Evolution of Herbivory in Terrestrial Vertebrates Perspectives from the fossil record Edited by Hans-Dieter Sues Royal Ontario Museum and University of Toronto CAMBRIDGE UNIVERSITY PRESS Cambridge, New York, Melbourne, Madrid, Cape Town, Singapore, São Paulo Cambridge University Press The Edinburgh Building, Cambridge CB2 2RU, UK Published in the United States of America by Cambridge University Press, New York www.cambridge.org Information on this title: www.cambridge.org/9780521594493 © Cambridge University Press 2000 This publication is in copyright. Subject to statutory exception and to the provisions of relevant collective licensing agreements, no reproduction of any part may take place without the written permission of Cambridge University Press. First published 2000 This digitally printed first paperback version 2005 A catalogue record for this publication is available from the British Library Library of Congress Cataloguing in Publication data Evolution of herbivory in terrestrial vertebrates: perspectives from the fossil record / edited by Hans-Dieter Sues. p. cm. Includes index. ISBN 0 521 59449 9 (hardcover : alk. paper) 1. Herbivores, Fossil–Evolution. 2. Vertebrates, Fossil. I. Sues, Hans-Dieter, 1956– QE841.E96 2000 566–dc21 00-020863 ISBN-13 978-0-521-59449-3 hardback ISBN-10 0-521-59449-9 hardback ISBN-13 978-0-521-02119-7 paperback ISBN-10 0-521-02119-7 paperback Contents List of contributors page vii Preface ix 1 Herbivory in terrestrial vertebrates: an introduction 1 Hans-Dieter Sues 2 Herbivory in late Paleozoic and Triassic terrestrial vertebrates 9 Robert R. Reisz and Hans-Dieter Sues 3 Prosauropod dinosaurs and iguanas: speculations on the diets of extinct reptiles 42 Paul M. Barrett 4 The evolution of sauropod feeding mechanisms 79 Paul Upchurch and Paul M. Barrett 5 Plant-eaters and ghost lineages: dinosaurian herbivory revisited 123 David B. Weishampel and Coralia-Maria Jianu 6 Dental constraints in the early evolution of mammalian herbivory 144 John M. Rensberger 7 Patterns in the evolution of herbivory in large terrestrial mammals: the Paleogene of North America 168 Christine M. Janis 8 Origin and evolution of the grazing guild in Cenozoic New World terrestrial mammals 223 Bruce J. MacFadden Taxonomic index 245 Subject index 249 [v] Contributors Paul M. Barrett Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK Christine M. Janis Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912 Coralia-Maria Jianu Muzeul Civilizatiei Dacice si Romane Deva, B-dul 1 Decembrie Nr. 39, 2700 Deva, Romania Bruce J. MacFadden Florida Museum of Natural History, University of Florida, Gainesville, FL 32611 Robert R. Reisz Department of Biology, Erindale College, University of Toronto, 3359 Mississauga Road, Mississauga, ON L5L 1C6, Canada John M. Rensberger Burke Museum and Department of Geological Sciences, Box 353010, Uni- versity of Washington, Seattle, WA 98195 Hans-Dieter Sues Royal Ontario Museum, 100 Queen’s Park, Toronto, ON M5S 2C6, and Department of Zoology, University of Toronto, Toronto, ON M5S 1A1, Canada [vii] viii Contributors Paul Upchurch School of Biological Sciences, University of Bristol, Woodland Road, Bristol BS8 1UG, UK David B. Weishampel Department of Cell Biology and Anatomy, The Johns Hopkins University School of Medicine, 725 North Wolfe Street, Baltimore, MD 21205 Preface This book presents a collection of paleontological perspectives on the origin and evolution of herbivory in various major taxa of terrestrial ver- tebrates. The complex interactions between plants and their animal con- sumers have long been the subject of much interest to evolutionary biologists. At the same time, most studies exploring coevolutionary rela- tionships have focused on extant organisms, and generally little atten- tion has been paid to the historical development of plant–animal interactions through time documented by the fossil record. Most contributors to this volume review the nature and acquisition of structural features of the skull and dentition suitable for feeding on high- fiber plant material in various major lineages of herbivorous tetrapods. In some instances, they also discuss other lines of evidence (such as isotopic data) bearing on this issue as well as the possible impact of herbivory on the evolutionary diversification of that group. Traditionally, paleobiolog- ical studies have assumed a direct relationship between form and func- tion, but current research on the functional morphology of extinct organisms is much more mindful of the inherent theoretical and practical difficulties in reconstructing the habits of ancient organisms. The present volume cannot and does not provide a comprehensive account of her- bivory in extinct vertebrates. Rather, it is intended as a review of current research on some of the key issues for advanced students of evolutionary biology, historical ecology, and paleobiology and, it is to be hoped, as a stimulus for further work. Most chapters are based on contributions presented at a symposium on the evolution of herbivory in insects and terrestrial vertebrates held during the Sixth North American Paleontological Convention (NAPC-96) at the Smithsonian Institution in Washington, D.C. in June 1996. Special [ix] x Preface thanks are due to the co-organizer of this symposium, Conrad C. Laban- deira (National Museum of Natural History), for his co-operation and for sharing my enthusiasm for this subject, and to the Organizing Commit- tee of NAPC-96 for its interest and support. As editor, I am indebted first to the contributors, for taking part in this project, for (in some cases) meeting deadlines, and for cheerfully putting up with my editorial efforts. At Cambridge University Press, I would like to thank Robin Smith, who first encouraged me to compile this collection of papers, and