Hypsodonty in Mammals Evolution, Geomorphology, and the Role of Earth Surface Processes

Home , Astrapotheria, Astrapotheriidae, Astrapotherium, Cephalomyidae, Insular India, Mesaxonia

The evolution of high-crowned teeth, hypsodonty, is a deﬁning characteristic of many terrestrial herbivores. To date, the most prominent focus in the study of the teeth of grazing herbivores has been co-evolution with grasses and grasslands. This book develops the idea further and looks at the myriad ways that soil can enter the diet. Madden then expands this analysis to examine the earth surface processes that mobilize sediment in the environment. The text delivers a global perspective on tooth wear and soil erosion, with examples from the islands of New Zealand to the South American Andes, highlighting how similar geologic processes worldwide result in convergent evolution. The ﬁnal chapter includes a review of elodonty in the fossil record and its environmental consequences. Offering new insights into geomorphology and adaptive and evolutionary morphology, this text will be of value to any researcher interested in the evolution of tooth size and shape.

Richard H. Madden is a research professional in the Department of Organismal Biology and Anatomy at the University of Chicago. In over 30 years of studying mammalian ecology, he has spent extensive periods conducting paleontological surveys throughout South America. His current research focuses on geographic variation in tooth wear rates in herbivores and the impact of environmental and geologic processes.

Hypsodonty in Mammals Evolution, Geomorphology, and the Role of Earth Surface Processes

RICHARD H. MADDEN Department of Organismal Biology and Anatomy University of Chicago, Chicago, IL, USA University Printing House, Cambridge CB2 8BS, United Kingdom

Cambridge University Press is part of the University of Cambridge. It furthers the University’s mission by disseminating knowledge in the pursuit of education, learning and research at the highest international levels of excellence. www.cambridge.org Information on this title: www.cambridge.org/9781107012936 © R. H. Madden 2015 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 2015 Printed in the United Kingdom by TJ International Ltd. Padstow Cornwall A catalogue record for this publication is available from the British Library Library of Congress Cataloguing in Publication data Madden, R. H. (Richard H.) Hypsodonty in mammals : evolution, geomorphology and the role of earth surface processes / Richard H. Madden, Department of Organismal Biology and Anatomy, University of Chicago. pages cm Includes bibliographical references. ISBN 978-1-107-01293-6 (Hardback) 1. Hypsodonty. 2. Teeth–Growth. 3. Teeth–Evolution. 4. Mammals. I. Title. SF869.5.M33 2015 599.9043–dc23 2014021006 ISBN 978-1-107-01293-6 Hardback Cambridge University Press has no responsibility for the persistence or accuracy of URLs for external or third-party internet websites referred to in this publication, and does not guarantee that any content on such websites is, or will remain, accurate or appropriate. Bernard Healy and Mike Rudge, pioneers in the study of soil ingestion and island comparisons of tooth wear. For Callum, Fredy, and Guiomar, and the love of Annie, Clay, Kendy, and Regan Contents

Preface page xi Acknowledgments xviii

1 Hypsodonty in South America 1 1.1 The tangled history of precocious hypsodonty 1 1.2 Explaining the prevalence of hypsodonty in South American mammals 9

2 Hypsodonty in the South American fossil record 12 2.1 Background 12 2.2 Hypsodonty as a feature of notoungulate evolution 19 2.3 Hypsodonty in the middle Cenozoic of Patagonia 25 2.4 Crown height and the single-chamber stomach in notoungulates 50 2.5 South America exceptional? 55

3 South America and global hypsodonty 59 3.1 Mammalian hypsodonty in South America 59 3.2 Sigmodontine hypsodonty and geography 73 3.3 Hypsodonty in mammals around the world 80

4 Excess tooth wear in New Zealand 85 4.1 History of study 85 4.2 The epidemiology and etiology of excess tooth wear 92 4.3 Geographic patterns 93 4.4 Temporal patterns 101 4.5 ENSO, erosion, and tooth wear 111 4.6 Conclusions about the etiology of excess tooth wear 116

5 Soil erosion, soil ingestion, and tooth wear in Australia 120 5.1 Introduction 120 5.2 The original study of sheep tooth wear 122

vii viii Contents

5.3 Dust ﬂux and soil ingestion in southeastern Australia 132 5.4 Methods 135 5.5 Results and discussion of time series analysis 137 5.6 A more complex etiology? 144 5.7 Human tooth size and molar wear 144 5.8 Conclusions 150

6 Crown height and tooth wear on islands 154 6.1 Why islands? 154 6.2 Crown height evolution on Mediterranean islands 154 6.3 Environmental change on Mediterranean islands 161 6.4 From consequences to processes 163 6.5 Feral goats and sheep on islands 164 6.6 Conclusions 190

7 The East African Plio-Pleistocene 191 7.1 Introduction 191 7.2 The terrestrial fossil record 195 7.3 The record of soil erosion from source to sink 198 7.4 Data analysis 211 7.5 Conclusions 233

8 The middle Cenozoic of Patagonia 236 8.1 Introduction 236 8.2 Climate intimacy between Patagonia and the Southern Ocean 238 8.3 Drake Passage 242 8.4 Paleotemperature and paleoprecipitation 244 8.5 Volcanic activity 255 8.6 Vegetation in Patagonia 260 8.7 Wind, marine productivity, and hypsodonty 266 8.8 Discussion 270 8.9 Summary 278

9 Ever-growing teeth 280 9.1 Introduction 280 9.2 Ever-growing teeth 285 9.3 Why ever-growing teeth? 298 9.4 Consequences of the evolution of ever-growing teeth 299 9.5 Environmental impact of ever-growing teeth in South America 313 9.6 The Vicugna 315 9.7 Engines of erosion? 320 Contents ix

10 Summary and conclusions 323 10.1 Summary 323 10.2 The metaphysics of causation 337 10.3 The past and prospects for the future 342

References 348 Index 406

Preface

This work will summarize many years of active research and thinking about an explanation for the evolution of high tooth crowns in South American mammals, and the global path that curiosity has taken me in the search for the causes and broader implications. The subject of the book is nearly iconic in paleontology and is active in the minds of many in evolutionary morphology. The approach used in this book is different. It takes inspiration from diverse disciplines: from the earth sciences (and specifically geomorphology and the study of earth surface processes) to island biogeography, and to the mammalogy, geology, and paleontology of the southern continents in the quest for a universal explanation for both prevalent and unique patterns of tooth shape evolution. Most recently, impetus has arisen from the fruits of a research project that Cambridge University Press published in 2010 (The Paleontology of Gran Barranca). In many ways, this book is an extension of that work and might be considered a companion volume to that title...in effect, this is all the stuff left out of that book for lack of space. Further impetus has come through the generosity of the National Evolutionary Synthesis Center (NESCent) in Durham, North Carolina, which supported a catalysis meeting in April 2011 on the subject of Earth Surface Processes in the Evolution of Mammalian Tooth Shape, to which many attending listened patiently. The range of life and earth science disciplines incorporated into the whole is diverse, and it has required much effort on my part, as a nonspecialist paleontologist, to approach reasonable familiarity with disciplines this diverse. Moreover, the geographic coverage is vast, and obtaining familiarity with every geography used in the argument has been demanding. Were the contents published piecemeal in the standard journal format and following the narrow disciplinary strictures of that format, each individual component would become subject to easy criticism, and the case made in each chapter might be dismissed as circumstantial. The deficiencies in each component are not hard to find, and some (in fact, many) are obvious to me. Serious criticism of each component, while perhaps meritorious in the narrow application of each, would probably prove devastating. Taken together, however, the case for the environmental causation I invoke seems to explain a lot of mammalian tooth evolution, and in its entirety, is far stronger as an integrated theory than its parts taken separately. In other words, the central idea of this book is stronger than the sum of its individual parts. xi xii Preface

Adequate explanation requires that we consider two different timescales, ecological and evolutionary. An ecological timescale is a mere day in the life compared with the evolutionary timescale. Excess tooth wear is the pathology that drives the evolution of hypsodonty and elodonty. Etiology, the study of causes in veterinary or animal pathology, is the science that deals with the causes of excess tooth wear. Epidemiology, the study of temporal and geographic patterns of animal health and pathology and their associated factors at the population level, is the cornerstone of this treatise. While it deals with the study of causes, distribution, and control of pathology in animal populations, epidemiological associations or correlations never prove causation; that is, they cannot prove that a specific agent actually causes excess tooth wear. Causality is the relationship between an event (the cause) and a second event (the effect), where the second event is a consequence of the first. Aristotle distinguished four causes: material, formal, efficient, and final. Although cause and effect typically are related to events, characterizing the causal relationship can be the subject of much debate. In a causal pathway, there is a natural flow to events and cause precedes effect. Factual causation is established by answering the question: did the agent act in the loss of tooth mineral substance? This is equivalent to finding a phytolith embedded in tooth enamel at the end of a long scratch. On the basis of its morphology, a phytolith could be attributed to a grass plant, but the phytolith may have been ingested along with other soil minerals directly off the soil surface. In this case, the physical cause of this wear event was the phytolith, but the temporal cause of excess tooth wear would be the ingestion of soil minerals. Concurrent causes where separate acts combine to produce the effect and sufficient combined causes where either would have been sufficient to produce the effect complicate the picture further. As I will argue, there may be concurrent causes, but only one is sufficient to produce the effect. If this one sufficient cause results in extraordinary results in one place at one time, is it fair to hold the actor responsible for all resultant consequences everywhere? When we ask whether the agents of abrasion are either phytoliths or soil mineral particles, and attempt to distinguish them and weigh their relative roles by proposing to search for distinctive features in the wear striations they produce on the tooth surface, we are demarcating a disciplinary boundary between the life and earth sciences. Either we are trying to establish a claim for the role of botany by restricting the view to substances within the organic foods animals consume, or alternatively, we may be trying to establish a claim for the role of geomorphology by placing emphasis on mineral particles external to the foods animals eat. To say it is either phytoliths or soil mineral particles is to assert the boundary. Adversarial “either/or” approaches that would look for a smoking gun (or abrasive) embedded in the tooth enamel at the end of a scratch, to prove that one or the other has a dominant role in the evolution of tooth shape, is, in my judgment, a misguided search for legalistic proof and would be fruitless in the face of the complexity of the real world. Why would we expend any energy or resources in an effort to simplify what are naturally complex processes, especially when we have tools at our disposal for Preface xiii

managing complexity? To assert that one or the other dominates tooth wear (and thereby partake in a dialog in paleontology that perpetuates a false dichotomy but a convenient straw man), denies the ability of science to manage complexity and diminishes appreciation for the complexity of the thinking of scientists. When it is observed that suspended sediment yield cannot possibly have anything to do with soil ingestion or tooth wear, and that most tooth wear occurs when the animal grazes not when soil mineral particles are being swept downstream, the same disciplinary boundary between life and earth sciences is being demarcated to establish a claim against the role of geomorphology in evolution. For zoology, what I propose does not deny the role of animals in both creating and modifying the interaction between their oral environment and the external environment. Animals are active agents that live on the surface of the Earth and interact with it. To claim that food texture and food physical properties drive the evolution of tooth shape arises from the obvious fact that what is important about diet is the energy and nutrients animals derive from the food they eat. This is certainly true and it is only rational that the shape of teeth is related to the requirements of reducing the foods animals eat. What I am definitely not saying, however, is that zoology, botany, and geomorphology have nothing to do with mineral particle ingestion or tooth wear. There is a role for earth surface processes in the delivery and movement of mineral abrasives through the animal’s environment, but ultimately, animals must be the active agents that bring these soil mineral particles into their mouths. Much of the lack of a history of the idea could be described as a consequence of the tension at the boundary between these traditional disciplines. We have ignored the role of earth surface processes in tooth evolution, much like we have ignored the role of the earth system on human economic activity. Changing the way we think about tooth evolution is like changing the way we think about climate change; we confront the entrenched interests that benefit from ignorance. Disciplinary boundaries in the funding of life and earth science still exist. However, pervasive evidence for the evolution of many conspicuous features of tooth shape makes it equally certain that much of tooth shape evolution has been driven by abrasive wear. It may be that tooth mineral substance itself evolved in response to the confrontation inherent in the interaction between life and the Earth’s surface. We do not live outdoors, and we have little to no idea what the experience of living outdoors entails. If you have ever been a Scoutmaster trying to teach urban children (and their parents) how to experience life outdoors, you will know what I mean. There is a huge disconnect between the urban and natural worlds, and many are afraid of the outdoors. If we are lucky, we occasionally do fieldwork. True lovers of fieldwork who spend long intervals outdoors over many years are few and far between and seem to be getting fewer all the time. Fewer still travel outdoors extensively, so even fewer have had the experience of living outdoors in diverse environments. Most highly paid experimental- ists and most theoreticians in our discipline do not do so, and the museum collection or herbarium is as close to the outdoors as they get. While it is my belief and my hope that fieldworkers have a better appreciation of the things I am talking about, I am not sanguine about the prospect that others have. xiv Preface

