless, equids living in the glacial periods show more robust limb bones than do

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inter-glacial horses (Van Asperen, 2010), which agrees with Allen’s rule. This principle predicts that animals would have shorter limbs in colder than in warmer climates to reduce the ratio of surface area to body mass (Tilkens et al., 2007). This decrease in the surface-to-volume ratio, again, might entail a thermoregulatory advantage (Tilkens et al., 2007). Body size variations in Equidae have also been related to habitat changes. Most publications (e.g., Alberdi et al., 1995), however, do not specify whether changes in body size are caused by an adaptation to the habitat itself or to some components of the habitat (e.g., forage, predators). Based on the idea that large extant zebras usually dwell in more open habitats as compared to small ones (Alberdi et al., 1995), for example, large- and small-sized extinct Miocene and Pleistocene equids were traditionally correlated with open (e.g., steppes and grasslands) and closed (e.g., woodland) environments, respectively (Alberdi et al., 1995; Ortiz-Jaureguizar & Alberdi, 2003). Alberdi et al. (1995) used this relationship, along with Bergmann’s rule, to provide an explanatory framework for the size trends observed in Pleistocene Equus (Fig. 5.2, see previous section). However, while body size increase in North American Equus might agree with a change from warm humid habitats to colder and drier open environments (Alberdi et al., 1995), a decrease in Equus body size in Europe, Asia and Africa does not match the transition from warm wooded environments to cold open habitats that occurred in these continents (Alberdi et al., 1995). Indeed, given the relationship between body size and landscape’s characteristics described in extant zebras (Alberdi et al., 1995), as well as Bergmann’s rule, the opposite trend would be expected. Other authors have proposed that the body size decrease observed in Equus could have been the result of a decrease in the environment’s productivity during glacial fluctuations (Cantalapiedra et al., 2017). The association between landscape and equid body size, thus, seems to be far more complex than initially proposed by Alberdi et al. (1995) and requires further study. Recent research on the paleodiet of European Pleistocene Equus (Saarinen et al., 2021) shed some light on this issue, as it revealed the opposite relationship between equid body size and habitat. According to Saarinen et al. (2021), large Pleistocene Equus from Europe had a mixed-feeding and browse-dominated diet, and preferentially lived in wooded environments, while small-sized taxa were mostly grazers and appear associated to open habitats. For these authors, differences in body size among Equus were probably driven by resource quality and availability per individual, which is mainly dependent upon population density (Saarinen et al., 2021). Since large-sized species are more abundant than small-sized taxa in those palaeontological sites where both equids appear sympatrically, they propose that large Pleistocene taxa would have lived in smaller groups (Saarinen et al., 2021). This would have allowed large Equus to have access to more resources, and finally achieve a larger body size (Saarinen et al., 2021). Smaller Equus, on the other hand, would have experienced high population densities that might have limited their access to resources and their body size (Saarinen et al., 2021). Generally, shifts in resource availability have been proposed as the most important drivers of body size changes in different extinct ungulates, including middle and late Pleistocene European horses (Boulbes & van Asperen, 2019; Forsten, 1991a; Saarinen et al.,

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2016), Holocene Equus from North America (Guthrie, 2003), the Asiatic E. eisenmannae (Wang & Deng, 2011) and other Pleistocene ungulates from Europe (Saarinen et al., 2016).

Hard Tissue Palaeohistology and Life History Theory: A New Tool and Framework to Study the Evolution of Equid Body Size The study of body size variation in extinct vertebrates, within the framework of the life history theory, is a relatively new area of research (e.g., Köhler, 2010). As explained above, this research considers that body size changes are an indirect result of modifications in specific life history traits to which body size is sensitive, such as growth rate or age at maturity (Palkovacs, 2003). In most living species, information about these demographic characteristics can easily be obtained from field monitoring, but unfortunately, for obvious reasons, this methodology cannot be applied to extinct taxa. Nonetheless, hard tissue (i.e., bones and teeth) palaeohistology can be used as a valuable tool to reconstruct the biology and life history of extinct animals (Chinsamy-Turan, 2005; de Buffrénil et al., 2021; Hogg, 2018; Nacarino-Meneses & Köhler, 2018; Padian & Lamm, 2013) (Box 5.3). Bones and teeth preserve a permanent record of the growth and development of an organism at the tissue level (Klevezal, 1996). By studying different features of fossilized bones, such as the annual microscopic growth marks embedded in the tissue (Köhler et al., 2012) or the pattern and number of vascular canals (de Margerie et al., 2002) (Box 5.3), researchers are able to deduce, with some degree of conviction, the time at which extinct vertebrates achieved skeletal and/or sexual maturity or their rates of growth

Fig. 5.3 Periodical growth marks (white arrows) in the teeth of Equus ferus from La Carigüela (Late Pleistocene, Spain). Collection number IPS87509, Institut Català de Paleontologia Miquel Crusafont (Barcelona, Spain). Credits: Carmen Nacarino-Meneses. (a) Circa-weekly growth marks in the dentine (i.e., Andersen lines). (b) Daily growth marks in the enamel (i.e., enamel laminations)

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(Köhler & Moyà-Solà, 2009; Nacarino-Meneses & Chinsamy, 2021; OrlandiOliveras et al., 2018). Rates and timings of tooth formation and eruption can also be inferred from the analysis of periodical growth marks embedded in dental enamel, dentine and cementum (Fig. 5.3) (Hogg, 2018; Klevezal, 1996; Smith, 2008). This, in turn, allows for the estimation of the key life history parameters age at weaning, age at maturity or age at death, among others (Jordana et al., 2012; Jordana & Köhler, 2011; Nacarino-Meneses & Chinsamy, 2021; Orlandi-Oliveras et al., 2019). Box 5.3. Inferring Life History Traits in Extinct Horses from Bone Histology: The Example of Equus steinheimensis (Middle Pleistocene, Germany) Over the recent decades, bone palaeohistology has become an important tool to deduce life history information in extinct animals (Chinsamy-Turan, 2005). The methodology begins with the preparation of very thin cross-sections (around 100 mm thick) from fossil remains that are later observed under the microscope (a, b) (Padian & Lamm, 2013). Using plane and polarized light microscopy, palaeohistologists analyze certain features of the bone tissue, such as some characteristics of the vascular canals (yellow arrows in c) and the growth marks (white arrows in d) (de Buffrénil et al., 2021). The latter are very thin dark lines that are deposited around birth (Nacarino-Meneses & Köhler, 2018) and every winter thereafter (Köhler et al., 2012). Sometimes, the whole path of these growth marks can be traced along the cross-section (white dotted line in b), providing a proxy of the bone’s perimeter at certain ages that can be used to obtain growth plots (e.g., Nacarino-Meneses & Orlandi-Oliveras, 2021). The middle Pleistocene horse Equus steinheimensis is one of the few extinct equids in which bone palaeohistological analyses have been performed so far (Nacarino-Meneses & Orlandi-Oliveras, 2021). This research has shown that bones of this horse were much more vascularized (i.e., they had a higher number of vascular canals) as compared to those of extant zebras and asses (Nacarino-Meneses & Orlandi-Oliveras, 2021). This, along with the growth plots obtained from the analysis of histological growth marks, suggest that it grew at higher rates than modern equids (Nacarino-Meneses & OrlandiOliveras, 2021). (continued)

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Box 5.3 (continued)

(a) Fragmented metacarpus of Equus steinheimensis from Steinheim an der Murr (Middle Pleistocene, Germany). Collection number 32803/321, Staatliche Museum für Naturkunde Stuttgart (Stuttgart, Germany). Credits: Carmen Nacarino-Meneses. (b) Cross-section obtained from the metacarpus shown in A. Image taken under polarized light in a Zeiss Scope.A1 microscope. The white dotted line indicates the path of a growth mark. Red rectangles indicate areas of image magnifications shown in C and D. Credits: Carmen Nacarino-Meneses. (c) Detail of bone tissue showing multiple vascular canals (yellow arrows). Image taken under polarized light in a Zeiss Scope.A1 microscope. Credits: Carmen Nacarino-Meneses. (d) Detail of bone tissue showing growth marks (white arrows). Image

(continued)

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Box 5.3 (continued) taken under polarized light in a Zeiss Scope.A1 microscope. Credits: Carmen NacarinoMeneses. (e) Growth plot obtained from the analysis of bone growth marks in E. steinheimensis and several extant Equus. Modified from Nacarino-Meneses and Orlandi-Oliveras (2021)

The use of hard tissue palaeohistology, to obtain life history information in extinct horses, has only been applied to a small number of Miocene and Pliocene hipparionines (Martínez-Maza et al., 2014; Nacarino-Meneses & Chinsamy, 2021; Nacarino-Meneses et al., 2021; Orlandi-Oliveras et al., 2018, 2019) and Pleistocene Equus species (Nacarino-Meneses et al., 2017, 2021; Nacarino-Meneses & OrlandiOliveras, 2021; Tomassini et al., 2021). The results obtained to date, however, are highly encouraging and relevant for the analysis of the body size trends observed in Equidae. These works have shown, for example, that the small body size of dwarfed European hipparionines was probably achieved by following two different life history strategies: while taxa from Eastern Europe (e.g., Greece) stopped growing early in ontogeny (advanced maturity) and grew at high rates, species from Western Europe (e.g., Spain) matured later and grew at slower rates (Orlandi-Oliveras et al., 2018). Regarding European Pleistocene Equus, recent research has revealed higher rates of growth in larger middle Pleistocene horses as compared to smaller late Pleistocene and extant species (Nacarino-Meneses et al., 2019; Nacarino-Meneses & Orlandi-Oliveras, 2021). Based on predictive life history models (Palkovacs, 2003), these investigations further provided insights into the selective pressures that may have driven the life history changes that indirectly may have caused body size variation in extinct horses. Specifically, the authors propose that high levels of predation in hipparionines from eastern Europe might have triggered their early maturity (Orlandi-Oliveras et al., 2018), while a decrease in resource availability could have induced slow rates of growth in hipparionines from western Europe (Orlandi-Oliveras et al., 2018) and late Pleistocene and extant Equus (NacarinoMeneses et al., 2019; Nacarino-Meneses & Orlandi-Oliveras, 2021).

Body Size Variation in Extant Wild Equus: Size Unimorphism in Zebras, Asses and Feral Horses Extant wild taxa of Equus comprise three species of zebras (Equus quagga, Equus zebra, and Equus grevyi), three species of asses (Equus africanus, Equus hemionus, Equus kiang) and one species of feral horse (Equus ferus przewalskii) (Groves, 2002; Nowak, 1999). With a mean body mass of almost 400 kg (Ernest, 2003; Fig. 5.2e, Table 5.1), E. grevyi is both the largest zebra and the largest wild equid. E. hemionus (230 kg cf. Ernest, 2003; Fig. 5.2c; Table 5.1), on the other hand, is the

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Table 5.1 Adult body mass of extant wild Equus Group Zebras

Asses

Horses

Common name Plains zebra Grevy’s zebra Mountain zebra African wild ass Asiatic wild ass Kiang Przewalski’s horse

Species name Equus quagga Equus grevyi Equus zebra

Adult weight (kg) 257 384 296

References Ernest (2003) Ernest (2003) Ernest (2003)

Equus africanus

250

Ernest (2003)

Equus hemionus

230

Ernest (2003)

Equus kiang

250–300 females, 350–400 males 200–300

St-Louis and Côté (2009) Nowak (1999)

Equus ferus przewalskii

smallest wild living Equus and ass. Generally, zebras are slightly larger than asses, as the former have a mass of around 300 kg (e.g., E. zebra: 296 kg cf. Ernest, 2003; Fig. 5.2e) while the latter approximately 250 kg (e.g., E. africanus: 250 kg cf. Ernest, 2003; Fig. 5.2e). The kiang, an Asiatic ass endemic of the Tibetan plateau, however, is reported to reach a body mass of 350–400 kg in the wild (St-Louis & Côté, 2009) (Fig. 5.2c, Table 5.1). Nevertheless, this estimation should be considered with caution. Two kiangs from the Bronx Zoo in New York only had a mass of 223 kg (male) and 214 kg (female) (G. Schaller, pers. comm. 28 June 2021). Since zoo animals are usually heavier than wild ones, a mass of 350–400 kg for the wild kiang seems an overestimate (C. Mishra, pers. comm. 29 June 2021). The only living caballoid, the endangered Przewalski’s horse (King et al., 2015), has a mass between 200 and 300 kg (Nowak, 1999) (Fig. 5.2c, Table 5.1). As already noted, all extant species of wild equids are smaller than Pleistocene taxa (Fig. 5.2). Equus are usually considered monomorphic (also termed homomorphic) (Linklater, 2000), meaning that adult males and females are of a similar body size (Fig. 5.4). Although equid males are generally slightly larger than females, these differences are statistically insignificant (Van Asperen, 2013). Mares of Grant’s (Equus quagga boehmi) and Grevy’s zebra (E. grevyi), for example, only weigh 10% less than stallions (Kimura, 2000), and sex-related mass differences in Hartmann’s zebra (Equus zebra hartmannae) are not statistically significant (Joubert, 1974). The lack of sexual dimorphism in most extant equids is also reflected in the size of their metapodia, which overlaps between sexes (Van Asperen, 2013). The height of the pelvic inlet, an anatomical feature more related to reproduction, is, however, sexually dimorphic in true horses (E. ferus) and asses but not in extant zebras (Groves, 2002). Zebra stallions, on the other hand, often present thicker necks as compared to mares, and both sexes even walk differently (H.H.T. Prins, pers. comm. 27 June 2021). Male Przewalski’s horses in the desert of Northern China look massive as compared to females but, intriguingly, stallions of the same species in a safe environment (without wolves and lynxes) in West Europe (or in the zoo) show

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Fig. 5.4 Cape mountain zebras (Equus zebra zebra) in Mountain Zebra National Park (South Africa) showing no signs of sexual dimorphism in body size. The arrow highlights the stallion. Credits: Iñigo Marzo Puerta

much less of this massive neck structure and sheer strength (H.H.T. Prins, pers. comm. 27 June 2021). Generally, body size dimorphism, in terms of body mass, has only been reported in E. kiang (St-Louis & Côté, 2009). Females of this Tibetan ass have a mass of 250–300 kg, while male body mass varies between 350 and 400 kg (St-Louis & Côté, 2009) (Table 5.1). However, mass dimorphism in this species should be corroborated with new measurements and observations since, as previously explained, mass estimations for wild specimens of E. kiang might be overestimated. Some authors have argued that monomorphic equids like E. quagga could have evolved similar body sizes to minimize the costs of synchronizing their feeding behaviour among the different group members (Neuhaus & Ruckstuhl, 2002). Moreover, monomorphic and dimorphic taxa tend to differ in their social structure (Berger et al., 2001). In polygynous animals such as equids, where one male mates with several females while each female mates only with one male, monomorphism would be expected in those species that live in mix-sexed groups (Neuhaus & Ruckstuhl, 2002). This is the case of the non-territorial zebras E. quagga and E. zebra, the feral horse E. f. przewalskii, and some populations of E. hemionus (Feh et al., 2001; Grubb, 1981; Nowak, 1999; Penzhorn, 1988). These equids, which generally dwell in temperate environments, typically live in permanent groups of one stallion and several females and their offspring (i.e., harems) within large herds (Feh et al., 2001; Grubb, 1981; Nowak, 1999; Penzhorn, 1988) (Fig. 5.4). In these harems, breeding might occur at any time during the year—although it usually takes