Tracey Sanderson for her continuing encouragement and support. During the editing of this volume, I have heavily relied on the expertise of many reviewers. I would like to acknowledge the generous assistance and thoughtful comments provided by Richard Beerbower (State University of New York, Binghamton), Robert L. Carroll (McGill University), Peter Dodson (University of Pennsylvania), Robert J. Emry (Smithsonian Institution), James O. Farlow (Indiana University–Purdue University, Fort Wayne), Mikael Fortelius (University of Helsinki), the late Nicholas Hotton III (Smithsonian Institution), John P. Hunter (New York College of Osteopathic Medicine, Old Westbury), Christine M. Janis (Brown University), Gillian King (University of Cambridge), Paul L. Koch (University of California at Santa Cruz), David B. Norman (University of Cambridge), Robert R. Reisz (Erindale College, University of Toronto, Mississauga), Richard K. Stucky (Denver Museum of Natural History), David B. Weishampel (The Johns Hopkins University), and Jeffrey A. Wilson (University of Chicago). I thank Janice Robertson for her careful copy-editing and especially Joan Burke (Royal Ontario Museum) for her meticulous proof-reading. Hans-Dieter Sues hans-dieter sues 1 Herbivory in terrestrial vertebrates: an introduction Introduction Understanding the ecological attributes of extinct organisms has long been a major research topic in paleobiology, dating back to the pio- neering work of the French paleontologist Georges Cuvier in the early nineteenth century. Inferences concerning the ecology of an extinct organism can be based on functional interpretation of its structure, by analogy with present-day relatives, or from the sedimentary context and distribution of fossil remains referable to this taxon (Wing et al. 1992). Traditionally, functional morphology has been the most widely used of these approaches. It basically relies on the analysis of organisms as simple machines with functional attributes that can be inferred from the physi- cal properties of their bodies as well as from their shape and size. Chemi- cal analyses of hard tissues (such as extraction of preserved stable carbon isotopes) increasingly are providing significant new data for inferring diet in extinct animals. In recent years, researchers have developed various procedures for linking inferences concerning function in fossils to phylogenetic analyses, increasing confidence in the robustness of these reconstructions (see various papers in Thomason [1995]). Herbivory, the consumption of plant tissues, is a widespread phenom- enon among terrestrial vertebrates. It has frequently and independently evolved in many lineages of amniotes during the last 300 million years or so. Some major groups of herbivorous tetrapods, such as ungulate mammals and ornithischian dinosaurs, attained great abundance and taxonomic diversity. Indeed, the advent of herbivory among land- dwelling tetrapods was one of the key events in the history of life on land. It led to the establishment of ‘modern’ continental ecosystems, with vast [1] 2 hans-dieter sues numbers of herbivores supporting a relatively small number of carni- vores, during the Permian period (Olson 1966; Hotton et al.1997; Sues and Reisz 1998). Feeding on plants requires many morphological and physiological modifications to facilitate the efficient reduction and digestion of plant tissues. Plant fodder contains less caloric energy per volume unit than do animal foods (Southwood 1973). Furthermore, in most instances, much of that energy is tied up in substances that are difficult to digest for verte- brates. The contents of plant cells are enclosed by walls that are primarily composed of cellulose, hemicellulose, and lignin. Cellulose is a polymer of glucose, but its glucose units are linked together in such a fashion that it cannot be readily broken down. This makes plant tissues, to varying degrees, more difficult to digest than animal tissues, which are devoid of resistant cell walls. Extant vertebrates lack any endogenous enzymes to hydrolyze the compounds forming the cell walls of plant tissues, but many micro-organisms (bacteria, protists) can produce them. Thus many plant-eating tetrapods have entered into endosymbiotic relationships with such organisms to facilitate cellulysis in their digestive tracts, result- ing in the production of sugars and volatile fatty acids that can be absorbed by the vertebrate host. Not only are the walls of the plant cells themselves resistant to unaided digestion by vertebrates but they often protect the digestible cellular contents such as lipids, sugars, organic acids and proteins. Initial breakdown of the cell walls by mechanical or chemical action is thus required. Plant tissues are highly variable in terms of their nutritional value to vertebrate consumers. Certain plant parts, such as fruits, seeds, and immature vegetative tissues, contain much digestible matter that is only protected by relatively delicate cell walls and often require only little pro- cessing to make the enclosed nutrients available to the consumer. However, these are seasonally available resources, and most herbivores subsist on the tougher, more cellulose-rich vegetative structures, such as leaves, roots, shoots and stems that form the bulk of available plant material. The effective utilization of such fodder by the vertebrate consu- mer requires two steps. First, the plant material must be mechanically broken up by oral processing or by comminution in a muscular foregut or gizzard using ingested grit and pebbles. Grinding the plant fodder more finely clearly increases the rate at which herbivores can process it (Bjorn- dal et al. 1990). Second, symbiotic micro-organisms in the gut must convert the cellulose into volatile fatty acids (especially acetic, butyric,