I have done a lot of paleontology fieldwork, over 54 times in South America, almost all of it in the Andes. I do not know how many days and nights I have spent outdoors in the Andes, but conservatively, I would guess about 2000. I have worked in Venezuela, Colombia, Ecuador, Peru, Bolivia, Chile, and Argentina, and during that work, have traveled and walked over much of the cordillera. What I have seen, and my cumulative experiences have shaped my understanding of the natural world. Soil ingestion is acknowledged to contribute to tooth wear, but is rarely an area of active study. Why? In domestic animal husbandry, effective management solutions for excess tooth wear are known and used every day. Stocking rates are adjusted and the animals are provisioned during harsh seasons. Consequently, excess tooth wear is not a problem of active interest because it is a problem that can be solved. Excess tooth wear in Patagonia is solved by sending older animals out of the “roaring 40s” in the Southern Volcanic Zone to lower latitudes for final fattening. Excess tooth wear is solved in New Zealand by carefully controlling the season of exposure. Excess tooth wear is solved in Australia by careful attention to stocking rates in winter. Our own experience is also wrapped tightly by food preparation. This is big industry. Washing harvests and preparing and packaging foods prevent soil contamination and shield us from experiences that might wear out our teeth and open our eyes. All the diverse ethnic cuisines that thrill the palate and all of ethnography’s description of human diet variation document an impressive array of cultural diversity in food handling. However, ethnographers rarely if ever describe the mineral grit in the human diet and it is not evident by their accounts. Archaeologists also spend considerable effort in understanding the long history of changing human diets and cultural activities associated with food procurement, gathering, preparation, and consumption. One thing we can conclude from all this is that humans put a lot of effort into avoiding dirt. So does evolution. A lot of physiological and structural adaptation involves the avoidance of mineral grit and windborne particulates. Eyelids, the nictitating membrane, lacrimal apparatus, guard hairs around the nostrils, vermillion lips, orbicularis oculi and oris, histamine reactions to dust, the sneeze reflex, coughing, and outsized salivary glands with ducts that deliver saliva at the point of contact between tooth surfaces are all adaptations to an environment rich in mineral particles. This whole idea that earth surface processes may have a role in the evolution of tooth shape has been building for thirty years. As the idea for this book began to take shape and throughout its gestation, I have been plagued with doubts about it. I do not see this idea as displacing any pre-existing ideas about tooth shape evolution. Too much good work has been done and too many interesting and plausible ideas have been voiced. All these ideas seem worthy and all of them probably true for some times and some places. The only new insight really is that the sedimentary rocks in which we find fossils may preserve something besides the fossils, something so obvious that we have overlooked it: the mineral particles that shape teeth. The relationship between mineral particles and tooth shape (or at least many features of tooth shape) seems to be direct, was “discovered” in many different ways and in many different places, and can be expressed in many different graphical forms over many different timescales. If the idea of this relationship is original, then the question Preface xv

becomes: why have we missed it? There are many possible reasons and a host of suspicions fill my mind. As will become evident, the edifice is built upon vulnerable foundations. The weakest and most vulnerable parts of the foundation are my own limitations. This is a very deeply seated doubt that keeps me humble, and until now has kept me silent. While there are benefits to silence (peace of mind, room for contemplation and better concentration, more maturity, and time to complete laborious tasks and make more ambitious collections), there are also costs. In many ways, none of the ideas in this presentation are my own. I borrow shamelessly, and maybe sometimes without attribution, and I apologize for this. The fact that the pace of accumulating ideas, images, and experiences seems to be accelerating, is no excuse. Finally, as I grow older, I appreciate that the idea is more important than the purveyor. If the idea is to have any future at all, it must be aired and preferably to an audience in the best position to judge. This audience, hopefully, will include specialists from the disciplines I borrow from so shamelessly, as well as young people with critical minds and fresh energy. There are only two directions to take the idea now, and these are plausibility and universality. Plausibility is to be judged by the reader; universality is to be tested in the field. Readers taking their own path through the thicket of the text must examine the relationship in terms of a complex exercise in mass balance between sediment source and its ultimate sink on the sea-floor. In the balance hangs the mineral particle flux that passes through the mouths of herbivores. For universality, we must take the best tools possible to diverse islands where we will find the empirical truth and the limitations of its expression. We must measure soil loss, soil ingestion, and tooth wear rates, on each and every one of these islands, and we must compare among the islands to learn where the evolutionarily significant differences reside. It is growing late. Goats and rabbits are being eradicated from islands, and many, too many islands have been and are being liberated from their burden. Note: The editors requested that the term “hypsodonty” be used in the title of this book because of the popularity of the term. To a paleontologist, hypsodonty conveys more precise meaning. I try to explain my use of the term hypsodonty and related terms like elodonty for expressing tooth shape evolution where appropriate in the text. Once defined, I also try to be consistent throughout.

How to read this book

Chapter 1 is important, as it deﬁnes the problem and sets the stage for the remainder of the book. Chapter 2 provides a lot of background to the South American fossil record. However, the chapter also has many details about the Patagonian fossil record of the “precocious” evolution of tooth crown height and these details can be tedious, and can be skipped by readers not familiar with the South American fossil mammal record. xvi Preface

Chapter 3 explores the broad patterns of association between the prevalence of high- crowned teeth in South American mammals, and a host of environmental variables. Some of these associations suggest a role for earth surface processes. Additionally, broader global patterns are examined, and these serve to confirm this suspicion. Chapter 4 begins with a history of the study of excess tooth wear in New Zealand. Then, it presents the evidence for temporal and geographic variation in tooth wear and soil ingestion on the North Island. This is followed by a discussion of El Niño– Southern Oscillation (ENSO) interannual climate cycles and erosion. Suspended sediment yield, the fine-grained sediment transported in suspension by rivers that varies with erodibility is highly correlated with annual tooth wear. The lake sediment record of rainstorm deposits varies with decadal timescale phases in the intensity of ENSO and suggests how longer-term variation in erosion has its expression in soil ingestion and tooth wear. Chapter 5 examines the only available long-term study of tooth wear in dry climates, in southeastern Australia. This evidence is equivocal. There are suitable routing systems and a sediment cascade is evident, but there is little concrete evidence for its action on tooth wear. While much that was ingested was ignored during this classic study (and one wonders why), there is room for a contribution from earth surface processes. Australia is a unique continent, and today has only a very thin mantle of surface sediment available for these processes. During deglaciation phases of the Quaternary, however, this system did operate and may have contributed to slow tooth size evolution in modern humans. Chapter 6 describes the evidence for independent evolution of tooth crown height in insular mammals on islands in the Mediterranean. The fossil record of mammal evolution on these islands is remarkable, although probably deficient for any serious study of surface processes in the past. Islands are not usually hospitable for the preservation of fossil records, but the energy and persistence of paleontologists is legendary and the allure of islands too great to convey through mere words. This chapter also makes a comparison of tooth wear in feral goat and sheep populations from three small islands in the South Pacific with contrasting vegetation and soil erosion regimes. These examples suggest a way forward. Chapter 7 turns from the ecological to the evolutionary timescale and examines the fossil record of tooth shape evolution in the Plio-Pleistocene of East Africa. This may be the best fossil record of tooth shape evolution on Earth. Tooth shape evolution in many lineages of mammals can be followed here, unlike almost everywhere else on Earth. This record is made even more compelling because of the close coupling between this terrestrial fossil record and the downwind terrestrial sediment record on the sea-floor of the Gulf of Aden and North Arabian Sea. Here it is possible to track the intensity of surface processes as they deflated, entrained, transported, and then deposited surface mineral particles onto the sea surface and eventually the sea-floor. This remarkable record of the source-to-sink sediment cascade allows the capture of detailed records of volcanic eruption frequency, the intensity of erosion and surface winds, the flux of mineral particles through the atmosphere, and their consequences for the evolution of tooth structures that serve to prolong the functional utility of the dentition. Preface xvii

Chapter 8 provides some arguments for asserting that records of tooth wear and tooth evolution on islands provide meaningful inspiration and new tools for reconstructing and understanding broadly similar mechanisms as preserved in less continuous records elsewhere, particularly in Patagonia and the Southern Ocean. This chapter presents an example of the application of these principles to the fossil record in deep time, in particular, the middle Cenozoic record of tooth shape evolution in Patagonia. This is one of the few records that captures tooth evolution in clades of mammals in deep time, and in the context of a rich geology and paleooceanography. Chapter 9 explores elodonty, and is more speculative. It presents some thoughts about the evolution of ever-growing teeth and their possible significance to earth surface processes. Of the 26 clades of mammals that evolved high-crowned teeth in South America, half of them went on to evolve ever-growing teeth. The significance of the evolution and appearance of completely elodont dentitions in so many mammals is explored. Eventually this exploration turns the relationship around, and points out how elodont herbivores may have left an important and unique signal in the history of surface erosion. The final chapter attempts to summarize what I think I have learned. Acknowledgments

Where to begin? It all began with Richard Frederick Kay, my professor, mentor, colleague, and friend. Nobody could ever have inspired work on the relationship between tooth shape and the environment in a more disinterested and informed way. The subject of tooth shape evolution has been Rich’s life, and I am a mere usurper into his domain. He has graciously made space for me by providing intellectual life and liberty. Others at Duke tolerated my presence, and I will be forever grateful to Matt Cartmill, Elwyn Simons, Paul Baker, Dan Livingstone, John Lundberg, Joseph Bailey, Steve Churchill, and Naomi Quinn for their many courtesies and inspiration. The Medical School at Duke University unwittingly endured much of the gestation of this book, especially former Dean Ed Halperin and current Dean Edward Buckley. Similarly, the authorities of the Pritzker School of Medicine at the University of Chicago have tolerated my idiosyncracies. In addition to these admirable administrators, many medical students, residents, and faculty divided my attention by reminding me that there are more important things in life than the cloistered pursuit of an abstract idea in paleontology. Thanks to all those mentioned, I have enjoyed the continued support of the United States National Science Foundation and the taxpayers who support it, and I wish to thank all the anonymous reviewers, panelists, and program directors who were instru- mental to the support that got me into the ﬁeld. Among those I must single out are my steadfast colleagues Aaron Hogue, Alex van Nievelt, Callum Ross, Marcelo Sanchez, Eduardo Bellosi, Gerry Eck, Alfedo Carlini, and Guiomar Vucetich. I must also recognize the patience and interest of my former students Alejo Scarano, Elizabeth Kowalski, Maria Inez Perez, and Patricia Braun. In South America, I have been assisted in all aspects of this work. In Patagonia, I must thank all the students from the Universidad Nacional de La Plata who helped collect the fossils, including Carolina Vieytes, Esteban Soibelson, Magallanes Soledad, German Gasparini, Diego Brandoni, Sebastian Poljak, Damian Glaz, Roberto Cidale, Veronica Gomis, Mauricio Vinocur, Roberto Avila, Jorge Noriega, Georgina Erra, Maria Encar- nación Pérez, Adrian Guillaume, Valeria Bertoia, Martin Ciancio, Daniel Aquino, Alejandra Alcaraz, Valeria Clar, Viviana Seitz, Analia Francia, Cecilia Krmpotic, Alejo Scarano, Noelia Corrado, Patricia Garcia, Ramiro Almagro, and Alejandra Abello. In the Andes of Colombia, I was helped in many ways by Don Butler, Ricardo de la Espriella, Reinaldo Quintero, Javier Guerrero, and the authorities and capable staff of the Servicio xviii Acknowledgments xix

Geológico Colombiano (formerly the Instituto Nacional de Investigaciones Geológico- Mineras, INGEOMINAS). In Ecuador, I need to thank Emilio Bonifaz, Father Pedro I. Porras G., Dr Salvador Lara, Ing Guillermo Cabrera, César Cabrera, Dra Eugenia del Pino, Drs Carmen, and Luis Albuja, and Dr Ramiro Barriga, and the authorities of the Escuela Politécnica Nacional in Quito. In Peru, I received generous hospitality from Dra Josefina Ramos de Cox, Mercedes Cardenas, and Inez del Aguila Rio at the Seminario de Arqueologia de la Pontificia Universidad Católica del Perú in Lima. In Bolivia, I was warmly received by Leonardo Branisa, Carlos Villarroel and Raul Carrasco of GeoBol, Federico Anaya, Bernardino Mamani Quispe and Rueben Andrade of the Museo de Historia Natural in Cota Cota. In Chile, I wish to thank Patricia Salinas and Alejandro Godoy for all their help. In Argentina, the list is long, but I especially wish to acknowledge the assistance of Rosendo Pascual, Mario Mazzoni, Mario Franchi, Rubén Somoza, Carlos Dal Molin, Norberto Malumian, Guillermo Ré, Juan J. Vilas, Edgardo Ortiz-Jaureguizar, Marcelo Reguero, Alejandro Kramarz, Alberto Cione, Cecilia Deschamps, Guillermo López, Mariano Bond, Javier Gelfo, Pancho Goin, Alejandra Abello, Zulma Gasparini, Martin Ciancio, and Edgardo Latrubesse. In Brazil, I have been warmly welcomed by Ana Maria Ribeiro and Jorge Ferigolo and their students at the Fundação Zoobotânica do Rio Grande do Sul, by Alceu Rancy at the Universidade do Estado do Acre in Rio Branco, and by Herculano Alvarenga in Taubaté. My work in New Zealand was made possible by Janet Wilmshurst and John Parkes of Landcare in Lincoln, and I have been warmly received by Bernard Healy, Mike Rudge, and Les Basher. Basil Gomez, now in Hawaii, patiently responded to my many questions. John Damuth and the NCEAS Working Group, especially Jessica Theodor, Catherine Badgley, Christine Janis, Mikael Fortelius, Jan Van Dam, and Lars Werdelin, all generously made their data and ideas available to me. The NESCent Catalysis Group, especially Matt Kohn and Caroline Strömberg, listened patiently while I pontificated on the idea that earth surface processes might have something to do with tooth shape evolution, and in turn, everybody who attended provided much useful feedback and inspiration. In Zurich, where I first launched this idea, I was hosted by Marcelo Sanchez and Marcus Clauss. Many museum curators have allowed access to their collections. At the Museo de La Plata (MLP), Rosendo Pascual and Marcelo Reguero have always been helpful. At the Museo Argentino de Ciencias Naturales (MACN) José Bonaparte and Alejandro Kramarz allowed me access to the Ameghino Collection. At the Museo de Geologia de INGEOMINAS in Bogotá, Victor Laverde Eastman and Luis Felipe Rincón allowed me to work with the fossil mammals from La Venta, and Carlos Villarroel at the Universidad Nacional provided access to useful and important material. At the incom- parable American Museum of Natural History (AMNH), I wish to thank the late Malcolm C. McKenna, Susan Bell, Mike Novecek, and many others among the staff who helped with my inquiries. The Field Museum of Natural History (FMNH), through its curators John Flynn and collections manager Bill Simpson, gave me unhindered access to the material in their care. At the University of California Museum of Paleontology (UCMP), my work was enabled by Howard Hutchison and Pat Holroyd. xx Acknowledgments