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place during the favourable season—(Klingel, 1974), and males do not fiercely compete for access to females (Neuhaus & Ruckstuhl, 2002). Thus, sexual selection might not generally favour a male increase in body size. In some populations of tarpans (feral horse) in the Netherlands, North America, New Zealand or Australia, however, harems might comprise one dominant stallion and several subordinate males (Linklater, 2000; Linnartz & Linnartz-Nieuwdorp, 2017). In such populations, the dominant male is the one who usually mates with mares, while subordinate stallions defend the harem (Linnartz & Linnartz-Nieuwdorp, 2017). These different roles within the social system might have prevented an increase in male body size. Yet, not all wild equids live in a herd or harem system. The territorial species adapted to arid environments, like the Grevy’s zebra, the African ass, the Kiang, and some populations of E. hemionus, do not form adult permanent bonds (Feh et al., 2001; Grinder et al., 2006; Nowak, 1999; St-Louis & Côté, 2009). In these taxa, adults are commonly sexually segregated into groups of mares or mares and foals, and in male groups of bachelors or solitary stallions (Grinder et al., 2006; Nowak, 1999; St-Louis & Côté, 2009). Mixed groups can also occur, but they are always temporal and with no bonds (Grinder et al., 2006; Nowak, 1999; St-Louis & Côté, 2009). Mating opportunities are further reduced in these species, as this only occurs during the few months of the favourable rainy season (Klingel, 1974). Under these circumstances of sexual segregation and limited reproductive opportunities, sexual dimorphism in body size might also be expected (Berger et al., 2001). Specifically, a large male size will be selected for because of sexual competition and thus to get a prolonged access to females and/or to resources attractive to females (Andersson, 1994). Among equids living in arid environments, however, only the Tibetan kiang shows a slight male-biased dimorphism (St-Louis & Côté, 2009) (but see before the discussion of possibly unreliable body mass estimations for wild specimens of this species). Maybe, the low resource availability of these habitats has not allowed an increase in male size in arid-adapted equids, which instead might have relied on a territorial behaviour to provide females access with resources and, therefore, to increase their mating success. Why E. kiang is both territorial and sexually dimorphic (if it really is) remains unresolved, and only future studies on its ecology and sociology might shed some light on this issue.

Body Size Variation in Domesticated Equus: About Miniature Donkeys and Draught Horses Domesticated species of Equidae include the horses (Equus caballus), the donkeys (Equus africanus asinus), and the sterile horse-donkey hybrids known as mules and hinnies (Orlando, 2015). Over the last 6000 years, these mammals have been shaped through artificial selection to obtain an array of breeds that differ in behaviour, physiology and morphology (Orlando, 2015). One of the most striking differences among equid breeds is their variation in body size (Brooks et al., 2010) (Fig. 5.5). In

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Fig. 5.5 Body size variation in donkeys (a, b) and domesticated horses (c, d). (a) Poitou donkey (height at the withers of 140–155 cm). Credits: Amada44 under CC BY 4.0 (https:// creativecommons.org/licenses/by/4.0/). (b) Miniature Sardinian Donkey (height at the withers less than 90 cm). Credits: Jim Linwood under CC BY 2.0 (https://creativecommons.org/licenses/ by/2.0/). (c) Miniature horse (height at the withers less than 90 cm). Image distributed under licence CC BY 2.0 in Wikimedia Commons. Credits: Just chaos under CC BY 2.0 (https:// creativecommons.org/licenses/by/2.0/). (d) Shire horse (height at the withers of 175 cm). Credits: Julian Tysoe under CC BY 2.0 (https://creativecommons.org/licenses/by/2.0/)

horses and donkeys, this biological feature has actively been selected over centuries to meet a variety of human requirements related to agriculture, warfare, and transportation (Dohner, 2001; Orlando, 2015). This has ultimately led to more than 800 and 200 horse and donkey breeds, respectively (FAO, 2019). With a withers height of 140 cm, the American Mammoth Jackstock and the Poitou are the largest breeds of donkeys (Dohner, 2001) (Fig. 5.5a). They are usually employed in agricultural works, although the American Mammoth Jackstocks are also good riding animals (Dohner, 2001). Miniature Mediterranean donkeys (Fig. 5.5b), on the other hand, constitute the smallest donkey breed (Dohner, 2001). Their height at the withers of less than 90 cm makes them the ideal pet in some areas of America and England (Dohner, 2001). The withers height of the smallest domesticated horses, i.e., the North American miniature and the Falabella horse, is also less than 90 cm (Brooks et al., 2010) (Fig. 5.5c), while their mass is around 100 kg (Malinowski et al., 1996). These small-sized horses are also often kept as pets, and they are commonly used for research (Dohner, 2001). Conversely, the largest breeds of domesticated horses are much taller than the largest donkeys. The Shire and the

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Clydesdale draught horses (Fig. 5.5d), for instance, present an average height at the withers of more than 175 cm (Brooks et al., 2010). Large-sized draught horses, such as the Percheron and Breton breeds, have a mass of around 850 kg (Ozawa et al., 1995). All these heavy draught horses were traditionally used in farming, war or transport, and nowadays they constitute the most common carriage horses (Dohner, 2001). The analysis of body size variation in domesticated Equus, as well as the study of its relationship with the biology of these mammals, has received more attention in horses as compared to donkeys. Recent research has shown, for example, that the small-sized Shetland ponies (height at the withers ~100 cm cf. Brooks et al., 2010) and the large-sized Shire horses (height at the withers ~175 cm cf. Brooks et al., 2010) present similar gestation lengths (Heck et al., 2017). This suggests that this specific life history trait is not influenced by body size in domesticated horses (Heck et al., 2017). Large and small horse breeds differ, however, in their absolute birth weight, probably as a result of differences in prenatal growth rate among breeds (Heck et al., 2017). The rate and duration of postnatal growth also vary among horse breeds of different body sizes (Heck et al., 2019). Specifically, differences in skull shape and morphology between different-sized breeds suggest that large-sized breeds grow more slowly and over longer times as compared to small-sized ones (Heck et al., 2019). As a result, the skull of adult miniature horses (height at the withers 148 cm) (Heck et al., 2019). As in other domesticated mammals, body size in domesticated horses is controlled by a small number of genes (i.e., fragments of DNA that contribute to the phenotype or to a specific function) and loci (i.e., locations of genes within the chromosomes). Specifically, four quantitative trait loci (QTLs) on chromosomes 3, 6, 9, and 11, respectively, contain a variety of genes that explain more than 80% of the variation in size at the withers observed in horse breeds (Makvandi-Nejad et al., 2012). The QTL in chromosome 3 harbour the ligand dependent nuclear receptor corepressor-like (LCORL) and the non-SMC condensin I complex subunit G (NCAPG) genes (Makvandi-Nejad et al., 2012; Petersen et al., 2013; Signer-Hasler et al., 2012). The high mobility group AT-hook 2 (HMGA2), the zinc finger and AT hook domain containing (ZFAT) and the LIM and SH3 protein 1 (LASP1) genes, on the other hand, are found in QTLs in chromosomes 6, 9, and 11, respectively (Makvandi-Nejad et al., 2012; Petersen et al., 2013; Signer-Hasler et al., 2012). Research has shown that all these genes determine the withers height in domestic horses (Makvandi-Nejad et al., 2012; Petersen et al., 2013; Signer-Hasler et al., 2012). Nevertheless, LCORL has been postulated as the most important gene for body size variation within and across horse breeds (Metzger et al., 2013). Interestingly, HMGA2 seems to play an important role in the selection of small stature in Shetland and the Debao ponies (Frischknecht et al., 2015; Liu et al., 2020). In these miniature breeds, additional genes such as the TBX3 (Kader et al., 2016), the ADAMTS17, the OSTN and the GH1 (Metzger et al., 2018) have further been described in relation to their small body size.

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Important mammalian growth hormones such as insulin-like growth factor 1 (IGF1), triiodothyronine (T3) and thyroxine (T4) do not seem to play a key role in the body size variation observed in domesticated horse breeds (Caetano & Bowling, 1998; Malinowski et al., 1996; Ozawa et al., 1995; Reader et al., 2011). Several studies have shown, for instance, that plasma levels of IGF1 do not correlate with adult body mass in these mammals (Malinowski et al., 1996; Ozawa et al., 1995). Specifically, plasma concentrations of this hormone vary greatly among horse breeds (Malinowski et al., 1996), but miniature (e.g., Shetland pony, 110 kg) and light horses (e.g., Thoroughbred horses, 400–500 kg) do not present lower levels of IGF1 as compared to heavy breeds (e.g., Percheron, 850 kg). Similarly, differentsized horse breeds do not show allelic variation of IGF1 gene (Caetano & Bowling, 1998; Reader et al., 2011), and, therefore, it is unlikely that this hormone regulates adult body size in domesticated horses (Reader et al., 2011).

Conclusions The evolution of equid body size is a key research topic in numerous scientific disciplines, including palaeontology, zoology, and veterinary sciences. The longstanding notion of Equidae conforming to Cope’s rule is now completely debunked, since body size evolution in these mammals is known to involve both phyletic gigantism and dwarfing, as well as periods of size stasis. Within the genus Equus, a chronological cline of size increase has been described in North American horses during the Pleistocene. Conversely, equids slightly decreased in size in Asia, Europe and Africa during the same epoch. Based on the close relationship that exists between body size and the ecology of a species, evolutionary changes in equid body size have traditionally been related to differences in habitat, diet and/or behaviour. Recently, however, research based on life history theory and hard tissue palaeohistology suggests that equid size trends might have resulted from modifications in the timing and rate of key life history traits to which adult body size is sensitive, such as the age at maturity and/or the growth rate. Regardless of the traits and features of selection (i.e., body size or life history parameters), it is apparent that extant wild Equus are smaller as compared to their extinct direct relatives. Extant wild Equus are generally not considered sexually dimorphic in mass. In temperateadapted species (e.g., E. quagga, E. zebra) this may be related to their social organization in herds or harems, which likely promotes low male competition. In arid-adapted species, such as E. grevyi and some populations of E. hemionus, their territorial behaviour might be the reason behind the general lack of sexual dimorphism in mass. Since the beginning of horse domestication 6000 years ago, body size has been an important biological feature under the scrutiny of artificial selection. As a result, height at the withers in donkeys and domesticated horses ranges 90–140 cm and 90–200 cm, respectively. Moreover, adult body mass of domesticated horse varies between 100 and 850 kg. Recent research has shown that largeand small-sized horse breeds differ in growth pattern and life history traits, and that

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most of the size variation observed in these domesticated mammals only depends on a small number of genes and loci. Acknowledgements I thank the editors of this book, Prof. Herbert H.T. Prins and Prof. Iain J. Gordon, for inviting me to write this chapter on the evolution of equid body size. They are also acknowledged, along with Dr. Juan L. Cantalapiedra, for providing useful revisions that highly improved earlier versions of this chapter. I am grateful to Prof. Anusuya Chinsamy-Turan (University of Cape Town) for her encouragement and support during the initial writing of this manuscript and my time as a postdoctoral fellow at the University of Cape Town. DST-NRF Centre of Excellence in Palaeosciences (South Africa) is acknowledged for providing support through grants COE2019-PD03 and COEPD2020-39. This research also received support from the Spanish Ministry of Science and Innovation through the Spanish State Research Agency (PID2020117118GB-I00 funded by MCIN/AEI/10.13039/501100011033), the Beatriu de Pinós program funded by the Ministry of Research and Universities of the Generalitat de Catalunya (2021 BP 00078) and the CERCA Programme (Generalitat de Catalunya). The consolidated research group Evolutionary Paleobiology (EPB) is recognized without funding by AGAUR (Generalitat de Catalunya) (2021 SGR 01184).

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Chapter 6

Forage Consumption and Digestion in the Modern Equids Iain J. Gordon and Herbert H. T. Prins

Abstract Equids are herbivores that consume a wide range of plant species and plant parts. They have adaptations of their anatomy, physiology, and microbiology (still in this infancy as a scientific research area) that help them crop, masticate, and digest forage of a range of qualities. The major anatomical structures that distinguish equids are their hypsodont and selenodont teeth (able to finely masticate forages) and their hindgut (caecum and large intestine). Overall equids appear to be able to derive much of their nutrition from the soluble parts of the cell and the easily digests parts of the cell wall. They are also not constrained (as are ruminants) by high cell wall and large particles in the alimentary tract, clearing the way for more intake. This means that equids appear to have a high intake, fast throughput strategy as compared to ruminants. Some recent studies suggest that the lack of proline-rich proteins in the saliva limits the ability of zebras to consume a diet high in tannins (i.e., from bushes and trees) but kulans and kiangs consume much browse and forbs. Most of our knowledge on foraging and digestion comes from domestic horses, meaning that there is still a great deal to be learnt about the diversity of anatomy, physiology, and microbiology of equids in the wild. Recent microbiome studies show how different they can be between equid species living in the same area, making it likely that not all equids are equal. In conclusion, the long-held view that equids are better adapted to consuming very low- and very high-quality forages than are ruminants may still stand but this is largely based on studies on domestic horses versus sheep and cattle. What is becoming more apparent is that the foraging and digestion strategies of equids are different from and not inferior to those of ruminants.