At Te Papa in Wellington, New Zealand, I need to thank Colin Miskelly, and at Landcare in Lincoln, John Parkes, who have made available their collections of feral ungulates. At the United States National Museum (USNM), Linda Gordon authorized a loan of sigmodontine material. Chuck Schaff and Farish Jenkins at the Museum of Comparative Zoology, Harvard University, gave me access to the fossils in their collection. At the Museo Nacional de Historia Natural in Santiago, Chile (MNHN [Ch]), Patricia Salinas was a helpful host. The East Africa chapter benefitted materially from the generous and enthusiastic help of Rebecca Cuddahee, formerly at Duke University. Tooth measurements for northeast African Theropithecus were provided by Gerald G. Eck, and for Suidae by Rebecca Cuddahee. Tooth size data for Australopithecus and Theropithecus were compiled by two Duke undergraduates, Jose Castillo and Steven Hafner, during their honors thesis work under the direction of Steven Churchill and Rebecca Cuddahee, respectively. Steven Frost at the University of Oregon and René Bobe at George Washington University provided valuable advice. Throughout this work, embedded deeply in its data structure, I use the unpublished and disinterested fruits of Carl C. Swisher III and the Berkeley Geochronology Center. It is so obvious, but it needs to be said, that nothing gets done in science without the work of librarians. Their work has changed mightily over time, but the whole edifice of knowledge is organized and maintained by their devotion. Only through their work and the custodial function of university libraries, is it possible to check bibliographic citations 30 years after having read something interesting. Additionally, I wish to thank the following microscopists, the late Tim Oliver in the extraordinary old Anatomy Department (now Cell Biology), Sharon Endow for the laser confocal microscopy, and Leslie Eibest in the SEM and ESEM laboratory in the Department of Biological Sciences at Duke University. Lastly, there was something about Duke University. Duke was my intellectual home for nearly 32 years. While it never gave me a raise in salary, it gave me nearly complete intellectual freedom constrained only by my self-imposed limits on ambition. While the Duke experience was extraordinary, it came to an end. Now, after two years, I can say that there is something as great about the University of Chicago. The University of Chicago, readers, is also a real university. To think I might actually have provided meaningful service to these institutions is almost beyond belief, and that this service could be performed in the noblest setting humanity has imagined, surrounded by the best students in the world is beyond words. Assaults on intellectual freedom be damned, here I will stand at the barricades. Most recently, Caroline Strömberg, Matthew Kohn, and Regan Dunn, have provided meaningful and critical support for the ideas expressed here. I hope this work serves their interests. Abegael West, now a graduate student at Columbia University, helped with many practical aspects of this work. Without the help of Regan Dunn, the final digitization and layout of the figures would never have been accomplished, and I would have not found the refuge and solace that was required to finish. Finally, I wish to thank the reviewers and editors at Cambridge University Press, who have been very, very patient. 1 Hypsodonty in South America

1.1 The tangled history of precocious hypsodonty

Increasing tooth crown height is an often repeated pattern in the evolutionary history of mammals. Probably the best-known example is the evolution of high-crowned teeth in horses (the family Equidae) and contemporary ungulates through a 12-million-year interval in the North American continental Miocene (MacFadden, 1992; Strömberg, 2006; Mihlbachler et al., 2011). Other noteworthy examples of the evolution of high-crowned teeth are found among extinct herbivores (e.g., Myotragus, Marremia) from islands where they were subject to the magnifying effects of geographic isolation and the instability of island ecosystems. Conspicuous examples are also found among extant mammalian herbivores (e.g., Antilocapra, Vicugna) in high arid and volcanic mountain environments. Presumably, when mineral particle ingestion is unavoidable, natural selection will enhance the physical structures in teeth that are useful for resisting abrasive tooth wear. However, neither the agencies nor mechanisms whereby continental, insular, or arid volcanic mountain environments present exceptionally abrasive environments to mammalian herbivores are understood very well. Among South American mammals, the number of examples of the independent evolution of conspicuous structures for resisting abrasive tooth wear seems extraordinary. As many as 26 clades of South American mammals evolved high-crowned or hypsodont teeth, among xenarthrans, marsupials, rodents, archaic native ungulates, and more recent immigrants among mice and ungulates. Of special note, nearly half of these clades evolved ever-growing teeth; that is, teeth that grow throughout the animal’s life, endlessly and continuously replacing tooth mineral substance lost through wear. Elodont or ever-growing teeth effectively neutralize the selective pressure imposed by environmental abrasives that would otherwise prematurely truncate the functional longevity of teeth and the reproductive life of the organism. The inventory of South American mammals with high-crowned and elodont teeth was started by Karl von Linne in 1758 (Vermilingua, Cuniculus, Silvilagus) with the mammals of the territory of the Virrenato del Rio de La Plata. Cingulata was added to the roster between 1803 and 1804 by Desmarest and Geoffroy, and Rodentia added between 1782 and 1837 by Molina, Fischer, Olfers, Brandts, and Waterhouse. The ﬁrst elodont fossil tooth from South America was described by Thomas Falkner (1774) and the ﬁrst complete skeleton of an elodont fossil mammal was the Megatherium 1 2 Hypsodonty in South America

americanum brought from Buenos Aires to the Royal Cabinet in Madrid in 1789 and described by Cuvier in 1796 (Mones, 2002). Some forty years later, Sir Richard Owen (1837) described Toxodon, the ﬁrst of several South American fossil mammals with ever-growing teeth collected by Darwin (Fernicola et al., 2009). The evolutionary transformation from low to hypsodont tooth crowns in toxodonts and the increasing prevalence of hypsodonty among archaic South American ungulates were revealed along with their context of stratigraphic superposition by the discoveries of Carlos and Florentino Ameghino (1904, 1906).

1.1.1 Precocious hypsodonty

The apparent fact of an older or precocious evolution of hypsodonty among terrestrial herbivores in the late Eocene of Patagonia has been of interest to paleontology for a long time. Without a doubt, while there are examples of the evolution of high-crowned teeth in older rocks, there is nothing like the manifest and parallel evolutionary trends among so many different taxa at about the same time in the Eocene and Oligocene as in Patagonia. Therefore, who actually “discovered” that the evolutionary trend to high tooth crowns in ungulates in Patagonia antedates similar evolutionary trends elsewhere? There are four contenders: (1) William Berryman Scott (1913, 1937a) at Princeton who, between 1913 and 1937, worked directly on fossil material from both North and South America while writing A History of Land Mammals of the Western Hemisphere in English; (2) Albert Gaudry in Paris who worked directly on fossils from both Europe and South America (the material collected by Tournoüer) and published on their morphology and evolution in French; (3) Karl von Zittel in Munich who was studying fossils from Patagonia purchased from the Ameghinos while compiling the Grundzüge, a comprehensive history, in German, of mammal evolution in the Cenozoic; or (4) Florentino Ameghino (1897, 1906) in Buenos Aires who, between 1897 and 1906 described, in Spanish and French, the original fossil material (collected by Carlos Ameghino), argued for phylogenetic afﬁnities with mammals on other continents, and documented the evolutionary trend to higher tooth crowns in Patagonia. Ameghino was the ﬁrst to describe the actual fossils and fossil taxa from pre- Santacrucian levels in Patagonia, and through his phylogenetic reconstruction of horses, is among the originators of the idea of precocious hypsodonty. For Ameghino, age control (and global correlation) was provided by the marine invertebrates from interbedded strata in Patagonia, studied and described by Hermann von Ihering in São Paulo. Ameghino’s contemporaries in Europe, Gaudry and von Zittel, also studied original fossil mammal material from Patagonia; Gaudry through the collections made by his employee Tournoüer and von Zittel through material sold to the Bavarian State Collec- tion in Munich by Ameghino. (Scott studied the type material from Patagonia in the Ameghino collection a little later, but after Ameghino’s death, and only type material of the younger Santacrucian.) 1.1 The tangled history of precocious hypsodonty 3

All four of these paleontologists (Ameghino, Gaudry, von Zittel, and Scott) were working with original fossils from Patagonia, but only three worked in positions that enabled them to make direct comparisons of material from different continents (Scott, Gaudry, and von Zittel), and of these three, only Gaudry and von Zittel benefitted by working directly with material from the older Cenozoic of Patagonia. Of these last two, only Gaudry (through the work of Tournoüer) had access to the stratigraphy and independent evidence from marine invertebrates (and global correlation) by which to make age assessments and intercontinental comparisons. But alas, nobody in the modern literature ever cites Gaudry as the originator of the idea of “precocious hypsodonty.” Why? Gaudry wrote in French, and language has a huge influence on citation history. For example, it explains why Patterson and Pascual (1968) are so often cited and Pascual and Odremán Rivas (1971) so often overlooked. Ameghino (1906) placed South American Notohippidae near the base of horse evolution, and noticed the implication that notohippid hypsodonty in Patagonia ante- dated the evolution of hypsodonty in northern hemisphere horses. However, the endemism and monophyly of Notoungulata in characters of the basicranium, revealed by Roth (1903), removed the precociously hypsodont Notohippidae from any direct phylogenetic affinity with true horses. More substantive evidence for an early occurrence of hypsodonty in South America was provided by Albert Gaudry (1903) and Andrés Tournouër (1903a, b) through a comparison of the European and Patagonian fossil mammal sequences. Using the new collections from Patagonia, Tournouër and Gaudry independently established the relatively older age of the deposits in Patagonia. Comparably high prevalences of hypsodonty among European mammals are attained only in much younger deposits. Tournouër (1903a, b) provided constraints on the age of the Patagonian sequence on the basis of the relationship of fossil-bearing continental units to marine beds along the Gulf of San Jorge. These marine beds contain rich and diverse fossils studied by French paleontologists at the Laboratoire, including molluscan taxa. On the basis of these studies, Tournouër and Gaudry concluded that the Notostylops and Pyrotherium beds could not be younger than l’Oligocène supérieur. Gaudry (1902, 1903) commented about the age relationships of the Pyrotherium and Santa Cruz faunas with respect to the le marche de l’évolution dans l’hémisphère boréal (the course of evolution in the northern hemisphere). Gaudry went beyond the evidence from marine fossils to note “jamais, à moins de recourir à l’étude des fossils marins places au-dessous, on n’aurait pu avoir l’idée de ranger dans le Miocène l’étage santacruzien où on ne trouve aucun Equidé ou aucun animal en voie de devenir Equidé” (without resorting to the study of marine fossils below, we would not have had the idea about placing the Santacrucian stage in the Miocene, as there are no equids nor any animal becoming an equid). Then, after a long list of such comparisons with the Miocene mammals of Europe, Gaudry concludes that “A en juger par les etudes faites dans nos pays, le Santacruzien devrait être du Tertiaire ancien, et pourtant e’est du Tertiaire relativement recent. La transformation des Mammifères en Patagonie s’est produite moins complètement que dans nos pays. Cela est d’un grand intérèt pour la paléontologie philosophique. L’évolution s’est avancée à travers des ages d’un pas 4 Hypsodonty in South America

inégal” (Judging by studies made in our country, the Santacrucian would be the older Tertiary, but it is relatively recent Tertiary. The evolutionary transformation of mammals in Patagonia was less complete than in our country. This is of great interest to philosophical paleontology. Evolution progresses through time at unequal rates.) (1903, p. 473). In the 1911 edition of the Grundzüge der Paläeontologie (Paläeozoologie). II. Abteilung, Vertebrata” (Text-book of Paleontology (Paleozoology), Part II, Vertebrata), Karl von Zittel, with F. Brioli, Ernest Koken, and Max Schlosser, summarized the middle Cenozoic sequence of Patagonia and provided a glimpse at broad patterns of crown height evolution among the notoungulates. Those of the Upper Eocene Notostylops beds were consistently brachydont, the notohippids of the Oligocene Astraponotus beds had moderate crown height, and the archaeohyracids had prismatic (apparently ever-growing) teeth, and by the Miocene Pyrotherium beds, the Typotheria and Toxodontia displayed complete elodonty. In the ﬁrst edition of A History of Land Mammals of the Western Hemisphere, William Berryman Scott (1913) argued that the explanation for high-crowned, persistently growing pattern of grinding teeth in horses, camels, ruminants, and rodents “is probably found in the spread of grassy plains at the expense of forests...[o]n account of the silica which they contain, the grasses are very abrasive and rapidly wear the teeth down. In adaptation to this new source of abundant and nutritious food, many kinds of mammals developed a form of tooth which was ﬁtted to compensate by growth for the loss through abrasion” (p. 233). Scott compared the Oligocene mammals of North and South America, and with respect to those of South America, wrote that a “large number of genera, especially among the toxodonts and typotheres...had high-crowned, cement-covered teeth...an indication that grazing habits had already begun to be prevalent” (p. 264) in the South American Oligocene. With respect to the older Eocene, Scott wrote that Casamayoran genera were “far more primitive and less specialized than their descendants in the Deseado and Santa Cruz stages. All of them had the low-crowned grinding teeth of the browsers, and no grazers were then in existence, so far as is known” (p. 282). He noted in passing that the mammals of the next successive level, the Astraponotus beds, or Mustersan, of either Eocene or Oligocene age, were scanty. At the same time, Scott (1913) explicitly establishes the greater antiquity of hypsodonty in Patagonia relative to North America (and Europe); he describes hypsodont teeth in general, and notes they occur in “many plant-feeders, such as horses, cattle, elephants, beavers, etc.” (p. 95). Note the diversity of mammals he includes in this statement. He goes on to note that “in very many instances the development of brachyodont into hypsodont teeth may be followed through every step of the change” and that “the advantage of the change is obvious in lengthening the animal’s life, especially in those which feed upon abrasive substances, like grass” (p. 95). In the second edition of A History of Land Mammals of the Western Hemisphere, Scott (1937a) acknowledges the fact of “prematurely specialized” Deseadan notoungulates “which had high-crowned (hypsodont), cement-covered teeth, and in which the 1.1 The tangled history of precocious hypsodonty 5