I. J. Gordon (*) Fenner School of Environment & Society, Australian National University, Canberra, ACT, Australia e-mail: [email protected] H. H. T. Prins Department of Animal Sciences, Wageningen University, Wageningen, The Netherlands e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 H. H. T. Prins, I. J. Gordon (eds.), The Equids, Fascinating Life Sciences, https://doi.org/10.1007/978-3-031-27144-1_6

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Introduction Of all the things that animals do, feeding is often the way that we chose to describe them—be they carnivores, insectivores, or herbivores. This is because feeding is fundamental to the way of life of animal species—how they garner nutrition from their environment provides individuals with the resources they need to grow, survive, and reproduce (Prins & van Langevelde, 2008). Feeding also shapes much of their anatomy, physiology, behaviour, and from more recent research, their microbiology. Fortunately, the hard structures (bones, teeth, and the like) of animals are generally well preserved in the fossil record, allowing researchers to interpret the feeding type of long-dead species. Recent advances in the use of isotopes, microwear, and phytoliths (e.g., Merceron et al., 2016; Roberts et al., 2018) means that we can analyze the teeth and bones of fossils to determine their diets and validate the interpretation from the anatomy of the hard structures (see Cantalapiedra, Chap. 2; Janis et al., Chap. 3). We realize that there are many other traits to consider that did not leave traces in the fossil record but which we may deduce through other means (see De Jong & Prins, Chap. 4). Yet, the hard anatomy gives us a reasonable understanding of the relationship between the animal and its food supply and allows us to see the evolution of adaptations for animals to survive in a changing world. Darwin, the paterfamilias of evolutionary theory, knew this well and used the variation in the beaks of finches and mockingbirds on the Galapagos (but not their guts or digestive details: Michel et al., 2018) to posit selection pressures driving changes in the feeding behaviour and anatomy on different islands in the archipelago, ultimately leading to speciation. More recently, the cycles of rainy seasons and droughts on the island of Daphne Major in the Galapagos have seen shifts in the prevalence of species of finches with beaks suited to consuming soft and hard seeds, respectively (Grant & Grant, 2014); evolution in operation in front of our eyes. Whilst animals that eat other animals are generally able to use their own enzymes to digest the majority of what they eat (excepting chitin, fur, and enamel), large mammalian herbivores face the challenge of digesting the bulk of plant material that is refractory to mammalian hydrolytic enzymes (i.e., the walls of plant cells). In newly growing plant material, the proportion of cell wall is lower than in more mature material, even then cell wall still generally makes up over 50% of the material consumed. Natural selection has favoured mammalian herbivores that acquired symbiotic relationships with microbes that are able to break down this material; parallel evolution took place in birds, e.g., in ptarmigan (Lagopus spp.) (Moss, 1977), ostrich (Struthio spp.) (Swart et al., 1993), and hoatzin (Opisthocomus hoazin) (Jones et al., 2000). These microbes require a set of specific environmental conditions (e.g., pH, temperature, nitrogen concentration) in order the digest plant cell walls, and the guts of these herbivores contain sites that have evolved to meet these conditions (whilst other parts of the gut are not conducive for the microbial communities). In turn, the microbes liberate volatile fatty acids (VFAs) (Fig. 6.1) that are absorbed through the animal’s gut wall and fuel the mammalian host’s

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Fig. 6.1 The chemical structure of some volatile fatty acids. They are the waste product of microbial digestion in the rumen and caecum of terrestrial herbivores and form the main source of energy for their equid or ruminant host. Formic acid has one carbon atom; acetic acid has two; propionic acid has three; etc.

activities. The most important VFAs are acetic acid (CH3.COOH), propanoic acid (CH3.CH2.COOH), and butyric acid (CH3.CH2.CH2.COOH) which are used as energy sources. This host–microbe symbiotic relationship appears to be tens of millions of years old, taking on many forms and occurring in different structures within the herbivores’ guts. Both in equids and in ruminants, these VFAs yield about 70% of the energy for the animal. See for more details Bergman (1990) and Fig. 6.2. In this chapter we describe the digestive anatomy and function of extant equids; the basis upon which they can digest the variety of plant foods that they consume. Below we will compare and contrast the digestion of the equids and the ruminants, not to determine which is ‘better’ at processing plant material but to show how evolution has led to very different adaptations to herbivory in the cervids/bovids and the equids.

What Is the Biological and Evolutionary Basis for Foraging and Digestion? Fundamentally they are to garner nutrients that lead first to satiation, then survival, and ultimately to lifetime reproductive success. This is done within the limits imposed on the animal by edaphic, climatic, and biotic constraints and the physiological and anatomical constraints of the animal itself. Animals that are not able to meet their metabolic needs for maintenance, growth, or reproductive activity die or are not able to take as active a part in reproductive activities as their conspecifics, and so do not leave as many offspring. So, the evolutionary pressure on food intake and

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Fig. 6.2 Fatty acid (FA) synthesis pathway in ruminants. Microbes ferment polysaccharides into volatile fatty acids such as acetate, propionate, and butyrate in the rumen. The acetate and propionate acid can contribute to fatty acid (FA) synthesis. Acetate is converted to acetyl-CoA in the cytoplasm of ruminant cells and is used to synthesize FA. Propionate is transported into mitochondria where it enters the tricarboxylic acid cycle via succinyl-CoA and can be utilized as a substrate for the production of glucose via gluconeogenesis. Glucose, which is synthesized from propionate or rumen-bypassed and absorbed in the small intestine, can generate citrate in the tricarboxylic acid cycle, where it can be transported into the cytosol. The citrate in the cytosol is degraded into oxaloacetate and acetyl-CoA by ATP-citrate lyase, and the acetyl-CoA can be used to synthesize FAs (figure and legend from Park et al., 2018; courtesy of Animal Bioscience)

digestion is significant, particularly in challenging periods of an animal’s life (e.g., drought, dry season, winter) or in challenging environments (e.g., steppes, deserts, mountains, and tundras). This means that animals either have a flexible foraging and digestion system or have a system that is specifically adapted for tough times.

How Do Other Large Herbivores (Including Other Perissodactyls and the Artiodactyls) Digest Their Forage? The major taxa of extant large mammals that are herbivores feeding on terrestrial plants are the rhinoceroses, tapirs, and horses and their relatives (Perissodactyla) and the ruminants, that is, deer, antelopes, ovines, bovines, and giraffe (Artiodactyla). It should be noted that suids are members of the Artiodactyla but are relatively poor at digesting plant cell walls whereas camelids and the hippopotamus (Hippopotamus

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amphibius) are somewhere in between (Farrell & Johnson, 1972). The key dichotomy between these two major phylogenetic Orders of large mammalian herbivores is the fact that the perissodactyls have the major chambers that hold the symbiotic microorganisms in the modified colon and caecum (Fig. 6.3a), whereas most artiodactyls house them in a modified stomach (the number of chambers in the stomach varies depending upon the family) (Fig. 6.4). Even when stomachs are considered quite ‘simple’, they can host microbes that produce volatile fatty acids, as in collared peccary (Dicotyles tajacu) (Langer, 1978) or hippopotamus (Langer, 1976). If we first look at the ruminant digestive system. The ruminant stomach is the more recently evolved anatomy (50 Mya: Hackmann & Spain, 2010; 35 Mya Chen et al., 2019), which can deal with the breakdown and release of the nutrients held within plant cell walls (Choudhury et al., 2015). Probably, it initially evolved under selective pressure to deal with antifeedants in plant leaves and to allow for a longer passage time for digestion (see De Jong & Prins, Chap. 4) when ancestral forms moved away from a diet dominated by fruits, grubs, eggs, and rodents (like modernday Duiker antelopes) (cf. Kohl & Dearing, 2012; Kohl et al., 2014; Ley et al., 2008). The rumen appears to be the most “advanced” in terms of changes to the mammalian digestive tract (Fig. 6.4). Here there has developed a series of compartments in the forestomach—the rumen, reticulum, omasum, and abomasum (the latter is like the non-ruminant stomach) (Fig. 6.5). Note that the camels and their relatives have three compartments and the pigs and Hippopotamus have two compartments; we will not be dealing with these taxa here but see Fig. 6.4. The distantly related cetaceans also have four stomachs, but microbial digestion does not take place in dolphins but does occur in baleen whales (see Aznar et al., 2006; Mathiesen et al., 1995; Tarpley et al., 1987). In ruminants, the microbes live in the rumen and the reticulum, and the released energy and nutrients are absorbed across the walls of the digestive tract. The acidity and enzymes in the abomasum digest food in a similar way as in other mammals. One of the key features of the behaviour of ruminants is chewing the cud or rumination. This behaviour is unique to the ruminants (of course there is an exception in that the camelids too chew the cud) and occurs with them regurgitating the large particles of plant material held in the rumen, chewing the bolus, and swallowing it (Lechner-Doll et al., 1991). This reduces the size of the plant particles in the rumen (as small as 0.5 mm: Hofmann, 1989), increasing the surface area of the plant material on which microbes can act. Plant material must be broken down by chewing and microbial fermentation to pass from the rumen-reticulum into the omasum, and from there to the abomasum and the rest of the digestive tract. This retention of material in the reticulo-rumen helps to ensure effective digestion of the plant cell wall material. Ruminants will spend up to 10 h a day ruminating if the quality of the plant material is poor and the cell walls are difficult to break down, but the trade-off between allocating time to grazing versus ruminating is not straightforward (Prins, 1996, pp. 53 ff.). Rumination, the grinding of plant material in the pre-molars and molars has also led to the evolutionary loss of the upper incisors and canines (or vestigial canines) in ruminants (DeMiguel et al., 2014) as did some extinct relatives of the equids (namely

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Fig. 6.3 (a) Simplified representation of the digestive systems of hindgut fermenters (top) and ruminants (bottom). Note that nutrients that are obtained through digestion also enter the body but this is not indicated in the figure. Copied from Open University course ‘Studying mammals: Plant predators’, adapted from: Macdonald, D. (ed.) (2001) The New Encyclopaedia of Mammals,

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Chalicotheres: Prothero, 2017: pp. 195; see Janis et al., Chap. 4). Therefore, when normally foraging ruminants clasp plant material between their lower incisors and a fleshy pad where the upper incisors would have been found (only Bovini use their tongue if the grass is long enough). In contrast, some (but not all) extant perissodactyls, i.e., equids and tapirs (e.g., Hohl et al., 2020) retained their upper incisors (Fig. 6.6). However, African rhinoceroses have neither canines nor incisors (but flat or prehensile lips: white rhinoceros [Ceratotherium simum] and black rhinoceros [Diceros bicornis], resp.) whereas Asiatic species have one or two upper, but generally no lower, incisors in each half of the jaw (they have no upper canines but have sharp lower canines). Note that in ruminants the soil that is ingested is washed off in the rumen before the major chewing activity of rumination of regurgitated food. This may have an effect that molars wear at a slower rate than otherwise: indeed, very old ruminants, just like very old equids or elephants, may die because their molars are not functional anymore (I. Gordon pers. obs.; see also Ackermans et al., 2019). Data have not shown a clear pattern between different groups of herbivores (Damuth & Janis, 2014). Equally, the postulated deterrence of silica in plant material (grasses mainly, e.g., McNaughton et al., 1985) is not born out by the data (Sanson et al., 2017; Strömberg et al., 2016). One common feature of herbivory in both artiodactyls and perissodactyls is that to derive the energy and nutrients they need, foraging takes up a large part of every 24-h cycle (ruminants also must ruminate), and the weight of digesta is normally about 40% of body weight in ruminants and in horses only 15% (Benedict, 1936); in carnivores it is some ten times less (De Cuyper et al., 2020). So, the energy needed to maintain the optimal conditions for the microbes, and to carry the weight of digesta around is not insignificant relative to that of animals that eat other animals. Along with a presumed optimization of the weight of material carried in the gut to ensure the adequate supply of nutrients, the need to escape predators has a major impact on the adaptations of the anatomy and behaviour of the mammalian herbivores (see Kaashoek et al., Chap. 13; Rubenstein, Chap. 12). We will deal with the horses and their relatives (the Equidae that are part of the Order Perissodactyla) in the next section, but first we will briefly describe the digestive system of the other perissodactyls. The rhinoceroses and tapirs also eat a lot of vegetation, but the tapirs include up to one-third fruit in their diet (Bodmer, 1990). Of all rhinoceros species, the Sumatran rhinoceros (Dicerorhinus sumatrensis) may have a diet most like that of tapirs, but their diet does not comprise much fruit (Van Strien, 1985; Lee et al., 1993). Rhinoceroses and tapirs also house the microbial communities in the large intestine and caecum that digest and ferment the vegetative material that they consume. Their digestive tract does not have the same mechanisms to slow down the passage of plant material as described above for > ⁄ Fig. 6.3 (continued) Oxford University Press ©. With kind permission from Professor David Macdonald. (b) Schematic representation of an equid’s intestinal system. Most microbial digestion of refractory plant cell wall material takes place in the hindgut but hardly any in the ‘small colon’. Adapted from UGA Extension Bulletin 1449 . Equine Colic. With permission Dr Elodie Huguet

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Fig. 6.4 Schematic representations of the stomach structure of herbivores including ruminants and other artiodactyls. The top left simple stomach structure is that of humans or equids. Arrows indicate generalized movements of ingesta from the oesophagus (in all seven figures on the top-left) to the intestine (in all figures on the bottom-right). See for more detail of the typical ruminant stomach Fig. 6.5. Source: Pérez-Barbería (2020). Courtesy of Springer Nature

Fig. 6.5 The ruminant’s gastrointestinal tract. Black arrows indicate the direction of flow of food, and the white arrow is the regurgitation of food for rumination. Source: Pérez-Barbería (2020). Courtesy of Springer Nature

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Fig. 6.6 (a) The skull of a stallion. Note the incisors with which it could crop grass short, and the canines (typical for a male). Source: Vassil, Public Domain, https://upload.wikimedia.org/ wikipedia/commons/3/32/Cr%C3%A2ne_cheval.jpg). (b) The upper side of the mastication and biting apparatus of an adult stallion (‘maxillary arcade’) (courtesy Richard Bowen, Colorado State University). (c) The jaw or underside of the mastication and biting apparatus of an adult stallion (‘mandibular arcade’) (courtesy Richard Bowen, Colorado State University). (d) Teeth of equids are hypsodont as is well-illustrated in this worked-open skull of a young horse showing its long cheek teeth (courtesy Richard Bowen, Colorado State University)

ruminants, and so the digestion of plant cell material in the guts of rhinos and tapirs is not as extensive as it is in the guts of ruminants. They do, however, have their site of mammalian enzyme digestion before the sacs housing the microbes and so, in the case of the tapir, appear to be able to exploit nutritious fruit using normal mammalian digestion in the stomach (Bodmer, 1990). Apparently, therefore, perissodactyls, including rhinoceroses and tapirs appear to be better at using starch, oils, and sugars as a source of energy (see Prins & De Jong, Chap. 4 for more details).

How Do Equids Collect and Ingest Their Forage? That is the background and now we come to the interesting part of the story as we focus on forage consumption and digestion in the equids. Our narrative shows that rather than being some evolutionary “has been” (in terms of the efficient exploitation of plant material) (cf. Cantalapiedra, Chap. 2; De Jong & Prins, Chap. 4; Gordon & Prins, Chap. 15; Janis et al., Chap. 3; Kaashoek et al., Chap. 13; Prins & Gordon, Chap. 1), playing second fiddle to the ruminants, equids are extremely good at

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Fig. 6.7 Horses are good in cratering (like reindeer and caribou) in snow, like these Siberian horses (courtesy of Susan Alexandra Crate https://susanalexandracrate.squarespace.com/)

gathering nutrients under very challenging conditions (see also Clauss et al., 2003; Duncan et al., 1990; Janis, 1976, 1989; Langer, 1987). In taking a deeper dive into the foraging and digestion of equids we will start with the ingestion of forages, their processing, through digestion, and then voiding what is not used. Whilst equids forage, plant material is gleaned from the environment by clasping together the upper and lower incisors (Fig. 6.6a–c). These incisors are big and strong and can crop tough as well as fresh plant growth. They can crop grass swards even when these are very short (one of the characteristics of equine pastures is these shortcropped areas of new growth). Yet, in dystrophic savannas, sour veld, miombo woodlands (where few sward-forming grasses occur), or in sea buckthorn (Hippophaë spp.) and willow (Salix spp.) thickets along brooks in the TransHimalaya or Inner Asia with tall grasses, equids snap grasses much more superficially and often feed on culms (H. Prins pers. obs.). Burchell’s zebra (Equus burchellii) do the same in the tall grasslands of the Serengeti or in the sourveld of southern Africa. Equids also have very mobile lips, and these can sort out the preferred morsels from the thatch prior to the food items being bitten off (e.g., https://www.storyblocks.com/video/stock/horse-grazing-eating-green-grass-closeup-mouth-lips-teeth-chewing-h1bavj0upkh1sjjbo). In stony grasslands or in snow, the lips are used to selectively feed on clean forage; horses, mules, and donkeys with their lips to move away stones and pebbles whilst simultaneously gathering forage leaves to bite off (H. Prins pers. obs.). Horses can even dig well to reach their food (Fig. 6.7). Once the material is taken into the mouth, it is chewed by the molars before it is swallowed; this could affect the ability of the animal to take the next bite (i.e., not being able to nip and chew at the same time) (Gross et al., 1993); however, horses appear to maintain a rhythmic chewing motion whilst foraging (Dittmann et al.,

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2017) that may mean that biting and chewing are not competitive processes as they are in ruminants. Effective chewing in equids increases the digestibility of the food, both of roughage as well as of seeds. In the equids, the chewing of the food upon first ingestion is an important part of the process of gaining nutrition from plants (Janis et al., 2010). Equids have extremely large molars and premolars, so called hypsodont teeth (i.e., with high-crowned teeth and enamel extending past the gum line; from Greek ‘hypsos’ is ‘height’ and Latin ‘dentes’ meaning teeth) (Fig. 6.6d). Hypsodonty may have evolved in response to an increase of grass in the diet over the course of time even though hypsodont browsing horse-like animals also evolved (see Janis et al., Chap. 3), and some browse species are very abrasive too (Jordana et al., 2012). Leaves of Cordia monoica are even used as sandpaper in East Africa, and a great variety of leaves of browse species contain phytoliths to the same extent as do grass species (Piperno, 1988; Rabenold & Pearson, 2011). It also has been suggested that hypsodonty evolved as an adaptation to buffering the animal against the soil that is ingested whilst feeding on plants close to the ground (Hatt et al., 2019). However, results reported by Strömberg et al. (2016) and Sanson et al. (2017) also make this explanation unlikely. Perhaps the best explanation is that because hypsodont teeth are long lasting, they enable longevity (see Carranza et al., 2004; Jordana et al., 2012). Another feature of the molars of both ruminants and equids is the evolution of selenodonty—teeth with crescent-shaped patterns of enamel and dentin (from Greek ‘selene’ for moon) (see the patterns in the molars of Fig. 6.6b, c). This entails molars to ‘maintain a consistent occlusal morphology throughout the wear process. Therefore, molars are particularly effective grinding tools because as they wear down, the occlusal surfaces become a series of sharp-edged enamel ridges separated by deep depressions and low-lying islands of dentin’ (DeMiguel et al., 2014). Over evolutionary time, the occlusal surface became increasingly complex (Evans & Janis, 2014) and probably increasingly good at grinding. Ingestion chewing in horses leads to very small, ingested food particles that are smaller than that which ruminants achieve when first chewing food (Clauss et al., 2009); horses can grind seeds much finer than can cattle or sheep (Dittmann et al., 2017; Zwirglmaier et al., 2013). The evolution of selenodonty enables the fine grinding of cropped food. Then we come to a key point which is that as forage quality declines (i.e., a greater proportion of the plant material is cell wall) equids would be expected to chew the food for longer (for any given bite size) to reduce the particle size of the swallowed material and improve the efficiency of digestion (Janis et al., 2010; Müller, 2011). They appear to do so (Edouard et al., 2010). Horses, like ruminants (and in contrast to omnivores) have saliva without amylases (Boehlke et al., 2015); they digest starch in the small intestine and in the caecum (Richards et al., 2004). Equid chewing is very important not only for fractioning fibrous material but also for mechanically rupturing the starch grains that otherwise cannot be attacked by amylases after ingestion (Van Soest, 1982 pp. 106). Starch, which is a polysaccharide, forms an important component of the diet of horses, in contrast to that of ruminants, and upon digestion yields glucose (see De Jong & Prins, Chap. 12). Yet horses should not consume too much starch in their diet because when the starch load is too high, not all is digested in the stomach or in

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the small intestine, and starch then would enter the caecum where bacteria convert it into lactic acid. This, in turn, lowers the pH to such an extent that severe mortality of the cellulytic bacteria in microbiome may occur (comparable to acidosis in ruminants), but a proliferation of bacteria that thrive at a low pH may include some pathogenic bacteria. The net result is the production of endotoxins. These then enter the blood circulation and may even lead to death. The symptoms of these are called colic (see Huguet & Duberstein, 2015). An interesting approach to investigating ingestion in herbivores has been to see chewing as being limited by two processes, one is the power the muscles can actively enforce on the chewing activity, and the other is the amount of saliva required to wet the material before it can be swallowed (Virot et al., 2017); note that horse saliva does not appear to contain much proline-rich protein for binding to plant tannins (see De Jong & Prins, Chap. 4 on the effect of polyethylene glycols and browse consumption). As forage quality declines the amount of lubricant supplied by the forage declines and, therefore, the amount of saliva required before swallowing increases. Lubrication, however, can be impaired by tannins in the food that bind the muco-proteins in the saliva. Rather than being purely foragers of grass, in which there are no or very few tannins, as is suggested by their highly hypsodont teeth, some equids consume a variety of shrubs and trees as well as grass and forbs (see above; De Jong & Prins, Chap. 4), depending upon the circumstance or time of the year. These may contain many tannins. Of all equids, Grevy’s zebra (Equus grevyi) appears to be a one-hundred percent grazer, but forbs (e.g., Indigofera spp.) form a non-trivial component of diet in plains zebra across Africa (unpublished data Robert Pringle). In Hwange NP (Zimbabwe) and Addo NP (South Africa), Robert Pringle and his co-workers recorded ⁄ Fig. 8.6 (continued) 2015). The winter in these areas is extremely cold and dry. In contrast, the two places in Alaska that horses could sustain themselves across winter, White River and Healy (Guthrie & Stoker, 1990), have milder winter with slightly more snow

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Fig. 8.7 Yakutia in Arctic Russia is considered to be the coldest inhabited place on the Earth and the Yakut Horses have rapidly adapted to the extreme cold, aridity, and coarse vegetation (photo— Svetlana Ivanova, https://upload.wikimedia.org/wikipedia/commons/7/78/%D0%AF%D0%BA% D1%83%D1%82%D1%81%D0%BA%D0%B8%D0%B5_%D0%BB%D0%BE%D1%88%D0% B0%D0%B4%D0%B8.jpg, CC BY 3.0 (https://creativecommons.org/licenses/by/3.0/))

et al., 2020). In winter, when forage availability may be considerably lower and is usually of a much poorer quality, equids usually reduce their intake that is facilitated by their lowered metabolic rate and slower passage of forage through the gut (Kuntz et al., 2006). Since much of the faeces retains semi-digested forage, coprophagy is quite common among equids during all seasons (Schoenecker et al., 2016). Most equids need to drink every day, especially if they cannot obtain enough water through succulent forage. Often, however, they may use foraging areas based on proximity of water sources (Schoenecker et al., 2016). The kulan is best adapted to water deficient conditions and can venture over 20 km from water sources, even utilizing saline water (Nandintsetseg et al., 2016; Šturm et al., 2017) and digging to access water (Feh et al., 2002). Based on this ability, kulan can utilize vast areas, moving on average 8 km/day (Lugauer, 2010), with annual home ranges of ca. 5000–70,000 km2 (Kaczensky et al., 2008, 2011). Not much is known about water dependence of kiang, but they rarely are seen utilizing fresh water from rivers and streams (Schaller, 1998; St-Louis & Côté, 2009). Water may, however, be important for kiang as evidenced by radial trails originating from a small spring

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Fig. 8.8 Kiang in summer congregate on moist sedge meadows in the lake and river basins in late summer that offer relatively higher green forage biomass (top panel photo—courtesy of Karma Sonam; bottom panel photo—courtesy of Abhishek Ghoshal)

and spreading over a small plateau frequented by kiang in eastern Ladakh (Bhatnagar, personal observation). In winter, low to medium snow cover can satisfy their need for water and allow them to use foraging habitat with greater flexibility (Payne et al., 2020). Heavy snowstorms or dzuds can, however, cause starvation related mortality as has been observed in all the three species (Kaczensky et al., 2011; Schaller, 1998; Schoenecker et al., 2016). The Przewalski’s horse and kulan

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Fig. 8.9 The frequency of extreme snow fall in winters (dzuds) is on the rise in many parts of Central Asia causing starvation related losses. Equids tend to move to areas with less snow such as windswept crests or areas with browse. Low to moderate amounts of snow can help them reduce dependence on watering points and allow foraging with greater flexibility (panel a, Przewalski’s horse, photo—courtesy of Tara Buk, Smithsonian National Zoo and Conservation Biology Institute; panel b, Persian onager, photo—courtesy of Amanda Carberry, Columbus Zoo and Aquarium; panel c, Kiang, photo—courtesy of Rigzen Dorjay)

do avoid deep snow by shifting latitudinally or vertically to areas with lower snow cover (Cao, unpubl. data). In windswept, open habitats it is extremely difficult for equids to find shelter; however, perhaps they may behaviourally avoid hypothermia by facing against the wind and tucking their bushy tail under their hind legs (Mejdell et al., 2020). Other morphological traits including hair coat, skin thickness, and subcutaneous fat also have been attributed to cold adaptation in various breeds of domestic horse (Mejdell et al., 2020). Strangely enough, clustering behaviour has not evolved nor has lying down on a hairy underside to avoid wind despite the fact that even on a steppe, wind shear reduces wind speed dramatically close to ground level. In resource rich areas kulan aggregates in large groups, a strategy that possibly helped with exposing forage through thin snow (Cao, unpubl. data), but even in these circumstances inter-animal distances are much larger than they are in musk oxen or wild bovids. This may mean that the thermoneutral zone of these cold-adapted animals is much wider than that of bovines (bison, yak, Asian buffalo, etc.) which evolved under tropical conditions (see Prins et al., in press). To our knowledge, except for the study on the Przewalski’s horse (Arnold et al., 2006), there is no information on thermo-physiological adaptations under field conditions or the role of hormones and adipose tissue mobilization in other cold-adapted equids (i.e., kiang, kulan, and the Yakut and Alaskan horse), but we believe that this could be a fertile field of research. The three cold-adapted equids have adapted to utilize the relatively low amounts of seasonally available and dispersed forage, under conditions of extreme cold and aridity, thus perhaps filling among the most harsh and extreme niches inhabited by terrestrial large mammals (Fig. 8.9).

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Physiological Basis of Cold Adaptation Equids are homeothermic (warm-blooded) animals that maintain their core body temperature within a narrow limit even when the environmental temperature varies extensively (Sneddon, Chap. 9). They achieve this via endothermy (heat produced by the body). Endothermic animals maintain body temperature (Tb) constant by altering their metabolic heat production. When the ambient temperature (Ta) falls below Tb, the temperature gradient (ΔT = Tb – Ta) triggers mechanisms to increase heat production, decrease the rate of heat loss, or permit the core body temperature to drop below “normal” (Tattersall et al., 2012). When animals can maintain a stable core body temperature, using only physiological regulatory mechanisms, this is described as their thermoneutral zone (Autio, 2008; Rubner, 1982; Sjaastad et al., 2016a, 2016b). The lower end of the thermoneutral zone is referred to as the lower critical temperature (LCT; Autio et al., 2008; Mejdell et al., 2020). In ad libitum fed and cold-adapted yearling quarter and quarter horse crosses the LCT is –15 °C (Cymbaluk & Christison, 1989). When the ambient temperature drops below LCT, animals need to generate more body heat and conserve it via a reduction in body temperature and respiratory rate. In domestic horses, managed in cold environments, animals are provided with supplemental feed to meet the increased caloric needs. However, wild equids, living in extreme cold environments, may experience limited food availability further decreasing their ability to increase body heat and/or metabolic rate. Interestingly, Yakutian horses withstand temperature fluctuations between +38 and –70 °C, do not require additional shelter, and can graze on vegetation deep under snow cover (Librado et al., 2015). In domestic European breeds of horses and other mammals, under these circumstances, other physiological and anatomical characteristics may play a role in temperature regulation. A transient increase in heat production is achieved by inducing shivering (defined as uncoordinated or nonsynchronous contraction of skeletal muscles). Skeletal muscles generate heat via aerobic mechanisms which results in rapid heat production. Equids also increase body (surface) heat via piloerection (erection of the hair of the skin due to contraction of the tiny arrectores pilorum muscles that elevate the hair follicles above the rest of the skin and move the hair vertically). Furthermore, they allow the temperatures in the extremities (lower legs), ears, and muzzle to decrease to minimize surface heat loss. Increases in body heat is also accomplished via an increase in metabolism. Amongst wild equids, most information is available in the Przewalski’s horse (Arnold et al., 2006). Studies suggest that animals adapt to changing environmental/seasonal condition by altering their metabolic rate. Specifically, during winter months, Przewalski’s horse lower their heart rate, decrease locomotion, and exhibit significantly lower peripheral body temperatures leading to an overall reduction in energy requirements. However, there is a knowledge gap as to the physiological mechanisms involved in cold adaptation in kulans, kiangs, and Yakutian horses that warrants additional research. Alternatively, heat production can be increased by breakdown of fat reserves (converting triglycerides to free fatty acids) also referred to as the non-shivering

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thermogenesis (Jastroch et al., 2018). These mechanisms are controlled by catecholamines and the sympathetic nervous system. The primary target of this mechanism is the brown adipose tissue. Heat production occurs within fat cells and these deposits are highly vascularized with high concentrations of mitochondria. The heat generated is rapidly distributed throughout the body, via the blood stream, to increase core body temperature. Utilization of brown adipose tissue is catalyzed by the mitochondrial uncoupling protein, UCP 1 (Jastroch et al., 2018). UCP1 is almost exclusively expressed in the brown/beige fat tissues. Although brown adipose tissue is present in equids and is considered to play a role in non-shivering thermogenesis, the UCP1 gene is inactivated via conversion into a pseudogene even in cold-adapted domestic equids (Gaudry & Campbell, 2017; Jastroch et al., 2018). Further this inactivation in ancestral equids is estimated to have occurred ca. 20–25 million years ago. However, other UCP proteins (UCP 2, UCP 3) have been described and their role in equid brown adipose tissue utilization remains poorly understood. In the mouse and humans, UCP2 is expressed in brown adipose tissue in addition to several other tissue types and is considered to be involved in fatty acid metabolism and in turn, thermogenesis (Ricquier, 1999). Likewise, although little is known about the expression patterns of UCP 3 in equids, this mitochondrial protein is mostly expressed in skeletal muscles of humans and rodents as well as in the heart and brown fat, at least in rodents (Ricquier, 1999). These findings warrant additional studies in equids.