lower molars had a deceptively horse-like pattern (Rhynchippidae and Notohippidae). Next in frequency of occurrence were the Typotheria, of which many genera likewise had the hypsodont, cement-covered teeth” (p. 249). “This multiplication of grazing animals, with hypsodont, cement-covered teeth, is a very interesting parallel to the similar development which appeared in so many rodent, artiodactyls, perissodactyl and proboscidean families of the Miocene in the northern hemisphere, but the adaptation to grazing habits took place much earlier in South than in North America, from which fact it might be inferred that the extension of grasslands occurred much sooner in the southern continent.” (p. 249). He also noted that Mustersan (lower Oligocene or Eocene) Typotheria “were small animals and most of them had the hypsodont, rootless and cement-covered teeth” (p. 251). The idea of “prematurely specialized” hypsodont notoungulates in Patagonia was resuscitated in modern form for the English language audience by Patterson and Pascual in the late 1960s, and from that time forward, Pascual is the principal source of creative thinking about the environmental signiﬁcance of hypsodonty in Patagonia. Pascual argued that the cause of early hypsodonty in Patagonia may be related to (1) Andean tectonism and mountain uplift leading to change in physiographic conditions immediately after deposition of middle Eocene sediments (Pascual and Odremán Rivas, 1973), (2) the establishment of extensive herbaceous steppes and the early diversiﬁcation of grasses (Pascual and Odremán Rivas, 1971), and most recently, (3) the accumulation of pyroclastic sediments with abundant siliceous abrasives (Pascual and Ortiz-Jaureguizar, 1990). The two syntheses of Pascual and Odremán Rivas are seminal to the history of the growing complexity and sophistication of thinking about the environmental correlates of precocious hypsodonty in Patagonia.

1.1.2 Grasses

Fossil grasses were first discovered in Patagonia at the turn of the twentieth century (Dusen, 1899), but grasses are never a very prominent component of fossil macrofloras in Patagonia. Fossil grass leaves do not occur in any abundance in these classical floras, nor do they occur in circumstances that might have led paleobotanists to believe they indicated grasslands. For example, Berry (1925, 1928, 1934, 1937) described “Miocene” floras in Patagonia and his review cites all the available evidence for grasses; in sum, pitifully little. Hünicken (1955, 1966) studied the rich leaf floras of middle Eocene to Oligocene age along the Rio Turbio, and similarly found no grasses. Romero (1986b) reviewed the composition and environmental significance of the Patagonian floras and did not mention evidence for grasses. Most recently, Barreda and Palazzesi (2010) describe the composition and sequence of Cenozoic macrofloras and pollen records from Patagonia, and mention the oldest record of Poaceae at Rio Turbio during the Eocene and the oldest evidence of a more arid-adapted vegetation with grasses in low abundance in the early Miocene. Their review of the establishment of arid-adapted vegetation in Patagonia (2007) convinces the reader that grasses do not make a significant appearance in Patagonia until after the early Miocene. Grasslands do 6 Hypsodonty in South America

not appear in the pollen record of Patagonia until the Quaternary (Palazzesi and Barreda, 2012). Given there is little evidence from leaves or pollen for grasses in ﬂoras from Paleogene deposits in Patagonia, where did the evidence of early grassland evolution in Patagonia come from?

1.1.3 Phytoliths

The occurrence of phytoliths in Plio-Pleistocene sediments of the pampas of Argentina was established by Frenguelli (1930, 1955), Teruggi (1955, 1957), and Bertoldi de Pomar (1975). Their classification and affinities to modern plants were established by Bertoldi de Pomar (1970, 1971). The first mention of plant phytoliths in the Mustersan of the Sarmiento Formation of Patagonia was made by Renato Andreis (1972), and these were interpreted as grasses in light of known phytolith systematics at that time. Bertoldi de Pomar’s(1971) classification, while highly original, was based on descriptions of grass and monocot phytoliths then current in the botanical literature, and this literature had very limited phylogenetic scope. The insinuation of its implications into the literature about hypsodonty in the Patagonian fossil mammal record happened between 1970 and 1972. Spalletti and Mazzoni (1977) remarked that Andreis found evidence of escasas gramíneas (sparse grasses) because of “nidos de escarabéidos...requiere de superficies llanas libres de pastos” (flat exposures of soil free of grasses). The combination of tuffaceous sediments on a broad flat land surface, paleosol microstructure, the presence of dung-beetle brood balls and biogenic silica, together with high-crowned fossil mammals suggested that wide plains with a low vegetation of grasses became established during the Mustersan (Pascual and Odremán Rivas, 1971; Andreis, 1972). Luis Spalletti and Mario Mazzoni first mentioned the presence of phytoliths (ópalo biogénico) in the Sarmiento Formation at Gran Barranca in 1977 (1977) and noted “la notable abundancia de silicofitolitos (que contrasta con las deducciones de Feruglio, 1949 y Andreis, 1972), nos inducen a pensar–en coincidencia con las ideas de Pascual y Odreman (1971)–en amplias y temporalmente constantes estepas arbustivas” (p. 278). This is the first in a series of detailed studies of phytoliths in the dominantly windborne tuffaceous sediments of the Sarmiento Formation and the oldest clear interpretation of the phytolith evidence for widespread low shrubland steppe in the Patagonian Eocene. Later, from phytolith separations, Mazzoni (1979) established the presence of células de gramíneas (grass phytoliths), and described the diversity and relative abundance of a wide variety of distinct morphological classes of phytoliths. Alejandro Zucol and colleagues (1999, 2010) revised and updated the interpretation of the middle Eocene phytolith record from the Sarmiento Formation using Mazzoni’s original separations, and found that graminoid phytoliths rarely comprise more than 50% of assemblages, a remarkably low relative abundance for such productive plants. Nevertheless, Zucol et al. (2010) argued for the presence of grassland ecosystems in Patagonia during the middle Eocene. The evidence for this is a relatively higher proportion of diagnostic panicoid phytoliths in a single stratigraphic level, Simpson’s Y Tuff. This episodic occurrence of a relatively higher proportion of panicoid phytoliths 1.1 The tangled history of precocious hypsodonty 7

is the best available evidence for the establishment of grassland ecosystems in Patagonia in the late middle Eocene. Interestingly, this episode in Simpson’s Y Tuff occurred during the Barrancan South American Land Mammal Age, a time when no active evolutionary change in mammalian hypsodonty occurred, and seems to have been ephemeral at best, perhaps reﬂecting only the local inﬂuence of an important volcanic eruption event. Most recently, Strömberg et al. (2013) analyzed the phytolith content of the Sar- miento Formation at Gran Barranca, and while open-habitat grasses are indeed present, they are always at such low frequencies that there is no credible evidence for open grasslands or grassland ecosystems in the Sarmiento Formation anytime during the middle Cenozoic.

1.1.4 Grasses as sediment traps

Throughout the long history of ideas relating hypsodonty with grass diets, the grazing habit, grassy plains, or grassland ecosystems, there has been little mention of the role of grasses in the accumulation of erosion products or sediment deposition. Among the oldest published statements suggesting that intrinsic opaline silica abrasives in grasses may not be the sole cause of hypsodonty are those of Reuben Arthur Stirton who studied horse (1940, 1947) and beaver evolution (1935). Stirton believed hypsodonty was related more to soil ingestion than grass consumption (1947). Most recently, earth surface processes have been invoked in relation to hypsodonty by Reguero et al. (2010). “As is interpreted for all ungulates, the hypsodonty solve the problem [sic] of increased tooth wear resulting from various dietary and environmental factors: (1) high phytolith abundance in especially coarse grasses, (2) prevalence of grass life-forms with areas of exposed soil around them, (3) high levels of soil disturbance or soil mineral mobility, (4) large areas of continuously available accumulations of volcanic ash (and other potential sources of mineral dust) subject to erosion– entrainment–transport–deposition cycles extending over evolutionary timescales” (p. 366). This invocation of earth surface processes extending over evolutionary timescales by Reguero et al. (2010), without attribution or empirical substantiation, must rank as one of the most prescient claims ever made about the evolution of high- crowned teeth in South American mammals. However, the role of wind transport and trapping by grasses in the deposition of loessoid deposits in Argentina has long been recognized. “The wind-transported particles and grains which make up the loessoid deposits must have settled down slowly on the surface of the pampas, where they were trapped by a thick grass cover; the existence of this vegetation is shown in the sediments by the numerous siliceous cells found in all the levels of the Pampean Formation” (Teruggi, 1957; p. 330). Long before Reguero and Teruggi, the basic principles were recognized by William Diller Matthew in his description of the fossil mammals of the Tertiary of northeastern Colorado (1901): “In view of the important bearing that the origin of the sediments must of necessity have on the discussion of the character and relationships of the fauna found in them” (p. 360). Matthew argued for the eolian origin of the White River beds and 8 Hypsodonty in South America

invoked the interaction of eolian and fluvial surface processes. “I think too that the importance of river flood-plains as a source of [sediment] supply is likely to be underestimated. The areas [of exposure] are limited it is true, but the supply of sediment is unlimited and the conditions for sorting and removal by the wind are exceptionally favorable, if we take as example the modern rivers of the Plains. It should be remem- bered that while rivers bring large amounts they also take away large amounts, whereas whatever windborne sediment is caught in prairie grasses is not likely to escape again” (p. 363). Somewhat later, in the same paper he wrote “The sediments brought down by the various rivers from the mountains are deposited largely in the vast semidesert tract of eastern Wyoming, Colorado, and New Mexico. Here the prevalent westerly winds sift and sort them, rolling the sands but a short distance and leaving them as residual deposits, while all the finer material is carried much farther and caught by the grassy surface of the prairies to the east, finally merging perhaps into true flood-plain or lacustrine mud in the valley of the Mississippi. The denser the grass the more dust it sifts out and holds, hence the tendency to fill all lagoons and hollows, and bring the prairie surface to one uniform level...The fossils found in the loess are the fauna of the Plains...” (p. 367). Then he notes “the analogy of the clay fauna is with that of the modern plains...The species from the clays are comparatively small, slender-limbed, with much more advanced reduction in the lateral toes, and the ungulates have cropping incisors and comparatively hypsodont molars” (p. 371).

1.1.5 Mountain uplift and volcanism

The relationship between tectonism and volcanism is complex in Patagonia and all along the Andes and their influence on South American environments has been considerable throughout the Cenozoic. Thomas Falkner observed “the volcanoes, or fiery mountains, of the Andean cordillera in western Mendoza, and was witness to a vast ash cloud carried by the wind that spread over a great part of the jurisdiction of Buenos Aires, beyond the Rio de La Plata, and scattered on both sides of the river in so much that the grass was covered with ashes” (1774). Pascual and colleagues explored the possible causes and correlates of the evolutionary transformation of tooth crown shape and their discovery of a latitudinal gradient in hypsodonty (1985) and identified: (1) change in physical conditions related to the regional uplift that accompanied deposition of Mustersan age sediments, (2) the establishment of extensive herbaceous steppes, and (3) the deposition of pyroclastic sediments with abundant silicious abrasives (Pascual and Ortiz-Jaureguizar, 1990). Given there is not much discussion of volcanism and hypsodonty in the paleontology literature, how did Pascual come to his suspicion? In the words of Ortiz– Jaureguizar...“[A] Rosendo (y, por contagio, también a mi) lo le inquietaba era la diferente composición de las faunas mamalíferas de Patagonia y los sedimentos equivalentes del noroeste y el oeste argentino (Casamayorense, Mustersense y Divisa- derense de aquellos tiempos). Una de las principales diferencias (ya notada por 1.2 Explaining the prevalence of hypsodonty in South American mammals 9

Pascual en su trabajo de 1970 y en el escribieron luego con Odreman Rivas en 1973) es que los sedimentos mamalíferos al norte del río Colorado eran epiclásticos y los patagónicos piroclásticos. Y mientras en el norte los mamíferos eran predominante- mente braquiodontes, en Patagonia eran cada vez más hipsodontes. Consecuente- mente, era probable que los mamíferos patagónicos incrementasen la altura de sus molares como una respuesta a la presencia de sedimentos abrasivos que se incorpor- aban junto con el alimento” (Ortiz-Jaureguizar, personal communication, November 29, 2011). The idea that pyroclastic sediments played a role in the evolution of precocious hypsodonty is a uniquely South American contribution to the discussion about the possible and potential causes of tooth shape evolution.