Equids Also Utilize Additional Metabolic Mechanisms to Regulate Body Heat Specifically, animals can reduce their metabolic rate during winter, lower the heart rate, and lower thyroid hormone T3 levels with a concomitant increase in T4 (Brinkmann et al., 2016). Studies conducted in the Przewalski’s horse examined various factors influencing the metabolic rate in the context of changes in heart rate including thermoregulation, locomotor activity (LA), and heat increment of feeding (HI) (Arnold et al., 2006). During winter months, heart rate decreased to almost half the value (ca. 44 beats per min) of that during summer months (ca. 89 beats per min). Locomotor activity also decreased in winter, and the mean subcutaneous temperature declined to reach the lowest values in April. Results suggest that regulation of energy expenditure is not influenced by energy intake, but that animals appear to respond to diurnal changes which influence circulating hormone levels (e.g., T3 and other hormones that regulate metabolism) resulting in lower energy demands during winter. Although, in most species, thermoregulation is facilitated by peripheral vasoconstriction which in turn lowers the surface temperature and causes a decrease in heat loss from the body, Przewalski’s horses reduce their endogenous heat production by lowering the core body temperature with a concomitant decrease in skin surface temperature (Arnold et al., 2006). Furthermore, Przewalski’s horses decrease their food intake during winter and mobilize body fat for energy and heat

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production. Like Shetland ponies, the Przewalski’s horse also exhibits hypometabolism resulting in reduced energy needs (Brinkmann et al., 2012).

Morphological Adaptation to Cold Cold-adapted species often have numerous morphological characteristics that appear to be adaptations to cold environments including large body size, increased hair length, height, and higher subcutaneous body fat deposition/distribution. Extensive studies on cold adaptation have been conducted on Arctic species of mammals and birds, but studies are limited in wild equids (Feist & White, 1989; Scholander et al., 1950). Early studies showed an almost linear relationship between the basal heat production and body surface area, estimated using the Meeh’s formula (Scholander et al., 1950). Although several arguments have been presented in favour of the role of surface to volume ratio in thermoregulation, Steegmann (2007) stated that mass and not surface area influences cold adaptation in humans. Interestingly, analysis of inter-breed variation in the horse suggests that larger animals have an advantage over smaller animals since heat production is proportional to volume and heat loss is proportional to surface area (Langlois, 1994). This phenomenon is called the Bergmann’s rule. However, Meiri and Dayan (2003) reported that only 65% of mammal species evaluated adhered to this rule and more research is warranted in cold-adapted mammals, especially wild equids. Alternatively, animals may limit the ratio of surface area to volume by assuming a more spherical form, also referred to as Allen’s rule which hypothesizes that in response to cold species will evolve shorter limbs, tail, ears, and/or wings. In the context of equids, most cold-adapted equids tend to be stocky with shorter limbs (e.g., Yakutian horse, Icelandic pony, Przewalski’s horse). The latter adaptation also limits heat loss from the leg by minimizing the exposure of blood vessels to ambient temperature (Fig. 8.10).

Thermal Insulation Animals also combat cold induced heat loss by thermal insulation. This involves vasoconstriction of the peripheral blood vessels, resulting in the diversion of warm blood from the cooler surface to the warmer core. This results in equilibration of surface temperature with ambient temperature to complement the insulation provided by the subcutaneous adipose tissue, skin, and hair (Langlois, 1994). In the Plateau pika (Ochotona curzoniae), chronic exposure to cold leads to browning of subcutaneous white adipose tissue fat and a concomitant increase in the amount of brown adipose tissue in order to increase thermogenesis (Li et al., 2018). It is plausible that the cold-adapted equids also may express similar changes and warrants additional research. Most wild equids also grow a thicker undercoat and longer outer coat during the autumn. For example, the Przewalski’s horse grows a winter coat

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Fig. 8.10 Przewalski’s horse (a, b) and Persian onager (c, d) exhibit pronounced morphological adaptation (thicker coat) during summer (a, c) and winter (b, d) (Przewalski’s horse, photos (a, b)— courtesy of Smithsonian National Zoological Park and Conservation Biology Institute; Persian onager, photos—courtesy of Columbus Zoo and Aquarium (c) and Smithsonian National Zoological Park and Conservation Biology Institute (d))

annually to combat extreme cold. Interestingly, the Persian onager also grows a dense coat and does not exhibit extensive hair shedding with warming temperatures. Brinkmann et al. (2018) reported that, to support this hair growth, animals may require additional dietary protein. When a herd of Shetland ponies were maintained on a restricted diet, those in the treatment group exhibited limited hair growth compared to animals on a more nutritious control diet. The latter were able to grow their hair longer which increased their ability to protect from extreme cold. Under food restricted conditions, animals also metabolize more subcutaneous fat to generate the necessary body heat. A comparison of coats of horses, donkey, and mules demonstrates that while donkeys’ hair coat shows no seasonal changes, horses grow thicker hair during winter (Osthaus et al., 2018); the donkey is, of course, a North African species that is adapted to very hot circumstances. However, when hair width was analysed, mules had the thickest hair followed by the horse and then the donkey, suggesting that horses and mules have a greater ability to withstand extreme cold. It is not known yet how the genetics of hybridization of horse with donkey would lead to thick hairs. Horses with thicker coats can tolerate extreme cold. A thicker coat traps the body warmth and helps keep the skin temperature warmer than the environment. However, when exposed to rain, it leads to matting of the coat, and as a result the coat is

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no longer able to trap the warmth. Jørgensen et al. (2016) studied the shelter preference of horses exposed to Nordic winter conditions. Interestingly, although cold-adapted horses prefer to spend time outdoors, when exposed to wet conditions, these horses choose to seek shelter and spend more time indoor. This may support our conclusion that caballoid horses are dry-cold adapted species (c.f., Fig. 8.2).

Heat Loss in Wild Equids Heat loss is correlated with body size. A larger horse innately has a smaller surface area to dissipate heat compared to a similarly built smaller horse (Mejdall et al., 2020). Equids typically dissipate heat via their skin but there is limited information on what parts of the body are involved in this heat loss. Thermal imaging is currently used in animal health diagnostics, especially in animals afflicted with joint disorders and for evaluating animal performance during exercise (Cilulko et al., 2013). Further, the radiant energy measured is a manifestation of both the internal body heat and the thermal properties of the skin, coat, and the temperature gradient between the skin surface and the environment. Interestingly, these measurements also permit the analysis of muscle groups typically involved in heat production or dissipation. Recently, Domino et al. (2020) used infrared thermal imaging to compare the surface thermal patterns of horses and donkeys exposed to identical environmental conditions. This approach allows the detection of radiant heat which is converted into a thermogram wherein the colour gradient corresponds to the temperature gradient (Fig. 8.11). These authors report that, under similar environmental conditions (20.2 °C), horses exhibit higher surface temperature (ca. 22.7 ° C) as compared with donkeys (ca. 18.8 °C) and attributed the differences in the thermal properties of the skin and the coat between the horse and donkeys. Specifically, donkeys had a thicker skin, more subcutaneous fat, and a longer hair coat leading to better thermal insulation than in the horse. Thermal imaging of Przewalski’s horse and Persian onagers exposed to extreme cold environments reveals that both species have thermal signatures around the eyes and head, and lower surface temperatures on the other parts of their body (Fig. 8.11). Surface temperatures along the side of the muzzle, face, withers, and posterior gluteal muscles were generally warmer, overall, for the Przewalski’s horse than for the Persian onager. For Persian onagers, the limbs appeared cooler, in these extreme cold conditions, when compared with Przewalski’s horses. These findings suggest that, similar to donkeys, the Persian onager may have better insulation, and possibly a more efficient counter current exchange system in the limbs, than do horses, making them more cold tolerant.

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Fig. 8.11 Infrared thermal imaging of the Przewalski’s horse (panel a) and the Persian onager (panel b). Thermal images are global emissivity patterns of a target object displayed as a temperature gradient (colour spectrum). Hotter areas appear red or white (when the temperature exceeds the set threshold high limit). Colder areas appear purple or blue (lowest temperature measured). All images were captured when the ambient temperature (value shown on the bottom right corner of the image) was between –7.8 and –7.5 °C. The temperature indicated on the top left corner of the image corresponds to the temperature recorded at the location of the cursor. The colour scale depicted on the right side of all images represents a heat map corresponding to the temperature gradient depicted in the image. As shown in the images, both Przewalski’s horse and Persian onagers lose the most body heat in the region of their eyes and muzzle (white) while the limbs appear to lose the least amount of heat (as depicted by the blue colour) (photos—courtesy of Priya Bapodra)

Genetics of Cold Adaptation The Przewalski’s horse, Persian onager, and kiang are well adapted to cold environments, as are several breeds of domesticated equids occurring in such environments. As mentioned earlier in the chapter, all three species occur in latitudes/altitudes that experience extreme climatic conditions. All three species exhibit morphological adaptations critical for survival in extreme cold, including being exceptionally hairy (grow a dense winter coat), are compact, and have short limbs (Librado et al., 2015). Although some genetic data resources are available for the Przewalski’s horse, Persian onager, and the kiangs, no systematic studies have been conducted to reveal the genetic basis underlying cold adaptation. Most information available today is gleaned from studies conducted on the Yakutian horse (Librado et al., 2015). They can withstand ambient temperatures below –70 °C and prefer to stay outdoor even under extreme weather conditions. Since a significant portion of the

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year the ground is covered in several feet of snow, Yakutian horses often forage by digging for vegetation buried under snow. In a comparative analysis involving Yakutian horses, two ancient specimens (from early nineteenth century), two Late Pleistocene specimens, several domestic horses, and three wild Przewalski’s horses, genetic adaptation to cold appeared to be controlled by modification of non-coding and protein coding sites as well as gene duplication, suggesting the Yakutian horses are well suited for fast adaptive processes (Librado et al., 2015). Specifically, regions upstream of the translation start sites (TSS) revealed significant enrichment of adaptive candidates. Modifications were within the most proximal kilobase upstream from the TSS where regulatory gene elements are often localized. Candidate genes involved those that regulate hair density, subcutaneous fat accumulation, and relatively small surface area relative to body mass, all of which also minimize heat loss. Other genes involved include transglutaminase 3 (TGM3) whose loss of function in mice results in impaired and thinner hair (John et al., 2012), thyroid hormone receptor-associated gene (THRAP3) which interacts with adrenoreceptor α1B that regulates the vasoconstriction/vasodilatation reflex following cold exposure. Enrichment for hypothyroidism, endocrine system diseases, and type 1 diabetes mellitus also were observed. The latter was interpreted to reflect an adaptation to regulating glycaemia (glucose production to exert anti-freezing effects). Yakutian horses also exhibit adaptation in the protein coding sites; about 130 genes, enriched for number of pathways, including galactose, starch, and sucrose metabolism and diseases like Nelson’s syndrome which leads to an excess of adrenocorticotropic hormone. Furthermore, Yakutian horses also exhibit gene duplication that support cold adaptation; genes affected were enriched for several biological pathways including steroid hormone biosynthesis, fatty acid metabolism, metabolic pathways, and olfactory transduction. Genes associated with abnormality of temperature regulation (ACADSB, ATP1A2, CYP11B2, and HSPG2) also were enriched suggesting the Yakutian horses have evolved several mechanisms that support survival in subarctic climate. A recent study evaluated genes related to cold adaptation in Arctic or Antarctic environments in the human, Arctic fox, Yakut horse, mammoth, polar bear, and minke whale (Yudin et al., 2017). Although no cold-adaptive genes were conserved in all six species, several general mechanisms and biochemical pathways involved in reorganization of the cardiovascular function, thickness and strength of the skin, increased heat production, improved immunity, and behavioural changes were identified (Yudin et al., 2017). However, additional studies are warranted in wild equids to identify specific genetic signatures for cold adaptation.

Conservation Implications The three extant, cold-adapted equids face several threats across their wide range (Moehlman et al., 2016), however, here, we focus primarily on their possible responses to the changing climate, which is likely to result in global warming,

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climatic uncertainties, and increased extreme weather events (IPCC, 2021). Climate change can impact the very basis of survival—that is, food (Wu et al., 2017), water, and shelter, and could be very challenging for these equids. In fact, the vast declines in the historical range of equids (Orlando, 2015) may be due to a combination of climatic and anthropogenic causes (Bouman & Bouman, 1994; Buuveibaatar et al., 2016). It is, therefore, a matter of significant conservation concern as to what could happen as a result of more rapid climatic and land use changes. Overall, equids inhabiting extreme cold environments, appear to be well adapted to survive under these conditions. They also appear to tolerate a fairly large range of temperature and precipitation (Fig. 8.4), that may enable them to cushion the largely unknown changes in resources brought about by a changing climate. Despite this evolutionary advantage, it is likely that only species that are able either to, maintain core body temperatures near normal, or migrate to warmer areas, could still survive. In the absence of a similar adaptive behaviour, many species of wild equids could perish, as was previously reported in the reintroduced populations of Przewalski’s horse in Mongolia (Kaczensky et al., 2011). It remains unclear how the projected global warming trends (IPCC, 2021), with the related uncertainties, changes in habitats and increased extreme events, will impact the distribution and survival of wild equids. It is also possible that climate extremes may challenge the ability of animals to adapt quickly. Therefore, it will be important that large-scale conservation efforts designate large areas of the extant habitats, including areas that might become future refuges for conservation of equid species. The seasonally abundant forage in the equid range in Central Asia/Tibetan Plateau regions also attracts pastoralists who have livestock that often intensively graze the rangelands, resulting in competitive exclusion of many wild herbivores (Berger et al., 2013). This impact of humans and their livestock contributed to the decimation and extinction of the Przewalski’s horse in the nineteenth century (Bouman & Bouman, 1994). Competition between livestock and wild equids is already a growing issue of concern and may impact the survival of the latter by both interference and exploitative competition, as can be seen for the Przewalski’s and domestic horses in the Dzungarian Gobi during winter (Šturm et al., 2017), and reduced kiang abundance in high livestock density areas in Ladakh (Bhatnagar & Wangchuk, 2002). Using stable isotope studies, Kaczensky et al. (2017) showed that pre-extinction populations of Przewalski’s horses in Mongolia that were sympatric with domestic horses relied on browsing in winter but shifted to more suitable grazing in the reintroduced populations that were free of competition from domestic horses. Even though kiangs consumed barely 10% of available forage in eastern Ladakh (most of the rest being consumed by livestock) there is increasing consternation among nomads and officials that the kiang is competing for forage with the valuable cashmere goats (Bhatnagar et al., 2006). The combined effects of shifting climate niche and food resources (under the Representative Concentration Pathway 2.6) are likely to reduce suitable habitat for kiang on the Tibetan plateau by about 30% while also reducing preferred forage by over 7% (Wu et al., 2017). In much of their range, because of being outcompeted by livestock, kulan will need to increase the amount of browse in the diet (Šturm et al., 2017, 2021; Xu et al., 2012), which

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Fig. 8.12 Most people inhabiting equid range are pastoralists and their flocks may compete with wild equids (photo—courtesy of Yash Veer Bhatnagar).

can be a challenge for equids due to the higher presence of phenolic compounds in this food source (Duncan, 1992) (Fig. 8.12). The availability of water impacts pastures that can be utilized by equids (Nandintsetseg et al., 2016; Schoenecker et al., 2016). In fact, the most water tolerant of the three species, kulan, can use pastures about 20 km from water sources, and their long-range movements were governed by water availability rather than by the distribution of preferred habitats (Nandintsetseg et al., 2016). With light snow as a source of water in winter, kulan (and possibly other equids) can use pastures farther from water sources (Payne et al., 2020). However, heavy snow can make it difficult to access forage and prolonged deep snow can lead to heavy mortality of these ungulates (Schaller, 1998). Climate change may result in higher unpredictability in precipitation in some areas and years, that may cause corresponding uncertainties in habitat availability and the need for long-distance and frequent movements. Since Przewalski’s horses are often restricted to the small ranges where they were introduced, changing climate could limit their ability to migrate to ideal environments, hence they may not be able to adapt quickly to rapid changes (Kaczensky et al., 2011). This could affect the survival probability of this species. There is also a need to evaluate potential translocation and reintroduction sites for availability of food especially during extreme winters, and for water year-round.

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In some areas, such as the Gobi, Przewalski’s horses could thrive due to a greater tolerance by the herders who pride their lifestyle coexisting with the high-profile reintroduced species (Kaczensky et al., 2017). This underscores the importance of working closely with stakeholders to improve their perceptions as a means of conservation of the equids. With reference to the Przewalski’s horse, Kaczensky et al. (2017) also highlight the need for disaster planning by local herders, multiple reintroduction sites with spatially dispersed populations for reintroduced Przewalski’s horses, and a landscape-level approach beyond protected area boundaries to allow for migratory movements of Asiatic wild equids. This will need greater political will, resources, and integrated planning and implementation at landscape scales. The monodactyl equids have faced millions of years of competition with tridactyl equids and other herbivores to finally establish in the newly formed open habitats that expanded during the Pleistocene. However, climate and anthropogenic pressures, over the past 2 million years, have caused severe declines in their range, diversity, and abundance, but the recent declines have been the most dramatic. Without evidence-informed interventions, increasing pressure on the mountainous grasslands, deserts, and steppes from, e.g., livestock, mining, infrastructure, compounded by uncertainties of forage, water, and other resource availability due to the accelerated climate warming, could result in further declines of this amazing taxa of cold-adapted equids.

Perspectives As described in this chapter, our current understanding of cold adaptation in wild equids is derived from a small number of studies on the domestic horse and donkey. Most information on physiological adaptation to cold is extrapolated from systematic studies on domestic equids that have been studied in temperate conditions. It is, therefore, imperative to address this knowledge gap in all species of cold-adapted wild equids. Specifically, questions need to be addressed, such as are physiological mechanisms reported in domestic equids that permit adaptation to extreme cold environments conserved in their wild counterparts? Furthermore, with the availability of high-quality genome assemblies for several equids, studies also are warranted to identify the genomic/genetic basis of cold adaptation.

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Vincent, E., & Berger, W. H. (1985). Carbon dioxide and polar cooling in the Miocene: the Monterey hypothesis. In E. T. Sundquist & W. S. Broecker (Eds.), The carbon cycle and atmospheric CO2: Natural variations Archean to present (Vol. 32, pp. 455–468). American Geophysical Union. Wakefield, S., Knowles, J., Zimmermann, W., et al. (2002). Status and action plan for the Przewalski’s horse (Equus ferus przewalskii). In Equids: Zebras, asses and horses (pp. 82–92). Wang, H., He, Z. Q., Wang, H., & Niu, Y. X. (2012). Study on survival status of reintroduced Equus przewalskii in Dunhuang West Lake National Nature Reserve. Journal of Gansu Forestry Science and Technolgy, 37, 45–46, 65. Weinstock, J., Willerslev, E., Sher, A., Tong, W., Ho, S. Y. W., Rubenstein, D., Storer, J., Burns, J., Martin, L., Bravi, C., Prieto, A., Froese, D., Scott, E., Xulong, L., & Cooper, A. (2005). Evolution, systematics, and phylogeography of Pleistocene horses in the New World: a molecular perspective. PLoS Biology, 3(8), e241. White, M. A., Thornton, P. E., & Running, S. W. (1997). A continental phenology model for monitoring vegetation. Global Biogeochemical Cycles, 11(2), 217–234. https://doi.org/10.1029/ 97GB00330 Williams, S. D. (2002). Status and action plan for the Grevyís Zebra (Equus Grevyi). In Equids zebras asses horses status survey and conservation action plan (pp. 11–27). Wu, X., Dong, S., Liu, S., Su, X., Han, Y., Shi, J., Zhang, Y., Zhao, Z., Sha, W., Zhang, X., Gao, F., & Xu, D. (2017). Predicting the shift of threatened ungulates’ habitats with climate change in Altun Mountain National Nature Reserve of the Northwestern Qinghai-Tibetan Plateau. Climatic Change, 142, 331–344. Xu, W., Xia, C., Yang, W., Blank, D. A., Qiao, J., & Liu, W. (2012). Seasonal diet of Khulan (Equidae) in Northern Xinjiang, China. Italian Journal Of Zoology, 79, 92–99. Yang, S. X., Deng, C. L., Zhu, R. X., et al. (2020). The Paleolithic in the Nihewan Basin, China: Evolutionary history of an early to late Pleistocene record in Eastern Asia. Evolutionary Anthropology Issues, News, and Reviews, 29, 125–142. https://doi.org/10.1002/evan.21813 Yokoyama, Y., Lambeck, K., De Deckker, P., Johnston, P., & Fifield, L. K. (2000). Timing of the Last Glacial Maximum from observed sea-level minima. Nature, 406(6797), 713–716. Yudin, N. S., Larkin, D. M., & Ignatieva, E. V. (2017). A compendium and functional characterization of mammalian genes involved in adaptation to Arctic or Antarctic environments. BMC Genetics, 18, 33–43. Zhang, Y., Cao, Q. S., Rubenstein, D. I., Zang, S., Songer, M., Leimgruber, P., Chu, H., Cao, J., Li, K., & Hu, D. (2015). Water use patterns of sympatric Przewalski’s horse and khulan: Interspecific comparison reveals niche differences. PLoS One, 10, e0132094. Zhang, R., Zhang, T., Kelgenbayev, N., et al. (2017). A 189-year tree-ring record of drought for the Dzungarian Alatau, Arid Central Asia. Journal of Asian Earth Sciences, 148, 305–314. Zhang, X. C., Shao, C., Ge, Y., Chen, C., Xu, W.-X., & Yang, W.-K. (2020). Suitable summer habitat of the khulan in the Mt. Kalamaili Ungulate Nature Reserve and estimation of its population. Ying Yong Sheng Tai Xue Bao, 31, 2993–3004. https://doi.org/10.13287/j. 1001-9332.202009.032 Zimov, S. A., Zimov, N. S., Tikhonov, A. N., & Chapin, F. S. I. I. (2012). Mammoth steppe: a highproductivity phenomenon. Quaternary Science Reviews, 57, 26–45.

Chapter 9

Adaptations to Hot Environments Jennifer Sneddon

Abstract In this chapter, I focus on on Arab-based horses and other species of aridadapted equids. The chapter is based on my doctoral dissertation ‘Water homeostasis in desert dwelling horses’. I defended my thesis more than twenty-five years ago, and yet most of the basic physiological information in it still reflects the current level of scientific insight on this aspect of equid physiology. Few further physiological discoveries have been made, but there has been some progress, for example, aquaporin channels, specifically adapted for water transport in organs, were discovered in the early 1990s. Technological breakthroughs in bio-logging, over the last 20 years, have allowed scientists to move the lab into the animal in order to measure seasonal physiological responses to aridity. To assess to ‘what potential their physiological plasticity might have to contribute to success in future niches to be occupied by species’ (Fuller et al., Physiology, 29, 159–167, 2014), I split this chapter into three sections: (1) Behavioural and physiological responses to dehydration in equids; (2) The role of the hindgut as a fluid reservoir during dehydration; and (3) The sweating capacity of equids within the context of their small surface area relative to their volume, and what studies on the pathological condition of equid anhidrosis can reveal.

Box 9.1 Lack of research on horses from an ecological perspective Scientific approaches to equine energetics, specifically in veterinary agricultural contexts, blossomed in the 1930s, only to be interrupted by World War 2 when the displacing force of mechanisation became established. Equine Sports Physiology began as a serious discipline in the 1970s, but this field had (continued) J. Sneddon (✉) School of Biological and Environmental Sciences, Liverpool John Moores University, James Parsons Building, Merseyside, UK e-mail: [email protected] © The Author(s), under exclusive license to Springer Nature Switzerland AG 2023 H. H. T. Prins, I. J. Gordon (eds.), The Equids, Fascinating Life Sciences, https://doi.org/10.1007/978-3-031-27144-1_9

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Box 9.1 (continued) a strict remit and was largely confined to Thoroughbred racehorses. Today the million strong population of sport and leisure horses in Great Britain, for example, is approximately equal to the equine population in 1900 when the horse was the main source of power. Similarly high numbers occur in France or Germany. There is still comparatively little work on how the equine functions as an ecological entity. Physiological knowledge on horses and other equines, from genome to whole animal, is the next frontier in equine studies. The influence of season on metabolic rate has long been established in ruminants and yet was only first established in Welsh Mountain ponies in 2001 and Shetland ponies in 2014 (Fuller et al., 2001; Brinkmann et al., 2014).

Behavioural and Physiological Responses to Dehydration in Arid-Adapted Equids When I did the field work for my PhD in 1989–1993 (Fig. 9.1), the feral horses (Equus caballus) of the Namib desert represented an unique group in which to study mild (12%) dehydration (percentage dehydration is expressed as body fluid loss (kg) as percentage of body mass (kg)) in horses; they had been feral in the desert for 75 years, since the end of the first World War (Sneddon et al., 1991; Van der Merwe, 1981); (see Figs. 9.2 and 9.3). These horses were descended from those of a stud farm for breeding military horses, established by Baron Von Wolf of Duwisib Castle in German South West Africa (now Namibia), in the first decade of the twentieth century (Fig. 9.2). The horses became feral after WW1 and were subsequently de facto protected by inhabiting a forbidden area that was home to diamond mines, the so-named Spergebiet. There was a watering point for steam locomotives in the area (Fig. 9.1) (Van der Merwe, 1981). The first adaptations to hot envirnonments noticed by an observer are behavioural. The Namib horses frequented an area of up to 42 km from a single watering point (Fig. 9.1) around a single permanent watering hole, and their behaviour suggested that they had become desert-adapted like other wildlife in the area (primarily African oryx or gemsbok (Oryx gazella)), and drank about once in every three days. They could graze up to 42 km away from the permanent watering point. Similar watering behaviour has been observed in feral Australian horses using GPS technology (Hampson et al., 2010) and Przewalski’s horses (E. ferus przewalskii) released in the Taklamakan Desert of NW China (pers. comm. Qing Cao). Like these successful feral horses in Namibia and Australia, Burchell’s zebra (E. burchellii, a.k.a. Plains zebra a.k.a. E. quagga) is dependent on perpetual water sources (Klingel, 1969). Behaviour, allowing learned access to water, has been observed in onagers (Equus hemionus) accessing underground water by digging 1 m deep holes (Nazeri

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Fig. 9.1 Namib horse drinking at the permanent watering point in Namib Naukluft National Park ‘Wild Horses and Gemsbok’ by D-Stanley. Licensed under CC BY 2.0 (https://creativecommons. org/licenses/by/2.0/)

et al., 2015). The differences in drinking behaviour and water economy measured via bio-logging have been linked to potential survival in arid environments in Przewalski horses (Scheibe et al., 1998). It was speculated that these individual differences in water requirement, along with inter-generational knowledge about water resoures and quality of grazing areas, could provide a basis from which animals survive in arid wild environments (Scheibe et al., 1998). In arid environments, bio-loggers have been used on Gemsbok, (Boyers et al., 2019; Fuller et al., 2014), Alpine ibex (Capra ibex) (Mason et al., 2017), and African elephants (Loxodonta africana) (Wato et al., 2018; Thaker et al., 2019) to ascertain behaviours that promote survival, at coarse or fine landscape scales. These are: the selection of favourable microclimates; optimal foraging strategies incorporating intimate knowledge of watering points (Wato et al., 2018; Thaker et al., 2019) and, tolerance of wide swings in body temperature to economise on water loss (Boyers et al., 2019; Fuller et al., 2014) or control of body temperature within narrow limits by foraging at higher altitude on poorer quality forage thus compromising nutritional intake (Mason et al., 2017). Long-term bio-loggers placed in animals over seasonal timescales have revealed that, despite the lack of a carotid rete vessel protecting the brain tissue from hyperthermia, Plains zebra is capable of withstanding short intervals of

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Fig. 9.2 Mounted German military rider in the time period 1906–1918 South West Africa. Courtesy of Bundesarchiv, Bild 105-DSWA0132 / Photo: Walther Dobbertin/Licence CC-BYSA 3.0

Fig. 9.3 (a) Panoramic view of Namib horses in the Namib Naukluft National Park, Namibia (Source: Harald Süpfle, https://upload.wikimedia.org/wikipedia/commons/f/fd/Wildpferde_Aus. jpg; licensed under CC BY 2.5 (https://creativecommons.org/licenses/by/2.5/)). (b) Namib horses close-up view (Source: Gerald de Beer; https://upload.wikimedia.org/wikipedia/commons/2/2c/ NamWCp-246.jpg; licensed under CC BY 2.0 (https://creativecommons.org/licenses/by/2.0/))

high brain termperatures of 41°C during simulated predation events (Fuller et al., 2000). Is physiological adaptation more expensive, in energetic terms, than is behavioural adaptation? According to previous work on unglulates in arid environments, the answer is ‘yes, it is’. My view is that, although endotherms can recruit