1.2 Explaining the prevalence of hypsodonty in South American mammals

Formulating a plausible explanation for the precocious appearance and prevalence of high tooth crowns among South American mammals requires several things. First is an understanding of the prevalence of tooth structures for resisting abrasive wear among living mammals in South America. Geographic patterns of variation in the prevalence of hypsodonty can be amply demonstrated among living mammals. Among these mammals, special significance is given to sigmodontine rodents, recent immigrants into South America, which encountered the continent’s unique and varied environmental conditions and geography. The significance of their evolutionary accommodation to this physical reality will be explored using multivariate approaches. Second, a better understanding of the patterns and scale of geographic variation in the environment–crown height relationship in South America and in mammals around the world serves to identify the environmental conditions that are associated with it. Geographic coincidences are found among the prevalence of high tooth crowns, sources of environmental mineral abrasives, and the mechanisms that mobilize and transport these mineral particles. These coincidences lead to the proposition that earth surface processes, or more specifically, the intensity of soil erosion is the cause of much dental evolution, or mammalian herbivores, having evolved high-crowned teeth elsewhere for other reasons, once having acquired these adaptations, disperse into and exploit more marginal highly erosive environments. Third, to distinguish coincidence from cause, a more detailed review of what is known about tooth wear in mammalian herbivores and of the causal agents that underlay variation in excess tooth wear and tooth wear rates is undertaken. The record of tooth wear in sheep on the North Island of New Zealand and southeastern Australia reveals that tooth wear varies as a function of geographic distribution in the intensity of soil erosion. In addition to this geographic coincidence, tooth wear rates in sheep vary seasonally, annually, and at longer timescales consistent with the intensity of soil erosion. Seasonal variation in soil ingestion may be explained by reproductive demand and grazing density, but interannual variation is more difficult to explain except by invoking earth surface processes. The geographic and temporal patterns in tooth wear 10 Hypsodonty in South America

convincingly point to the primary role of soil ingestion in the otherwise complex etiology of excess tooth wear. Fourth, the findings at ecological timescales naturally lead to a set of expectations or predictions about what might be observed at evolutionary timescales in the fossil record. For these tests of the proposition, three examples are explored: (1) The fossil and rock record of mammalian herbivores on Mediterranean islands is examined where the independent evolution of high tooth crowns are a conspicuous feature of island history. These islands provide potential examples of the relationship between the rock record of volcanism and the earth surface processes known to drive tooth wear. (2) The potential universality of this finding is examined through a comparison of tooth wear rates among feral ungulate populations on oceanic islands where environments contrast in mineral soil substrate, the style and intensity of surface erosion, and the climate variables that mobilize and transport mineral particles. (3) Comparisons of tooth wear rates can be made between forested and non-forested islands, between islands with mineral soils and with organic soils, and contrasts between feral herbivore species traditionally classified as browsers and grazers. These contrasts point to earth surface processes, specifically the amount and type of exposed mineral soil at the surface, the susceptibility of the land surface to erosion, and the intensity of erosion, as contributors to the observed variation in tooth wear rates. Fifth, better examples are found in the East African Plio-Pleistocene, where a marine record of soil erosion intensity can be coupled directly to the terrestrial record of evolutionary change in tooth structures. Here again, the coincidence of mountain uplift and volcanism in the Rift System and a record of surface denudation preserved in the sediments on the floor of the Indian Ocean, provide a detailed temporal record of the intensity of erosion. When this record of soil erosion intensity is compared directly with evolutionary rates of change in tooth shape among diverse mammalian lineages, temporal coincidences indicate that threshold levels of atmospheric particle flux trigger evolutionary response. These diverse examples appear to confirm the proposed model for the environmental causation of some important structural features of mammalian tooth shape evolution. These findings are then related back to the fossil and rock record of South America, and specifically the Eocene–Oligocene transition in Patagonia and the southern oceans. In the fossil record at Gran Barranca in Patagonia is found evidence for multiple species undergoing independent and simultaneous evolutionary increase in tooth crown height. There were three episodes in this history. The first or oldest occurred through a one- million-year interval in the late middle Eocene in at least three monophyletic families of native herbivores at a time of significant local environmental change. The explanations for these are found to relate to the intimacy of terrestrial environments in Patagonia to oceanographic and atmospheric conditions associated with the circum-Antarctic current and West Wind Drift through the later Eocene and into the Oligocene, and their influence on widespread surface accumulations of volcanic ash. Finally, I explore the significance of ever-growing teeth. I review the evidence for their evolution in South American mammals, their evolutionary and developmental morphology, possible explanations for their evolution and prevalence, and then their 1.2 Explaining the prevalence of hypsodonty in South American mammals 11

consequences. I argue that ever-growing teeth are truly evolutionary marvels, and their possible and potential impact on the Earth may be far greater than we know now. The inspiration for this assertion arises out of the success of rabbit introductions and eradications around the world, their consequences in Australia and New Zealand and on small volcanic and non-volcanic islands, their fossil record in North America, and the evolution and environmental impact of rabbit-like notoungulates in South America. This discussion closes with a description of the evolutionary and current ecology of the Vicugña, an example of the evolution of ever-growing teeth among artiodactyls on an orographic island. 2 Hypsodonty in the South American fossil record

2.1 Background

Numerous South American mammal clades underwent evolution of tooth structures for resisting abrasion. These structures were of many kinds, including increasing enamel hardness by change in enamel microstructure (Sander et al., 1994; Vieytes, 2003)and adding tooth mineral substance in the form of enamel laminae (Vucetich et al., 2005; Deschamps et al., 2007). Here, I am interested in examples of the evolutionary increase in tooth crown height, particularly in the premolar and molar tooth row. The South American fossil mammal record documents many examples of morphological transition to higher tooth crowns during the Cenozoic (Table 2.1). Despite the apparent prevalence, no one has attempted to tally all the examples. In part, this deficiency reflects the fact that broad generalizations other than coincident timing, imply complexities in the interaction of habit (behavior) and habitus (environment), likely peculiar to each group. The taxonomic breadth of examples and the range of morphologically peculiar solutions make it difficult to express the structural character of the adaptation in a consistent way, let alone find homologous landmarks for measurement and comparison. Furthermore, the fickle nature of the fossil record always leaves us prospecting for more complete fossil sequences, so that any claims about evolutionary transformation rest on firmer evidence. Causal relationships with any particular environmental agent are exceedingly difficult to establish in the fossil record. As for a unitary explanation, how do we attempt such a thing? First, what constitutes an example of the evolution of high tooth crowns? Examples of the evolutionary transition can be found among closely related taxa within a clade that display unidirectional increase in tooth crown height (morphological character states in ascending order from low- to high-crowned) through time consistent with stratigraphic superposition or geochronological order of appearance. Substantiating these hypothetical cases requires familiarity with (1) the morphological evidence, (2) the stratigraphic context of the record, (3) the taxonomy and phylogeny of the clade, and (4) the preservation biases that shape the record. What can be learned from a simple list of all the examples? To start, just how prevalent is the actual record, and does the tally confirm the subjective impression that there were times and/or places when such transitions were more frequent? The compilation suggests there may have been periods or intervals of relatively more intense evolutionary change. The oldest interval must have occurred sometime before the 12 2.1 Background 13

middle Eocene and involved two or three non-therian mammal groups and possibly basal Xenarthra. The appearance of three taxonomically distinct non-therian mammals with high-crowned teeth (Sudamericidae, another perhaps related gondwanathere clade, and Dryolestida) is a striking feature of the earliest mammal record of South America. With respect to the major groups of xenarthrans (the two cingulate groups Glyptodontoidea and Dasypodoidea, and Tardigrada plus Pseudoglyptodon), it is not known whether they evolved ever-growing crowns independently or whether this trait appeared only once in a common ancestor. The fossil record only establishes that each of these three groups had euhypsodont and enameless (or nearly enameless, see Simpson, 1932) teeth in their oldest known representatives Machlydotherium, Uetatus,andPseudoglyptodon, respectively, in the middle and late Eocene. There may have been a long period of active evolution prior to their oldest known occurrences, as the molecular clock suggests an age of divergence between Tardigrada and Cingulata sometime before the Cenozoic (Delsuc, 2004). A possible second interval of noteworthy increase in molar crown height involved primarily the Notoungulata, but also some Marsupialia (Goin et al., 2010) and caviomorph rodents (Chinchillidae, Cephalomyidae, and Dasyproctidae) in the fossil record of Patagonia. This interval of “precocious” hypsodonty began in the late middle Eocene (at the Barrancan–Mustersan transition) and ended around the late Oligocene (Desea- dan). Some of these groups almost certainly evolved hypsodonty in Patagonia, but among Notoungulata, at least two clades (Hegetotheriidae and Mesotheriidae) were euhypsodont at their ﬁrst appearance in Patagonia. Their sudden appearance without antecedents suggests they attained this stage of evolution sometime before the Deseadan and perhaps somewhere outside of Patagonia. The Patagonian fossil record suggests that three clades (or families) of caviomorph rodents diverged before the Oligocene (Deseadan). The oldest representatives of these clades (Scotamys, Cephalomys,andIncamys) were either protohypsodont or close to it when they appear in the Patagonian fossil record, and this suggests the morphological transformation(s) probably occurred somewhere else. Molecular phylogenies for Caviomorpha resolve the divergence date for Chinchillidae and Dasy- proctidae and judging from estimates of the age of the arrival of caviomorphs into South America (Vucetich et al., 2010; Antoine et al., 2011), the evolutionary transformation to higher crowns could not have occurred much before the late Eocene (Poux et al., 2006). Evidence from the Central Andes and northwestern Argentina suggests tectonism and volcanism were active at the time these groups evolved high-crowned teeth (Horton et al., 2002; Dávila and Astini, 2007;DeCelles et al., 2007). A third apparent cluster of clades that evolved high-crowned molars is found in the middle to late Miocene of Patagonia from about the Colhuehuapian (20 Ma) to the Colloncuran (15.7 Ma). This interval saw the evolution of euhypsodonty in Toxodonti- dae (Figure 2.1) (with perhaps the Xotodontinae providing an independent example within Toxodontidae), Argyrolagidae and Patagoniidae (perhaps representing a single Table 2.1 Clades of South American fossil therian mammals with ﬁrst appearances of dental specializations of hypsodonty and elodonty in the premolars and molars 14

Locality and SALMA Age of FAD of oldest Genus and species Age of earliest known Oldest known at ﬁrst appearance of protohypsodont taxon FAD for hypsodonty in acquisition of rootless taxon with Clade hypsodonty in clade (Ma) clade or elodont molars (Ma) elodont molars Sources

1 Archaeohyracidae Cañadon Vaca (Vacan >43 Eohyrax rusticus NA – 1 (Notoungulata) SALMA) 2 Hegetotheriidae Cabeza Blanca (Deseadan ca 26 Propachyrucos ?26 Propachyrucos 1 (Notoungulata) SALMA) Prohegetotherium Cabeza Blanca Prohegetotherium (Deseadan SALMA) 3 Interatheriidae GBV-3 El Rosado, Gran 38.0–38.2 cf Eopachyrucos 21.1–23.4 Progaleopithecus 2 (Notoungulata) Barranca (Mustersan La Flecha tournoueri SALMA) (Deseadan SALMA) 4 Mesotheriidae GBV-19 La Cantera, Gran <30.77 cf Trachytherus >30–31.5 Trachytherus 3 (Notoungulata) Barranca 5 Notohippidae GBV-4 La Cancha, Gran 33.58 Eomorphippus 20–21 (Colhuehuapian Argyrohippus 4 (Notoungulata) Barranca (Tinguirirican obscurus SALMA) fraterculus SALMA) 6 Toxodontidae Cabeza Blanca (Deseadan ca 26 Proadinotherium 15.8 (Colloncuran Palyeidodon 5 (Notoungulata) SALMA) leptognathum SALMA) obtusum 7 Xotodontinae Middle Rio Santa Cruz, unknown Hyperoxotodon >15.8 (Colloncuran Hyperoxotodon 5 (Toxodontidae; also Cape Fairweather speciosus SALMA) speciosus Notoungulata) (Santacrucian SALMA) 8 Astrapotheriidae Pinturas Fm (“Pinturan” 16.5–18.75 Astrapothericulus NA – 6 (Astrapotheria) SALMA) iheringi 9 Argyrolagidae Curandera II ca 31.5 Proargyrolagus ca 20 Anargyrolagus 7 (Metatheria) (Tinguirirican SALMA) Gaiman primus (Colhuehuapian SALMA) 10 Patagoniidae Gaiman (Colhuehuapian ca 20 ? ca 20 Patagonia 8 (Metatheria) SALMA) Gaiman (Colhuehuapian SALMA) 11 Eocardiidae- Cabeza Blanca and GBV- >26 Chubutomys simpsoni 16–15.8 Eocardia spp. 9 Caviidae1- 19 La Cantera (Deseadan (Santacrucian Hydrochoeridae SALMA and earlier) SALMA) (Caviomorpha; Rodentia) 12 Ctenomyinae Chasicoan SALMA 9.1–9.4 Ma Chasichimys (Huayquerian Palaeoctodon 10 (Octodontidae2; SALMA) simplicidens or Caviomorpha; Xenodontomys Rodentia) ellipticus (i.e., >1) 13 Octodontinae Huayquerian SALMA 9.1–9.4 Ma Phtoramys All known taxa are – 11 (Octodontidae; elodont Caviomorpha; Rodentia) 14 Adelphomyinae Colhuehuapian SALMA 20–21 Prospaniomys NA – 12 (Echimyidae; Caviomorpha; Rodentia) 15 Eumysopinae3,4 Huayquerian SALMA 9.0–6.8 Reigechimys NA – 13 (Echimyidae; Caviomorpha; Rodentia) 16 Cephalomyidae Lacayani and Cabeza 26 Cephalomys arcidens ca 26 Cephalomyiopsis 14 (Caviomorpha; Blanca (Deseadan hypselodontus Rodentia) SALMA) 17 Dasyproctidae Salla (Deseadan SALMA) 26 Incamys bolivianus NA – 15 (Caviomorpha; Rodentia) 18 Erethizontidae Gaiman and Gran 20–21 Hypsosteiromys NA – 16 (Caviomorpha; Barranca (Colhuehuapian (mesodont) Rodentia) SALMA) 19 Chinchillidae Tinguiririca (Tinguirirican >31.5 Undescribed ca 26 Eoviscacia 17 (Caviomorpha; SALMA) and Lacayani Chinchillidae Gen et australis Rodentia) and Cabeza Blanca sp nov.; Scottamys (Deseadan SALMA) antiquus 20 Dinomyidae5,6 (Mayoan SALMA) 11.8 Simplimus Huayquerian Many taxa 18 (Caviomorpha;