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autonomic capacity to cope with environmental variations better than can ectotherms, endotherms are just as likely to alter behaviour when it is an option. Behavioural changes generally are less costly physiologically than are autonomic adjustments (Bartholomew, 1964) and discussed in Fuller et al., 2014). Desert ungulates, for example, use shade-seeking, nocturnally biased activity, and body orientation to reduce heat load in hot conditions. Does the lack of a carotid rete or a protective head boss limit thermoregulation of brain tissue? Zebra appears to prefer to be within a few kilometres of drinking water, perhaps because it displays a regular body temperature rhythm to within 2°C regardless of elevations in ambient temperature (Fuller et al., 2000; Mitchell et al., 2002; Fuller et al., 2014). This regular pattern in core body temperature, if not attained by evaporative water loss, must be the result of behavioural control mechanisms (Fuller et al., 2000). The stripped coat pattern of zebra has been shown to assist with thermoregulation, in tandem with deterring biting flies via a putative visual confusion mechanism (Cobb & Cobb, 2019) (Rubenstein, Chap. 12). Physiological control mechanisms applied in hot conditions include heat storage when dehydrated, often referred to in the literature as adaptive heterothermy (Mitchell et al., 2002). Adaptive heterothermy occurs on diurnal timescales as it addresses a failure to reconcile energy demands and water balance; heat stored during the day is radiated off at night (see Box 9.2). Reductions in body water turnover rate and feed intake when water and forage are scarce, over seasonal timescales, are also reported adaptations for reduced energy and water requirements in arid-adapted ungulates (Silanikove, 1994; Fuller et al., 2014) and, interestingly, at times of year when forage is scarce in northern latitudes (Fuller et al., 2001; Brinkmann et al., 2014). Reduced water turnover rate when dehydrated was observed in both the Namib and Boerperd horses from Gauteng, South Africa (Sneddon et al., 1991); see Table 9.1 and Fig. 9.4. This is not hibernation as such but a milder form of metabolic strategy for getting through hard times when resources are scarce. Moving on to further consideration of physiological adaptations to arid environments. Investigating mechanisms controlling water homeostasis in desert-adapted equids involves assessing a suite of physiological responses to dehydration. Hormonal control lies behind these physiological responses. Further genomic/epigenetic studies could assist our understanding about how the organ systems regulate this control in the face of environmental challenges (Dindot & Cohen, 2013; ChavattePalmer et al., 2018) . All there is at present are the studies that I conducted measuring clinical indices of dehydration and water turnover rate in Arab-based horses (Sneddon et al., 1991; Sneddon et al., 1993a, 1993b). The changes in standard clinical parameters used to indicate hydration status under a 12% body weight loss dehydration are displayed in Table 9.1. Previous work indicated that a period of 72 h of water withdrawal has no deleterious effects on horses in terms of wellbeing and yet produces significant physiological changes in terms of dehydration (Meyer et al., 1978; Carlson et al., 1979). Tasker (1966) dehydrated horses for 8 days with no deterioration in wellbeing other than a slight diarrhoea. There have been no studies published on dehydration and its effects on the different species of zebra, nor on kulan (a.k.a. onager, E. hemionus), kiang (E. kiang) or African wild ass (E. asinus).

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Table 9.1 Changes in standard physiological variables due to a 12% dehydration: a breed comparison between desert-adapted and control horse

Haematocrit (%) Total plasma protein g.l-1 Plasma sodium mM Plasma potassium mM Plasma osmolality mM.l-1 Body mass (kg % change) Total body water – Litres – ml.kg-1 body mass Isotope half-life (days) Body water turnover % body water pool – Litres.day-1 – ml.kg0.82.day-1

Namib horse (N = 6) +8.3 ± 3.5 +13.5 ± 4.0 +15.3 ± 2.3 -0.67 ± 0.58 +25.6 ± 6.1 -12.0 ± 1.22

Boerperd (N = 6) +6.7 ± 1.1 +15.1 ± 1.8 +13.0 ± 1.1 +0.38 ± 0.24 +21.5 ± 1.3 -12.0 ± 1.0

P-value (breeds) N.S. N.S. P ~ 0.05 N.S N.S. N.S.

-42.3 ± 3.5 -63.0 ± 12.7 +23.1 ± 14.5

-50.7 ± 6.7 -64.0 ± 7.4 +24.7 ± 20.9

P < 0.05 N.S. N.S.

-8.3 ± 2.3 -18.7 ± 3.2 -174 ± 29.6

-8.1 ± 2.0 -22.7 ± 3.4 -184 ± 23.3

N.S. P < 0.1 N.S.

Values are mean ± 95% CI. N.S. is not significant at 10%

Fig. 9.4 Boer General Koos de la Rey (1847–1914) on his Boerperd horse ‘Bokkie’. His nickname was ‘Leeuw van die Wes Transvaal’. Copyright-free image from public domain; photographer unknown

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These body mass losses, after dehydration, were not significantly different between the Namib and Boerperd horses. Boerperd are a local breed of farm horse. The Namib horses were significantly smaller as compared to the Boerperd (346 ± 22 vs. 411 ± 25 kg, respectively, 95% CI; P < 0.0001), and turned over 5 litres less water per day than did the Boerperd breed (Table 9.1). Increases in their plasma sodium were significantly higher than in the Boerperd horses (Table 9.1). I discovered that the Namib horses had no overt physiological control mechanisms for desert survival, pending a hormonal examination. Perhaps their smaller body size, and hence lower water turnover rate (Table 9.1), might assist with survival in a desert environment (Sneddon et al., 1991). The elevations in plasma sodium and osmolality—a driver of vasopressin activity and water turnover rates were close to significantly higher in the Namib horses. Were they showing similar physiological responses to other desert ungulates, in terms of more sensitive water turnover and hormonal responses to dehydration (Macfarlane et al., 1963; Macfarlane et al., 1971; Yagil & Etzion, 1979)? We shall see in subsequent sections. Box 9.2 The digestive strategy of hindgut fermentation, with continual food input over long daily grazing times, has allowed equids to reach a comparatively large body size and store sufficient water reserve for maintaining plasma volume and prevent cardiovascular shock at times of dehydration. If there is a water source within a couple of days walk—the Namib horses can survive. ‘As horses evolved into comparatively large ungulates, and as water is required for fermentation processes, and given that fibre has a high water-holding capacity, it is probable that physiological mechanisms linking the gut to water homeostasis evolved as these larger animals became adapted to function in the aridity of the plains ecosystem’ (Demment & Van Soest, 1985 discussed in Sneddon & Argenzio, 1998). The horses in my study in Southern Africa were all originally imported, and thus were all descended from European domestic stock. Would the wild populations of Equus caballus have survived without the process of domestication? Probably not. The steppe-grazing wild species of E. caballus were incorporated into the considerable genetic diversity of European domestic horse stock, predominantly from two Holocene steppe refugia; one on the Iberian Peninsula, and the other in the Eastern Steppe in the region of the Caspian Sea. There was a low level of diversity in breeds in the European gene pool from previously forested areas, consistent with dilution of their gene pool from steppe breeds (Warmuth et al., 2011). The steppes are an arid environment; the hindgut fluid pool of equines can help to maintain circulatory volume when access to water is restricted (Sneddon et al., 1993a). (continued)

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Box 9.2 (continued) The contribution of the fluid pool in the gut to the dehydration process: this is a parameter that is difficult to measure and monitor directly. Some basic physiological knowledge and a few sensible assumptions can come to the rescue. The size of the gut fluid pool contribution to the dehydration process can be estimated from the camel as follows (Sneddon et al., 1992): the assumptions are (a) sodium thiocyanate dye does not cross the gut barrier into circulation; (b) Evan’s blue dye remains in circulation bound to plasma albumin; (c) indicator dilution change in a given body fluid pool is due to water and not tissue loss over a comparatively short timescale; and (d) the proportion of extracellular fluid volume is 1/3 as compared to intracellular fluid volume, and their ratios are thus 1:2. Thus, if the extracellular fluid volume decreases by 14.5% (10 litres) with dehydration, the intracellular fluid volume decreases by 28% (20 litres). If, for example, the total body water fluid pool, determined by tritium dilution, drops by 20.5% (69 litres), then intracellular fluid volume + gut fluid volume = total body water – extracellular fluid volume, or (20 litres + gut pool contribution) = (69 litres – 10 litres). So, gut contribution was 39 litres or 56.5% of fluid to the dehydration process in this example. I also performed the same calculation to estimate the change in the equine gastrointestinal fluid pool during dehydration where bio-impedance was used to measure changes in the extracellular fluid and total body water pools (Lindinger, 2014). The technique was validated against the same indicators I used for monitoring body fluid pool volumes; details are given in Sneddon et al., 1993b. The gastrointestinal fluid volume changed by an estimated 23%. Yet, I have my doubts on the claims in this paper for non-invasive determination of intracellular fluid volume due to the electrical resistance of the lipid component of cell membranes. Indeed, their lack of success for direct non-invasive determination of changes in gut fluid volume, resulting from dehydration, was attributed to cell membrane resistance to electrical current (Lindinger, 2014). As far as I am aware, this technique is not in clinical use for monitoring hydration status in horses. The amount of fluid from evaporative fluid loss that a zebra can save by employing adaptive heterothermy can also be theoretically estimated: If a zebra has a mass of 250 kg, and lets its temperature increase, in the early morning, from, say, 35.5°C to sunset 40.5°C, then she has ‘stored’; 250 × 4 kCal = 1000 kCal = 4200 kJ that she did not have to lose through evaporative cooling and can dissipate this excess heat at night (H.H.T. Prins, pers. comm.).

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From Basic Indicators of Hydration Status to the Role of the the Hindgut in Equid Fluid Homeostasis and Hormonal Control Equids have a high input/high output digestive system with their digestive processes occuring in voluminous fermentation chambers (Fig. 9.5a, b) (see also Gordon & Prins Chap. 6). The precise role of the equid hindgut in maintaining plasma volume, and simultaneous hindgut fermentation, during dehydration activity remains largely

Fig. 9.5 (a, b). Schematic diagram of the gastrointestinal tract of a 164 kg Shetland pony showing sacculated large intestine. 19.4 litres or the extracellular fluid volume enters the large intestine each day, 95% of which is reabsorbed (Argenzio et al., 1974; Argenzio & Stevens, 1975; Sneddon & Argenzio, 1998). The large (ascending) colon is arranged in right and left ventral colons, and left and right dorsal colons, which terminate at the origin of the small colon. The arrow in (a) indicates the termination of the ascending colon. (c) Possible mechanism to explain absorption of un-dissociated short chain fatty acid (HAc) and its partial dependence on Na + absorption. From Sneddon & Argenzio, 1998. Courtesy of Elsevier Publishing

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unknown. Regrettably, not much progress has been made in this area since my published review from 1998 (Sneddon & Argenzio, 1998), but I did publish the result of an experiment on morphological changes to the hindgut mucosa in mildly (6%) dehydrated donkeys (Sneddon et al., 2006). Fermentation activity in the caecum and ventral colon was maintained in these dehydrated donkeys (Sneddon et al., 2006). These morphological changes in the gut and enhanced fluid retention, particularly in the caecum and ventral colon, collectively reflected enhanced fermentation activity in these gut regions after a 6% dehydration. The morphological changes in the hindgut chamber linings were observed using stereological methods (a powerful combination of histology and geometry that allows one to address otherwise impossible measurements on tissue) (see below). I found that the changes in gut structure took the form of increased gut mucosal and crypt surface area (and decreased tissue depth in mucosa and serosa) in all regions of the hindgut, and corresponded with the enhanced fermentative capacity, particularly in the caecum and ventral colon (Sneddon, 2010). The hindgut regulates cyclic co-reabsorption of ions, volatile fatty acids (energy precursors; see Gordon & Prins Chap. 6), and water from the large intestine (Fig. 9.5). The ionic composition and water content of the digesta are largely dependent on the rate of microbial fermentation, with sodium and water movement being closely correlated (Argenzio & Stevens, 1975; Sneddon & Argenzio, 1998). Hormonal control of these processes lies mainly with aldosterone and vasopressin. How was this discovered? Aldosterone is blocked by endogenous prostanoids and elevated plasma sodium concentrations, but when endogenous prostanoids are blocked, it promotes sodium and water reabsorption from the gut, and thereby nutrient reabsorption (Clarke & Argenzio, 1990; Clarke et al., 1992). In dehydrated, arid-adapted horses these responses are apparent; in response to dehydration in the Namib horses, I found that aldosterone activity was accompanied by positive changes in sodium concentration and negative changes in potassium concentration (Table 9.1). Likewise, vasopressin activity was accompanied by elevations in plasma sodium and osmolality in both Namib and Boerperd horses. Osmolality is the number of particles per unit volume plasma: mostly sodium and chloride and plasma proteins (see Fig. 9.6 and for more details (Sneddon et al., 1993a)). In Fig. 9.6a and b, I show that Namib horses had significantly higher (P < 0.001) values for plasma osmolality and vasopressin throughout the periods of dehydration and rehydration.This more sensitive vasopressin response has also been noted in other desert ungulates (Macfarlane et al., 1967). Plasma aldosterone, initially depressed by elevated sodium levels (Fig. 9.6c), increased between 48 and 72 h despite elevated plasma osmolality (sodium ions), when the supressive effects of sodium, and presumably endogenous prostanoids, were overridden by a need to supplement plasma volume by a supply of fluid from the hindgut (Sneddon et al., 1993a; Sneddon & Argenzio, 1998). In Fig. 9.6c, one can see that plasma aldosterone was released in a cyclical manner in the Namib horses which correlated with a rapid passage of water through the gastrointestinal wall as was shown by placing a marker (in the form of tritium-labelled water) in drinking water during rehydration (Fig. 9.6d). My interpretation is that this showed a more controlled release of fluid

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Fig. 9.6 Effects of dehydration and rehydration on two southern African horse races, viz., Namib horses and control Boerperd horses. (a) Plasma osmolality (mOsmol.l-1), (b) vasopressin, and (c) aldosterone concentrations (pg.ml-1) after dehydration (24 h intervals) and rehydration (10 minute intervals (5–10)) then 3, 6, and 24 h (11–13). Figure 9.6 (d) gives the rate of water passage through gut wall as measured with a marker (tritium-labelled water). Values are mean ± sem, N = 6. Dark symbols are Namib horses, open symbols are Boerperd horses (Sneddon et al., 1993a). Copyright granted by Elsevier Publishing

into the circulation by the Namib horses as compared with Boerperd horses, regulated under hormonal control (Sneddon et al., 1993a; Sneddon et al., 1993b). These patterns of fluid reabsorption from the gut are similar to those observed in desertadapted ruminants including camels (Camelus dromedarius) (Macfarlane et al., 1967; Finberg et al., 1978; Yagil & Etzion, 1979). In Table 9.2, I show that faecal moisture levels (%) altered by less than 10% with respect to pre-experimental (base) levels. This shows that controlled water release from the gut occurred throughout changes in hydration status (Sneddon et al., 1993a). There were no differences in faecal moisture content of the two horse breeds (Table 9.2). However, hydration status, not surprisingly, did significantly alter the moisture content of faeces as compared to pre-experimental (base) levels. It was interesting to note that the Namib horses recovered faecal moisture levels faster than did the Boerperd.