15 Rodentia) Table 2.1 (cont.) 16

21 Neoepiblemidae5,7 (Deseadan SALMA) 26 Perimys All known taxa are Perimys 19 (Caviomorpha; Neoepiblema elodont Rodentia) Dabbenea 22 Sigmodontinae Montehermosan (Farola 4–5(<5.3) Auliscomys formosus NA – 20 (Muroidea; de Monte Hermoso) Rodentia) 23 Tardigrada ? ? ? 38.0–38.2 Pseudoglyptodon 21 (Xenarthra) (Mustersan SALMA) 24 Glyptodontoidea ???<30.77 aff 22 (Cingulata; (La Cantera) Machlydotherium Xenarthra) 25 Dasypodoidea ???39–41.7 Utaetus buccatus 23 (Cingulata; (Barrancan SALMA) Xenarthra) 26 Sudamericidae Punta Peligro (early 61–62.5 Sudamerica NA 24 (Gondwanatheria) Paleocene, Peligran) ameghinoi 27 Gondwanatheria Los Alamitos (Alamitan) 75 Ferugliotherium NA 25 (Campanian, late windhauseni Cretaceous) 28 Dryolestida Los Alamitos 75 Leonardus NA 26 (Campanian, late cuspidatus Cretaceous)

FAD, ﬁrst appearance datum; SALMA, South American land mammal age. 1 Caviidae are direct descendants of Eocardiidae. Eocardiidae acquired elodonty in the Santacrucian. 2 Platypittamys may not be an Octodontidae. If excluded from the family, Octodontidae appear in the fossil record in the Huayquerian. 3 This clade becomes very hypsodont with Reigechimys in the Huayquerian. 4 Protadelphomys is not an Echimyidae, but rather Octodontoidea incertae sedis. 5 Neoepiblemidae and Dinomyidae are Chinchilloidea. 6 Dinomyidae FAP of hypsodonty in the Mayoan, FAP of elodonty in the Huaquerian (many genera). 7 Neoepiblemidae FAP is Scotamys from the Deseadan at Cabeza Blanca and is elodont. Notes on ages: age of Salla (Deseadan SALMA), 25 Ma; age of Colloncuran SALMA, 15.8 Ma; age of Cabeza Blanca (Deseadan SALMA) unknown but assumed to be 26 Ma; age of Gaiman (Colhuehuapian SALMA) uncertain but assumed to be about 20 Ma; age of Huayquerian SALMA unknown. Sources: 1 Reguero, 1998 2 Simpson, 1967 3 Reguero and Prevosti, 2010 4 Shockey, 1997a 5 Madden, 1990 6 Kramarz and Bellosi, 2005; Kramarz et al., 2010 7 Carlini et al., 2007; Kay et al., 2008 8 Pascual and Carlini, 1987; Kay et al., 2008 9 Ameghino, 1887; Wood and Patterson, 1959 10 Verzi, 2001, 2002; Verzi and Olivares, 2006; Verzi et al., 2008 11 Verzi, 2001 12 Vucetich et al., 2010 13 Verzi et al., 2008, 2011 14 Vucetich, 1989 15 Hoffstetter and Lavocat, 1970; Patterson and Wood, 1982 16 Patterson, 1958; Candela and Vucetich, 2002 17 Vucetich, 1989; Flynn et al., 2002, 2003 18 Mones, 1981; Vucetich et al., 1999 19 Wood and Patterson, 1959 20 Pardiñas and Tonni, 1998; Verzi and Montalvo, 2008 21 McKenna et al., 2006 22 Carlini and Ciancio, personal communication 23 Simpson, 1932; Bergqvist et al., 2004 24 Koenigswald et al., 1999; Pascual et al., 1999 25 Bonaparte, 1990; Krause, 1993; Pascual and Ortiz-Jaureguizar, 2007 26 Chornogubsky, 2011 17 18 Hypsodonty in the South American fossil record

1 23

2 A D 3

4 1 2 3 1 2

B E 4

1 cm

3 1 2

1 2

C F 3

Figure 2.1 Hypothetical evolutionary transformations to hypsodonty (right) and ever-growing molar crowns (left) among Patagonian Miocene Toxodontidae (Notoungulata). Left, lingual and occlusal aspects of mandibular tooth series for Adinotherium ovinum MLP 55-XII-13-79 (A), Hyperoxotodon speciosus MCZ 8532 (B), and Toxodontidae indet (MNHN(Ch)/DU ﬁeld number 87–288 (C). Right, occlusal, mesial, lingual, and buccal aspects of maxillary M1 or M2 crowns for Proadinotherium leptognathum FMNH P14714 (D), P. muensteri FMNH P13524 (E), and Nesodon imbricatus (F).

clade Argyrolagoidea), and a third clade encompassing the morphological transformation in Eocardiidae and Caviidae. This interval is particularly interesting as these groups attained euhypsodonty (or as I prefer, elodonty), a deﬁnitive solution to the problem of high rates of tooth wear and levels of abrasives in the diet. Elodonty may have been as signiﬁcant an evolutionary breakthrough for these rodent and notoungulate clades as it appears to have been for xenarthrans. That is, once evolved, it remained a characteristic feature of these groups. What grand geologic processes are coincident 2.2 Hypsodonty as a feature of notoungulate evolution 19

with the transformation to elodonty during this interval? The paleogeography of Patagonia (Ardolino et al., 1999; Malumian, 1999) suggests a combination of restricted geographic area by the Monte León marine transgression, wide and expanding geographic distribution of predominantly pyroclastic sediments (Trelew Formation, Colhue-Huapi Member of the Sarmiento Formation, Pinturas Formation, and Collon- Cura Formation), and conspicuous lithostratigraphic evidence of active Andean orogeny in the Rio Zeballos Group, Santa Cruz Formation, and Pedregoso Formation and its equivalents. A last interval of conspicuously increasing crown height began in the late Miocene and extended through the Great American Biotic Interchange. This involved the caviomorph rodent clades Ctenomyidae and Octodontidae (perhaps the same clade, Figure 2.2) that evolved elodonty, some early Sigmodontinae (Figure 2.3), and perhaps Vicugna (Camelidae). Sigmodontinae first appear in the Huayquerian and by the Montehermosan they are protohypsodont (Verzi and Montalvo, 2008). This interval appears to coincide with an acceleration in uplift in the Central Andes and environmental change that included intense pyroclastic volcanism (Trumbull et al., 2006), aridification, and unroofing leading to generally accelerated sedimentation rates along the foot of the eastern Andes (Gregory-Wodzicki, 2000; Anders et al., 2002; Garzione et al., 2008; Hoorn et al., 2010). One inescapable feature of the South American fossil record deserves special consideration: elodonty (or euhypsodonty). Half of the clades that evolved hypsodonty went on to evolve elodont or ever-growing teeth. No other mammalian fossil record from any other continent or landmass documents as many examples of the evolution of ever- growing teeth.

2.2 Hypsodonty as a feature of notoungulate evolution

2.2.1 The tooth

The tooth is an organ with a developmental unfolding, a genetically determined arrangement of mineral substances we identify as definitive unworn tooth shape, and a functional lifespan. The evolutionarily significant shape of a tooth includes all three aspects of these living structures. Teeth are complex and tooth structure can be adequately visualized only by 3D microtomography, although through cross-sections (occlusal surface or plane of wear) we can understand something of its internal architecture. Without these methods, we observe only the shape of the surface of the crown, and this is what is usually understood as tooth shape. The unworn surface, assumed to be the most informative stage of tooth development for phylogenetics, is assumed to be the genetically determined phenotype. It is usually a brief passing stage in the functional shape of a tooth. The more comprehensive and evolutionarily significant developmental and functional shape of a tooth can be revealed only through longitudinal study or pseudo-longitudinal reconstruction. 20 Hypsodonty in the South American fossil record

Figure 2.2 A particularly well-documented evolutionary transformation to an ever-growing tooth in late Miocene Octodontidae and Ctenomyidae of Western Argentina. (From Verzi (2001) with permission from Springer Science and Business Media.) 2.2 Hypsodonty as a feature of notoungulate evolution 21

Figure 2.3 The prevalence of high-crowned teeth extends to groups of mammals that arrived into South America at least six million years ago as participants in the Great American Biotic Interchange (Verzi and Montalvo, 2008). These include the very small mouse-size Sigmodontinae (Muridae). Left, Andinomys edax (USNM 541807) from near Putre, Tarapaca, Chile. Right, Reithrodon auritus (USNM 084196) from Cordilleros, Argentina.

Following its developmental unfolding, and eruption, the tooth enters into occlusion and immediately begins to wear. Thus, the unworn surface of a tooth is transitory and a momentary stage in the longitudinal history of the organ. While tooth wear may begin in utero (as attrition), abrasive wear normally begins following eruption of the crown through the gingiva and at the initiation of active occlusion against an opposite tooth or keratinous pad. With advancing age, the plane of wear descends progressively downward through the mineral substance of the tooth. In the mastication of soft foods, most wear is the result of attrition (tooth wear produced by the abrasion of enamel prisms that are deﬂated off the enamel surface). Food and oral chemistry act on the enamel and entire tooth mineral surface and when upper and lower tooth surfaces make contact during occlusion, enamel prisms are detached from the surface and become abrasive particles. In the mastication of abrasive foods or mineral particles on foods, tooth wear occurs through abrasion, in addition to attrition. Abrasion is the process whereby extrinsic abrasives in and on food lead to excess tooth wear in herbivores, especially those that feed close to the surface of the ground. The evolutionary unit of genotype and phenotype is the population and the unit of selection is the individual. While the failure of individual crowns can lead to premature mortality, the dentition (not individual tooth positions) is usually where tooth functional longevity is determined. In the dentition, the wear of individual tooth positions is summed. The sequential succession of crown formation, eruption, and wear along the premolar and molar rows serves to prolong the functional longevity of the dentition. It is my impression that either the largest or last tooth to erupt and enter into wear is usually the last to have its enamel or mineral substance exhausted and be expended. Thus, in 22 Hypsodonty in the South American fossil record

order to increase the reproductive life of the individual, natural selection will target the largest tooth preferentially, and structural enhancements through evolution will be first evident at this tooth position. It is surprising, but true, that geographic and temporal variation in tooth wear is rarely the subject of investigation in the evolutionary biology of tooth shape. Yet we will see that functional longevity varies temporally and geographically. Within the geographic range of a population, you find faster and slower rates of tooth wear, and rates of tooth wear can be mapped as an adaptive surface the peaks and valleys of which correspond with variation in the agents that cause tooth wear. Those agents may involve the response of plant tissues to the physical environment as expressed in their physical properties, or as I will argue, the adaptive surface most significant for excess tooth wear is variation in the abundance and availability of abrasive mineral particles. When excess tooth wear (or crown failure following the loss of structural integrity) truncates reproductive lifespan, natural selection operates by experimenting with developmental and structural solutions to prolong functional longevity. These adaptations may be expressed as (1) change in the developmental timing of crown formation, (2) the timing of tooth succession and eruption, or (3) change in the structural arrangement of tooth mineral substance. In general, tooth shape is the evolutionary solution to excess tooth wear, crown structural weakening, and eventually crown failure by the delivery of tooth mineral substance to the occlusal table. In normal tooth development, the enamel crown develops and at some point during development, enamel mineralization ceases and root formation begins. The moment in ontogeny when the enamel crown ceases to mineralize and root formation begins is termed the “onset of root formation.” The ontogenetic (or developmental) delay in the onset of root formation has huge consequences for tooth shape, as it is the mechanism whereby tooth crown height is increased evolutionarily. While the onset of root formation is progressively delayed, active enamel deposition and mineralization continues, and as the interval of active crown formation is lengthened, tooth crown height increases. When the onset of root formation is delayed beyond the somatic life of the individual (as reflected by the functional life of the tooth crown), we call the structural result an “ever-growing” or elodont (or sometimes hypselodont or euhypsodont) tooth. All these terms for ever-growing teeth are essentially synonyms. Thus, the evolutionary transformation from low-crowned to mesodont, hypsodont, and eventually the elodont tooth occurs as a consequence of the progressive delay of the “onset of root formation.” This ontogenetic delay is an example of heterochrony, and more specifically, pedomorphosis, the prolongation of juvenile stages of crown formation into later stages of development and somatic life.