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Table 9.2 Faecal moisture content (% wet weight) during dehydration, immediate rehydration, and after 24 h rehydration across two horse breeds Treatment Base 24 h dehydration 48 h dehydration 72 h dehydration Rehydration 24 h rehydration

Namib horse (N = 6) 77.8 ± 2.7 73.0 ± 2.6 70.6 ± 2.1 70.4 ± 2.2 73.6 ± 2.4 74.0 ± 2.7

Boerperd (N = 6) 78.9 ± 2.2 71.9 ± 2.0 71.3 ± 1.8 69.7 ± 2.1 72.2 ± 2.9 74.0 ± 2.4

P-value (breed) ns ns ns ns ns ns

P-value (time Namib)

P-value (time Boerperd)

0.050 0.001 0.001 ns ns

0.001 0.001 0.001 0.001 0.001

Values are mean (95% CI) [data from Sneddon et al., 1993a)

Box 9.3 I have included several dense Tables & Figures of data to provide evidence to substantiate my observations on the responses of horses to dehydration Often one is looking for patterns or indications in the data with limited experimental numbers even though I was working in an environment where I could control the water and food intake of my experimental animals. However, I could not control behaviour. Behaviour of ungulates in arid environments, as I show earlier in this chapter, has a huge influence on adaptive physiology. Bio-logging was not available to me but has since revealed physiological plasticity—variation in physiological data that we did not know existed, e.g. the brain temperatures of galloping zebra (Fuller et al., 2000). Behavioural, and possibly physiological, data can now be analysed from enormous, robust datasets, and we are told that such sets obey the central limits theorem—they tend towards a normal distribution. Perhaps, the way forward is the relatively novel application of established statistical methods, like generalised linear models. These models can be distribution independent and yet have the advantage of incorporating all combinations of the effects of treatment on the dependent variable. The output from such models is more informative, and certainly more powerful, than the rigid distribution dependent ANOVA based methods used in my PhD. It is a truism that large animal research is hugely under-represented in the scientific literature due to the dual challenges of expense and licensing that apply in many countries. Recently South Africa (Fuller et al., 2000; Fuller et al., 2014), and not so recently Australia (Macfarlane et al., 1963; Macfarlane et al., 1967; Macfarlane et al., 1971) and Israel (Finberg et al., 1978; Yagil & Etzion, 1979), seem to be better off in this respect. Unsurprisingly, important revelations of the interaction between physiology and environment have been revealed from research groups from these parts of the world.

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Impact of Sudden Rehydration on Red Blood Cells of Dehydrated Horses Water is erratically available in arid environments and often has to be taken on in large volumes (Silanikove, 1994). What is the effect of this on the volume of the fluid pool in plasma? I used indices of red blood hydration status (see Table 9.3) to answer this question (Sneddon et al., 1992). Hydration status rather than breed had a greater effect on the red cell parameters described in Table 9.3. With small experimental numbers (viz., six horses of any breed), as is so often the case in expensive experiments with large animals, I was largely confined to looking for patterns in the data that reflected mechanisms for the control of water homeostasis in the intravascular fluid pool. The slightly higher values for red cell parameters in Namib horses derived from a higher baseline haemoglobin concentration, as explained in (Sneddon et al., 1992). The Namib horses displayed haemoconcentration up to 48 h dehydration followed by haemodilution between 48 and 72 h dehydration. This indicates fluid withdrawal into circulation from the hindgut pool to maintain plasma volume while also maintaining red cell integrity. The hydration status of the intravascular space did not threaten red cell integrity at any stage of dehydration or rehydration (Table 9.3), once more indicating controlled release of fluid from the gastrointestinal tract. Plasma osmolality was significantly higher in Namib horses than in Boerperd horses (Fig. 9.6), and as previously stated, this could have been linked to a more nuanced response in hormonal control of fluid from the hindgut in Namib horses as compared to in Boerperd horses, of which at least the modern version is not bred for performance under hot, tiring conditions. The osmotic changes in the plasma of Namib and Boerperd horses ranged between 278–309 mOsmol.l-1 (Sneddon et al., 1992), and were far removed from those which engendered a 50% lysis of red blood cells estimated from proportion of a 300 mOsmol.l-1 bufferred saline concentration (130–145 mOsmol.l-1,Table 9.3). The lowest plasma osmolality post rehydration was 278 mmol.l-1 (Sneddon et al., 1992). The saline concentration at which the red cells of these Arab-based horses lysed was similar to that reported for camels and Arab horses (reported in Sneddon et al., 1992). This implies that the horses in this study had red cells of a similar resilience to the erythrocytes of camels and other Arab-based horses when the cells were exposed to imposed sudden changes is hydration status. What about water and food intake? I measured water intake using a cheap but robust system designed so that the horses could not spill water from the bucket (Fig. 9.7) Sneddon & Colyn, 1991). Water intake (ml.kg-1) was not significantly different between Namib and Boerperd horses during normal hydration (48 ± 4, 44 ± 2, Namib and Boerperd, respectively), during immediate rehydration (117 ± 6.8, 107 ± 6.8, respectively), and at 24 hr. post rehydration (39 ± 3, 42 ± 2, respectively). Intake of hay was also normal at pre-dehydration levels up to 48 h dehydration but dropped by 45% between 48 and 73 h dehydration. Intake of

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Table 9.3 Change in red blood cell parameters in Namib and Boerperd horses with change in hydration status

Variable Red cell count 1012.l-1

Status Base 24 h dehydrated 48 h dehydrated 72 h dehydrated 24 h rehydrated Haematocrit % Base 24 h dehydrated 48 h dehydrated 72 h dehydrated 24 h rehydrated Base Haemoglobin concentration 24 h dehydrated g.dl-1 48 h dehydrated 72 h dehydrated 24 h rehydrated Mean cell vol- Base ume (fl) 24 h dehydrated 48 h dehydrated 72 h dehydrated 24 h rehydrated Base Mean cell haemoglobin 24 h dehydrated (pg) 48 h dehydrated 72 h dehydrated 24 h rehydrated Base Mean cell haemoglobin 24 h dehy concentration 48 h dehy % 72 h dehy 24 h rehy * F50 mmol.l-1 Base buffered saline 24 h dehydrated concentration 48 h dehydrated at which 50% 72 h dehydrated of red cells lyse 10 min rehydrated 24 h rehydrated

Namib 8.1 ± 0.5 9.1 ± 0.7 10.2 ± 2.0 9.1 ± 0.9 8.7 ± 0.9 36.3 ± 2.2 40.1 ± 2.2 42.3 ± 4.2 42.5 ± 6.1 41.0 ± 3.4 14.4 ± 0.4 16.4 ± 1.7 17.5 ± 2.2 16.6 ± 1.4 15.5 ± 1.7 44.3 ± 2.7 44.1 ± 2.7 43.8 ± 2.8 46.7 ± 4.7 47.5 ± 3.3 17.8 ± 1.0 18.0 ± 1.0 18.0 ± 1.3 18.2 ± 1.2 17.7 ± 0.7 39.6 ± 0.9 40.7 ± 1.0 41.2 ± 1.5 39.2 ± 2.2 37.4 ± 2.4 0.43 ± 0.02 0.43 ± 0.02 0.44 ± 0.01 0.45 ± 0.01 0.45 ± 0.02

P-value Boerperd (breed) 7.7 ± 0.5 NS 9.1 ± 1.2 NS 9.1 ± 1.3 NS 8.5 ± 0.9 NS 8.1 ± 0.7 NS 35.4 ± 0.6 P < 0.1 39.4 ± 2.4 NS 39.8 ± 3.2 P < 0.1 39.0 ± 2.5 P < 0.05 38.0 ± 2.7 P < 0.1 13.5 ± 0.4 NS 14.9 ± 2.1 NS 14.9 ± 2.3 NS 14.5 ± 1.6 NS 13.4 ± 1.7 NS 46.0 ± 3.6 NS 43.9 ± 4.6 NS 44.6 ± 4.1 NS 46.2 ± 2.2 NS 47.3 ± 4.4 NS 17.3 ± 1.3 P < 0.05 17.5 ± 1.4 NS 17.4 ± 0.7 P < 0.1 17.9 ± 0.7 NS 17.7 ± 1.2 NS 38.3 ± 1.0 NS 40.1 ± 1.4 NS 39.5 ± 1.5 NS 38.7 ± 0.9 NS 37.0 ± 2.1 NS 0.40 ± 0.04 NS 0.41 ± 0.04 0.41 ± 0.04 0.42 ± 0.04 0.42 ± 0.04

0.44 ± 0.03 0.40 ± 0.04

P-value (status Namib)

P-value (status Boerperd)

0.0051 0.0051 P < 0.01 NS

P < 0.01 P < 0.01 NS NS

P < 0.005 P < 0.05 P < 0.1 P < 0.05

P < 0.05 NS P < 0.1 NS

P < 0.05 P < 0.05 P < 0.05 P < 0.1

NS NS P < 0.05 NS

NS NS NS NS

NS P < 0.001 NS NS

NS NS NS NS

NS P < 0.05 NS NS

P < 0.1 P < 0.1 NS P < 0.1

P < 0.01 NS NS NS

NS NS P < 0.001 NS

NS NS NS NS

NS

NS

Values are mean with 95% CI; n = 6. * indicates a separate experiment, therefore, extra time sample. F50 data are expressed as a proportion of a 0.154 mmol.l-1 or 300 mOsmol.l-1 buffered saline concentration. The range of buffered saline concentrations used to estimate F50 was 0.9–0.3% (0.154 mmol.l-1 – 0.051 mmol.l-1) or 300–50 mOsmol.l-1 (Sneddon et al., 1992)

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Fig. 9.7 Water bucket fitted with two metal rods across the diameter of the bucket and a heavy-duty rubber gaiter around the outer edge. (Sneddon & Colyn, 1991). Photo credit: J. Sneddon

concentrates remained normal throughout all periods of dehydration and rehydration (Sneddon et al., 1992).

Aquaporins or Water Specific Channels in Organ Systems: A Discovery of the 1990s The gut is a relatively non-selective barrier to the reabsorption of fluids and nutrients into circulation, and fine-tuning the water balance of vertebrates is predominantly the role of the kidneys. In 2007, there was some basic work on aquaporin channel locations in relation to endocrinological control of kidney tubule reabsorption (Floyd et al., 2007). The aquaprorins are small membrane proteins (AQP proteins) which have a similar basic structure in whichever organism they are found, consisting of six transmembrane helical segments and two additional short helical segments surrounding cytoplasmic and extracellular vestibules, with a narrow pore running through the centre to allow the passage of small molecules such as water. Indeed, ‘Equid renal AQP proteins are likely to be involved in acute and chronic regulation of body fluid composition and may be implicated in water balance disorders brought about by colic and endotoxemia’ (Floyd et al., 2007). This indicated a role for their

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function in the hindgut although this has not been put to an experimental test, and not much is known yet. Indeed, the equid kidneys do not seem outstandingly adapted for arid environments in dehydrated desert donkeys (Maloiy, 1970).

Sweating Capacity in Horses: Are They Compromised by a Low body Surface Area? Horses have body surface area constraints for coping with heat loss. The ratio of surface area to volume (expressed as m2 per kg body mass) is 1:35–40 in humans and 1:90 in horses (Hodgson et al., 1993). In other words, the skin surface of horses is relatively two to three times smaller than in humans. Both surface area and sweating anatomy are associated with heat loss and are larger by proportion in Arab-based horses (Sneddon et al., 2004). In Fig. 9.8, using sponges of known square dimension dipped in talcum powder to dab the body surface, some of my students and I showed, for example, that the relative area of the hind legs, fore legs, and head is larger in Welsh (Arab-based) ponies than in native British breeds. This implies a greater area for heat loss, particularly in the thermal window area of the upper hind limb, in these Arab-based ponies. The respiratory tract is an important site of heat loss in equids, together with the thermal windows in the upper hind and fore limb areas. These thermal windows are the sites of arterio-venous anastomoses that direct blood supplies to the skin in preparation for heat loss (Wilson et al., 2007). Sweating capacity is five times higher

Fig. 9.8 Mean regional surface area as a percentage of total body surface area (BSA) for a number of horse breeds (Section A – Welsh Mountain Section A ponies; WMP type – Welsh Mountain-type ponies; H – Hanoverians). Bars indicate standard error of the mean; histograms with differing letters (a, b, or c) are significantly different at P = 0.05 [from 24, and more details there]. Copyright granted by Cambridge Academic Press

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in horses than in humans (Hodgson et al., 1993 Wilson et al., 2007). In treadmill experiments, where uncompensatable heat stress was imposed and maximal evaporative capacity and rectal and pulmonary arterial temperatures were monitored, it was found that horses do have a limited capacity to acclimatise to hot, humid conditions. While exercising at modest rates, the rate of rise in pulmonary arterial temperature was slow and heat storage was minimal but this acclimatisation advantage disappeared at higher work rates (Geor et al., 2000; Lindinger, 2014).

Studies on Equid Anhidrosis Reveal Limitations in Sweat Gland Anatomy Anhidrosis in horses, or their inability to sweat, has been described for over fifty years for horses in heavy work in hot humid environments (Hodgson et al., 1994). It is not known (yet) whether anhidrosis occurs in other equids too or not. In 1999, the lowered response of sweat glands to β-adrenergic stimulation in anhidrotic horses underlined the physiological basis of sweat gland function in horses, and pointed the way to the pathology of anhidrosis (Marlin et al., 1999). Further work on sweat gland function, to support the working hypothesis that anhidrosis is due to a break down in secretory apparatus of the sweat glands, was carried out in 2007 (Jenkinson et al., 2007; Wilson et al., 2007). Elevations in core temperature during intensive exercise are the consequence of anhidrosis (Fig. 9.9).

Fig. 9.9 Weight loss (kg) pre- to post-exercise (°C) as function of increase in rectal temperature (° C) pre- to post-exercise (for each of two exercise treadmill runs of Thoroughbred horses). N = 6 (Sneddon, unpublished data)

264 Table 9.4 Mean 95% CI Sweat electrolyte concentrations post-exercise derived from sealed Tegaderm® patches eluted with deionised water (mmol.l-1) and total protein g.l-1 in sweat of control and anhidrotic horses

J. Sneddon

Sodium neck Potassium neck Sodium gluteal Potassium gluteal Na+/K+ ratio neck Na+/K+ ratio gluteal Total protein g.l-1

Control 94±18.4 20±6.1 87±20.8 17±5.1 5.7±3.55 6.6±5.17 60.3±1.71

Anhidrotic 69±34.2 14±8.8 42±36.7 6±8.1 4.9±0.90 5.1±1.64 63.8±4.40

P value