2.2.2 The tooth in notoungulates

The fossil record of mammalian tooth shape evolution has natural limitations as a consequence of preservation biases and discontinuity. However, on occasion, the fossil record provides exceptional examples of evolving lineages documenting the progressive evolution of higher tooth crowns. For example, in South American notoungulates, the 2.2 Hypsodonty as a feature of notoungulate evolution 23

ACCESSION M1F1 M1F2 M1F3 M1F4M2F1 M2F2 M2F3 M2F4 M3F1 M3F2 M3F3 M3F4 YPM(PU) 15746 MLP AMNH 9243 YPM(PU) 60 YPM(PU) 15252 YPM(PU) 15135 AMNH 9493 AMNH 9234 YPM(PU) 15336 dP2 dP3 AMNH 9288 YPM(PU) 13188 50 AMNH 9493 YPM(PU) 15338 dP4 M1 M2 M3 YPM(PU) 15305 YPM(PU) 15141 AMNH 9168 1 cm YPM(PU) 15257 UCMP 26641 40 5 cm YPM(PU) 15215 YPM(PU) 15208 YPM(PU) 15492 AMNH ?9533 YPM(PU) 15488 AMNH 9128 AMNH 9533 30 AMNH 9192

AMNH 9198 Maxillary molar crown length (mm) YPM(PU)15256 FMNH P13076 YPM(PU) 16029 YPM(PU) 15967 YPM(PU) 15335 Increasing wear

Figure 2.4 Nesodon imbricatus (Toxodontidae, Notoungulata) wear stage seriation of four enamel features (folds and fossettes) on each maxillary molar (left), plot of changing tooth size with increasing wear (middle), and maxillary deciduous and permanent premolar and molar occlusal patterns (right). Plot of tooth size for M1 (closed circles), M2 (closed triangles), and M3 (closed boxes). Maxillary tooth rows (from top to bottom) for YPM(PU) 15354; YPM(PU) 15746; AMNH 1896; YPM(PU) 15135; YPM(PU) 15257; YPM(PU) 16029. most conspicuous evolutionary change seems to be expressed as an ontogenetic delay of the onset of root formation. There are many examples among notoungulates of change in the relative timing of root development with respect to somatic development, or heterochrony. Because developmental timing cannot be measured with much precision in fossil taxa, we resort to comparing tooth developmental stages against a reconstructed population average functional longevity. Functional longevity is recreated from tooth wear series by seriation (the ordering of individuals by stage of wear). The relative timing of developmental events within the arc of functional longevity of the crown can be established by reference to this seriation. In Miocene Toxodontidae, we can establish the onset of root formation in relation to wear stage, and note that root formation begins at more advanced wear stages in Nesodon than in its presumptive ancestor Proadinotherium. Unlike in Proadinotherium, single isolated crowns of Nesodon do not preserve the complete crown. Instead, because of the greater crown height of Nesodon, a complete molar crown from unworn apex to completely formed roots must be reconstructed from isolated crowns of several different individuals (see Figure 2.4). This constitutes evidence for the developmental and evolutionary delay in the “onset of root formation.” In Patagonian Toxodontidae, the ﬁrst stage in the evolutionary transformation to ever-growing molars begins with Proadinotherium leptognathum in the late Oligocene–early Miocene Deseadan, progresses through P. muensteri in the Colhuehuapian and Nesodon (or Adinotherium)in the Santacrucian, and terminates hypothetically with Palyeidodon obtusum in the middle Miocene or Colloncuran. In Nesodon, the M3 crown is the largest molar and the tallest (or highest) among the molars. Occlusal surface features of the M1 crown are obliterated by wear at an earlier stage of wear than M2 or M3, and M3 retains its occlusal surface features into the most advanced wear stages. 24 Hypsodonty in the South American fossil record

Proadinotherium Palyeidodon

Figure 2.5 Maxillary molar tooth wear series for Miocene Toxodontidae (Notoungulata), Proadinotherium leptognathum (left) and Palyeidodon obtusum (right). Proadinotherium leptognathum tooth rows from top to bottom; FMNH P14714, FMNH P14714, composite of FMNH P13581 and P14670, FMNH P13615, FMNH P14712, and FMNH P14714. Palyeidodon obtusum tooth rows from top to bottom; MNHN(Ch)/DU field number 87–346, MLP 46-VIII-21-10, MNHN(Ch)/DU field number 87–347, MNHN(Ch)/DU field number 89–195, MLP 40-VIII-9-3. Scale bars ¼ 1 cm and 5 cm.

The last stage in the transformation, the attainment of elodonty is marked by the appearance of Palyeidodon (15.8 Ma) in the Colloncuran. Palyeidodon is known from Bolivia and Patagonia, and is a presumed descendant of Nesodon. The age of the ﬁrst appearance of Palyeidodon is well dated in Patagonia, but less well constrained by radioisotopic dating in Bolivia (Saint-Andre, 1994). That Palyeidodon had evolved ever-growing molars can only be established by the absence of any evidence of root formation at the base of the molar crowns in all known material (Figure 2.5). Palyeidodon appears in the fossil record in Patagonia at the same time as Hyperoxotodon, another toxodontid with ever-growing molars. Hyperoxotodon is the basal taxon (oldest known and most plesiomorphic) of a distinctive clade of Toxodon- tidae, the Xotodontinae (Figure 2.6). Hyperoxotodon appears in the fossil record at the base of this clade without any suitable ancestor or morphological intermediate between it and its sister-taxon. Thus, xotodontines may have evolved ever-growing crowns elsewhere in South America. Coincidentally, in the same deposits in Patagonia, a third taxon of Toxodontidae appears with ever-growing molars (see Figure 2.1c). This may constitute evidence that a third clade of toxodontids, perhaps related to Adinotherium, evolved ever-growing teeth. 2.3 Hypsodonty in the middle Cenozoic of Patagonia 25

Figure 2.6 Tooth wear series in the ever-growing crowns of Hyperoxotodon (Xotodontinae, Toxodontidae) from the middle Miocene of Patagonia. Left, maxillary premolar and molar series for Hyperoxotodon; (A) partial M1 or M2 of MNHN(Ch)/DU ﬁeld number 87–241; (B) P2-P3, M1-M3 of “Nesodonopsis burckhardti” MLP 12-2909; (C) P4-M3; (D) P3-M2 of MCZ 8532; (E) M1-M3 of MLP 12-59; (F) M2-M3. Right, mandibular cheek teeth of Hyperoxotodon speciosus; (G) occlusal surface and pulp cavity outlines of p3-m3 of “Nesodonopsis sp.” MLP 54-IV-22-1; (H) p2-m3 of “Nesodonopsis burckhardti” MLP 12-1901; (I) occlusal surface and pulp cavity outlines of m1 or m2; (J) p3-m1 of MCZ 8532.

2.3 Hypsodonty in the middle Cenozoic of Patagonia

2.3.1 The problem

Ameghino (1904, 1906) discovered that the Mustersan was the oldest fauna distinguished by “la aparición independiente, en varias líneas de Ungulados, de géneros cuyos molares presentan una tendencia muy acentuada hacia la hipselodoncia” (Ame- ghino, 1906, p. 593) (Figure 2.7). Patterson and Pascual (1968, p. 434) summarized the basic facts by highlighting “the precocity shown by certain ungulates in the acquisition of high-crowned, or hypsodont, and rootless, or hypselodont, teeth. Notohippids by mid-Eocene time were as advanced in this respect as equines were in the early Pliocene, about 30 million years later. By the Deseadan such teeth had been acquired by no fewer than six groups of ungulates, large and small, and this number stayed fairly constant through the Tertiary. Students of South American mammals are familiar with this situation. Some of them have commented on it, but the fact is not as widely known as it should be.” While Cifelli (1993) did not use any explicit character describing crown height in his phylogenetic analysis of family-level afﬁnities among Notoungulata, tooth crown height is a character often included in phylogenetic analyses. For example, among 26 Hypsodonty in the South American fossil record

Pleisoxotodon Toxodon

Toxodon Toxodontidae Andinotherium “rotundidans” Gronotheriun Santacrucian

Nesodon

Adinotheriun Nesodontidae Proedinotherium muensteri Colhuehuapian Proadinotherium

Eomorphippus

Acoelohyrax Proadinotherium leptognathum Deseadan

Eohyrax Archaeohyracidae

Paracoelodus Acoelohyrax coronatus

HyracoideaAcoelodus Toxodontia upper Notostylops

Oldfieldthomasia

Acoelodidae Eohyrax praerusticus Archaeopithecus upper Notostylops

Condylarthra Selenoconns

Protungulata

Figure 2.7 Florentino Ameghino’s 1904 discovery of the precocious evolution of high- crowned teeth in the maxillary premolars and molars of notoungulates. (Redrawn from Ameghino 1904.)

Toxodontidae, Madden (1990) found crown height to vary across taxa in both the incisors and cheek teeth, and apparently, different tooth positions evolved the rootless condition at different times in the phylogenetic history of the family. Five characters (out of 39 in total) were used to capture this variation, including the relative crown height of the first upper molar, lower first incisor, lower second premolar, lower fourth premolar, and lower first molar. The impression was that each of these tooth positions attained hypsodonty and elodonty at different times. In each of these characters, character states were brachydont, mesodont, hypsodont, or ever-growing, and in 2.3 Hypsodonty in the middle Cenozoic of Patagonia 27

phylogenetic analysis, these five characters relating to crown height were predefined as ordered character types. Hitz (1997) in an analysis of typotherian notoungulate affinities with special emphasis on Interatheriidae, used a three-state expression of maxillary posterior premolar and molar crown height (brachydont, hypsodont, and hypselodont), and used the same character in a later analysis of Interatheriidae (Hitz et al., 2000). Hitz characterized Santiagorothia as hypsodont (with closed roots), the same condition observed in Eopachyrucos (Reguero, 1998). All Deseadan and younger interathere taxa are elodont, whereas all basal interatheriids are brachydont (including two non-interatheriine taxa from the Tinguirirican of Central Chile). Reguero (1998), in his analysis of phylogeny of typotherian notoungulates, used three discrete states to describe molar and upper central incisor crown height. For molars, the states are brachydont, mesodont (moderately high-crowned), and hypsodont (very high-crowned). In his discussion of variation in this character, Reguero observed that in Archaeohyracidae the molars are generally very high-crowned but rooted, whereas in Interatheriinae they are ever-growing. In older and more primitive forms such as Eopachyrucos pliciformis, the crowns are very high but develop roots. Reguero et al. (2003b) provide hypsodonty index (HI) values for select species of advanced interatheres, and later provides HI values for all typotherians (Reguero, 2010). Croft et al. (2003) analyzed archaeohyracid phylogenetics using 22 characters (19 of which are dental). In this character data, cheek tooth crown height was scored by subdividing the range in values of a continuously varying HI. For Croft et al. (2003), brachydont is HI<1, moderately hypsodont is 11.75, and the rootless condition has an appropriately undefined HI. Of his eight taxa, only Oldfieldthomasia, the primitive outgroup, is brachydont. Only Acropithecus (Archae- opithecidae), and Eohyrax and Pseudohyrax among Archaeohyracidae are mesodont. Three taxa of archaeohyracids, Archaeotypotherium, Protarchaeohyrax, and Archae- ohyrax, are hypsodont, and the most derived taxon used in the analyisis, Hegetotherium (Hegetotheriidae), has the rootless condition. Similarly, Shockey (1997a) used a single character (out of a total of 29) for crown height and distinguished discrete states of maxillary first molar tooth crown height (Character 11) among Notohippidae by subdividing the continuous variation in the measurement of M1 HI. He defined brachydont as HI<1, mesodont as HI¼1, hypsodont as 12, the rootless condition only observed in Colhuehuapian Argyrohippus fraterculus. By Shockey’s observation, Pampahippus, Plexotemnus, and Puelia are brachydont, only Eomorphippus obscurus is mesodont, and all Deseadan and younger notohippids are hypsodont. Shockey’s cladogram suggests that hypsodonty was a breakthrough character for Notohippidae, with a large radiation following the evolution of hypsodonty sometime between the time of Puelia and the radiation of diverse taxa of the Deseadan. All these phylogenetic analyses affirm that most of the evolution of high-crowned teeth among notoungulates occurred during the middle Cenozoic, and all comprise pieces of the phenomenon of “precocious” hypsodonty. Only following the discovery and dating of the fauna from near Tinguiririca in the Chilean central Andes was a 28 Hypsodonty in the South American fossil record

chronologic age established for the oldest record of the manifest prevalence of hypsodonty across the mammalian fauna (Wyss et al., 1993, 1994; Flynn and Wyss, 1998). Following the temporal calibration of the faunal sequence at Gran Barranca, the precocious evolution of hypsodonty in South American unguligrade herbivores has become associated with the Eocene–Oligocene Transition (EOT) (Kay et al., 1999). Using the limited geochronology available at the time, Kay et al. (1999) pointed out the possibility that the precocious acquisition of hypsodonty may have been related to climate change associated with the onset of permanent ice in Antarctica. The temporal coincidence between climate change and hypsodonty was rendered somewhat more plausible by four broad correlations between the prevalence or percentage of high tooth crowns in living South American sigmodontines and (1) decreasing mean annual temperature, (2) increasing mean temperature of the coldest month, (3) decreasing mean annual precipitation, and (4) increasing annual amplitude of mean monthly temperatures. These four dimensions of terrestrial climate were thought to have characterized environmental change at high latitudes across the EOT (Sloan and Barron, 1992).

2.3.2 The record

Conventionally, notoungulate taxa are hypsodont when the height of a particular tooth crown exceeds its anteroposterior length (Simpson, 1967). For teeth that form roots, unworn crown height from apex to the cementoenamel junction just above the root is a measure of the amount of enamel crown available to the animal during its lifetime. For ever-growing teeth, much (sometimes most) of the crown height generated during the animal’s lifetime is not present in a preserved crown. Thus, measures of crown height on these two kinds of teeth (rooted and ever-growing) are not comparable, and consequently, indiscriminate measures of crown height may not provide a useful measure of the volume of mineral substance formed during the animal’s life. In what follows, crown height is discussed here in several different ways. (1) Measures of crown height in individual taxa are expressed as an HI, the ratio of ﬁrst (or second) upper molar enamel crown height to anteroposterior or ectoloph length (following Simpson, 1967). Ideally, this is measured on the best-preserved and least- worn adult specimen available for each species. Once a measure of HI has been obtained for the least worn specimen of a taxon, the same value is assigned to the species at every level or locality it is reported (Table 2.2). Shockey (1997b), Croft et al. (2003), Reguero et al. (2003a, b), Hitz et al. (2006), and Reguero et al. (2008, 2010) provide such measurements but the tooth position and linear dimensions that are used in each of these studies differs. The biggest differences involve whether upper or lower molars are measured, and whether anteroposterior length (or ectoloph length) or labiolingual breath is used in the denominator. Do HIs measured on upper molars differ systematically from HIs measured on lower molars? Answering this question requires anatomically associated and unworn ﬁrst and second upper and lower molar crowns for each species. Such associated maxillary and mandibular material is not available for all species. 2.3 Hypsodonty in the middle Cenozoic of Patagonia 29

A more serious problem arises if published HIs using anteroposterior length are mixed with HIs that use labiolingual breadth. The published HIs from Reguero et al. (2010) use crown breadth (labiolingual breadth) in the denominator, while all the other published HIs use crown length (anteroposterior or ectoloph length). The use of either anteroposterior length or labiolingual width as the denominator presents a special problem because notoungulate molars generally are anisodont; that is, the breadth of the upper molar is usually larger than the breadth of the lower molar. Where HI is measured on lower molars, using length or breadth will yield very different indices, with breadth measurements generally yielding larger HIs. Few have studied the problem of anisodonty in South American archaic ungulates, and fewer still have compared HIs measured on lower and upper teeth in the same species, while none have compared HIs on lower molars using both length and breadth measurements. (2) Hypsodonty can also be expressed as an average or mean HI among the species of a family-level clade. This provides a mean HI for each clade, and patterns of increasing HI for each clade can be established at each stratigraphic level (Table 2.3). (3) A measure of faunal hypsodonty, for example, notoungulate hypsodonty, is the percentage of hypsodont taxa among Notoungulata. As used in the following discussion, notoungulate hypsodonty is the proportion of species of Notoungulata with rooted molars that have a measured HI>1.0. (If a measurement of HI cannot be obtained for a species because of inadequate preservation, that taxon is ignored in the computation of both clade and notoungulate hypsodonty.) In general, the evolution of higher crowns is a process, not an event. That is to say, arbitrary rubicons (HI>1) were probably crossed at different times and at different evolutionary rates in each lineage. While changing environmental conditions can result in either independent or coincident change, coincident change in tempo and magnitude across a fauna suggests environmental causation more strongly than independent phyletic change in individual lineages. For the discussion of the precocious evolution of hypsodonty in Patagonia that follows, fossil-bearing stratigraphic zones or levels are distinguished in the Sarmiento Formation of Patagonia, nine of which occur in superposition at Gran Barranca. Some of the nine are zones that include more than one fossil level (for example, the Barrancan below Simpson’s Y Tuff includes several different levels), whereas others are single, particularly rich horizons (such as the Barrancan fauna of Simpson’s Y Tuff, the fauna from GBV-4 La Cancha, and the fauna from GBV-19 La Cantera). Although the age range of the Sarmiento Formation is somewhat greater, the age range of the sequence relating to precocious hypsodonty extends from about 41.5 to 30 Ma; that is, from the base of the Barrancan up to the level of GBV-19 La Cantera. The evolutionary trends continue above this level. In terms of measured HI for individual taxa and mean HI for monophyletic groups, the oldest examples of the evolution of hypsodonty in Patagonia antedate the EOT. The Archaeohyracidae is the ﬁrst family-level group or clade of Notoungulata in Patagonia to include hypsodont taxa (Figure 2.8). The oldest hypsodont notoungulate is the archaeohyracid Eohyrax rusticus. Its occurrence in the Sarmiento Formation at Cañadon Table 2.2 Hypsodonty indices for species in clades (families) of middle Cenozoic mammals in Patagonia by stratigraphic level

Age Locality/level (Ma) Notohippidae Archaeohyracidae Interatheriidae Astrapotheriidae Toxodontidae Notostylopidae

Pinturan 19.2 Protypotherium sp. Interatherium sp. Colhuehuapian 20.9 Argyrohippus cf. Cochilius Parastrapotherium Proadinotherium (Big Mammal A.boulei ¼ 2.55 volvens ¼ (2.54) symmetrum muensteri ¼ 3.67 Tuff) Astrapotherium? ruderarium (¼Astrapothericulus) ¼ 1.0 Parastrapotherium herculeum ¼ 0.87 Uruguaytheriinae incertae sedis La Flecha 24.1 Argyrohippus Archaeohyrax Argyrohyrax Parastrapotherium Proadinotherium and Cabeza praecox ¼ 2.55 patagonicus proavunculus ¼ 0.87 leptognathum Blanca ¼ (>2.5) ¼ (2.10) ¼ 1.98 (La Flecha Tuff) Rhynchippus Progaleopithecus pumilus ¼ 1.56 tournoueri ¼ (1.9) Morphippus Plagiarthrus clivus imbricatus ¼ 2.12 ¼ 1.17 Coresodon Archaeophylus scalpridens? patrius ¼ (1.70) Rhynchippus equinus? ¼ (1.56) Rhynchippus equinus ¼ 1.56 Eurygenium latirostris ¼ (1.7) GBV-34, GBV-1 26.3 Parastrapotherium ¼ (0.87) (Basalts) GBV-19 30.8 Patagonhippus Archaeotypotherium Eopachyrucos Maddenia canterensis propheticus ¼ (1.50) sp. ¼ (1.58) lapidaria ¼ (1.56) (Cantera Tuff) Patagonhippus Archaeotypotherium cf. Santiagorothia dukei ¼ 1.56 sp. ¼ (1.50) ¼ (1.26) Protarchaeohyrax gracilis ¼ (1.73) Protarchaeohyrax minor? ¼ (1.70) ?Archaeohyrax (>2.5)

Tinguiririca 31.5 Eomorphippus Archaeotypotherium Santiagorothia sp. nov tinguiriricaense chiliensis ¼ 1.26 ¼ (1.50) “Eomorphippus” Archaeotypotherium Johnbell hatcheri cf. pascuali pattersoni ¼ (1.50) ¼ 0.86 Rhynchippinae Pseudhyrax Ignigena New taxon A strangulatus ¼ (1.6) minisculus ¼ 0.79 Rhynchippinae Pseudhyrax cf. New taxon B P. eutrachytheroides ¼ (1.30) Pseudhyrax eutrachytheroides ¼ (1.30) Protarchaeohyrax gracilis ¼ (1.73) Protarchaeohyrax intermedium ¼ (1.70) Protarchaeohyrax minor ¼ (1.70) # Taxa Hypsodonty among Notoungulata (in all notoungulates Oldﬁeldthomasiidae Isotemnidae Leontiniidae Mesotheriidae Hegetotheriidae Didolodontidae this table) (%)

Pachyrukhos sp. 3

Colpodon 475 distinctus

Ancylocoelus Trachytherus Prosotherium 22 77 frequens spegazzinianus garzoni ¼ (2.72) ¼ 2.32 Leontinia Anatrachytherus Medistylus gaudryi soriai ¼ 1.92 dorsatus ¼ (2.41) Prohegetotherium sculptum ¼ (2.23)

Prohetetotherium shumwayi? Propachyrucos smithwoodwardi ¼ 2.50

Scarrittia barranquensis

Pleurocoelodon? Scarrittia cf. Trachytherus 13 69 barranquensis

Henricoﬁlholia vucetichia

15 60 Table 2.2 (cont.)

Age Locality/level (Ma) Notohippidae Archaeohyracidae Interatheriidae Astrapotheriidae Toxodontidae Notostylopidae

GBV-4 La 33.6 Puelia plicata Archaeotypotherium Guilielmoscottia Astraponotus Cancha ¼ (0.75) propheticus ¼ (1.5) plicifera ¼ 0.86 sp. ¼ (0.90) (Carlini Tuff) Puelia sp. Protarchaeohyrax Eopachyrucos ¼ (0.81) gracilis ¼ (1.73) pliciferus ¼ 1.58 Eomorphippus Pseudhyrax ? Santiagorothia obscurus ¼ 1.01 strangulatus ¼ (1.6) sp. ¼ (1.26) Eomorphippus Pseudhyrax Proargyrohyrax sp. eutrachytheroides sp. ¼ (1.2) ¼ (1.30) [Eomorphippus pascuali ¼ 0.72]

GBV-3 (also 38 Puelia plicata Pseudhyrax Antepithecus Astraponotus asymmetrus Otronia Coley’s Quarry) ¼ (0.75) strangulatus ¼ (1.6) brachystephanus ¼ (0.90) muhlbergi ¼ (0.61) (Rosado Tuff) Puelia coarctatus Pseudhyrax sp. Guilielmoscottia? ¼ (1.6) ¼ (0.86) cf. Eopachyrucos? ¼ (1.58)

GBV-60 38.5 Eohyrax sp. ¼ (1.25) Notopithecus sp. Homalostylops ¼ (0.69) parvus Protarchaeohyrax sp. Transpithecus sp. ¼ (0.70) ¼ (1.70) ¼ (0.73) Antepithecus sp. ¼ (0.61)

Above 39.1 Eohyrax sp. ¼ (1.25) Notopithecus Albertogaudrya ¼ (0.69) Notostylops Y (Mazzoni adapinus ¼ (0.69) murinus Tuff) Antepithecus ¼ (0.53) brachystephanus ¼ (0.61)

Y 39.86 Eohyrax isotemnoides Notopithecus Albertogaudrya sp. Notostylops ¼ (1.28) adapinus ¼ (0.69) ¼ (0.69) murinus (Simpson’sY Transpithecus ¼ (0.53) Tuff) ¼ (0.73) Antepithecus brachystephanus ¼ (0.61)

Below Y 41.7 Notopithecus Albertogaudrya Notostylops adapinus ¼ (0.69) unica ¼ (0.69) murinus (VRS Tuff) Transpithecus ¼ (0.53) obtentus ¼ (0.73)

Cañadon Vaca >43 Eohyrax rusticus Notopithecus Albertogaudrya Notostylops ¼ (1.25) adapinus ¼ (0.69) sp. indet. pendens ¼ (0.69) Homalostylops sp. # Taxa Hypsodonty among Notoungulata (in all notoungulates Oldﬁeldthomasiidae Isotemnidae Leontiniidae Mesotheriidae Hegetotheriidae Didolodontidae this table) (%)

Periphragnis sp. 17 53

Rhyphodon?

Gen et sp. indet.

Anisotemnus distentus

Periphragnis Paulogervaisia 12 25 exauctus inusta

Rhyphodon sp.

Distylophorus alouatinus Periphragnus sp. Ultrapithecus Didolodus 825 rutilans ¼ (0.78) magnus cf. Pleurostylodon ?

Ultrapithecus Isotemnus 714 rutilans ¼ (0.78) primitivus Pleurostylodon modicus

Ultrapithecus Anisotemnus sp. Didolodus 911 rutilans ¼ (0.78) Indet. multicuspis Pleurostylodon Ernestokokenia modicus nitida Thomashuxleya rostrata

Pleurostylodon Didolodus 40 modicus multicuspis

Maxschlosseria Didolodus 520 consumata minor ¼ (0.67) 34 Hypsodonty in the South American fossil record

Table 2.3 Average hypsodonty indices for clades of native “ungulates” in Patagonia and at Tinguiririca in Central Chile. Number of species used to calculate average in parenthesis

Age Level (Ma) Notohip Archaeohy Interath Astrapo Toxodont Notosty Oldﬁeld Hegeto

Colhuehuapian 20.9 2.55 (1) . 2.54 (1) 0.935 (2) 3.67 (1) . . . La Flecha and 24.1 1.68 (6) 2.5 (1) 1.96 (4) 0.87 (1) 1.98 (1) . . 2.397 (3) Cabeza Blanca GBV-34, 26.3 . . . 0.87 (1) . . . . GBV-1 GBV-19 30.8 1.56 (2) 1.786 (5) 1.42 (2) . . . . . Tinguiririca 31.5 1.576 (8) 0.97 (3) . . . . . GBV-4 33.6 0.823 (4) 1.53 (4) 1.225 (4) 0.9 (1) . . . . GBV-3 38.0 0.75 (1) 1.6 (2) 1.016 (3) 0.9 (1) . . . . GBV-60 38.5 . 1.475 (2) 0.676 (3) . . 0.7 (1) 0.78 (1) . Above Y 39.1 . 1.25 (1) 0.65 (2) 0.69 (1) . 0.53 (1) 0.78 (1) . Simpson Y 39.86 . 1.28 (1) 0.676 (3) 0.69 (1) . 0.53 (1) 0.78 (1) . Below Y 41.7 . . 0.71 (2) 0.69 (1) . 0.53 (1) . . Cañadon Vaca >43 . 1.25 (1) 0.69 (1) 0.69 (1) . . 0.67 (1) .

Notohip, Notohippidae; Archaeohy, Archaeohyracidae; Interath, Interatheriidae; Astrapo, Astrapotheridae; Toxodont, Toxodontidae; Notosty, Notostylopidae; Oldﬁeld, Oldﬁeldthomasiidae; Hegeto, Hegetotheriidae.

Vaca in Patagonia is still the oldest record of a hypsodont notoungulate anywhere in South America. The Archaeohyracidae were the ﬁrst family of notoungulates to become hypsodont (mean HI>1), and the rubicon was passed sometime before 43.0 Ma. Between 39.0 and 38.0 Ma (in the late middle Eocene) there is a further increase in the mean HI for species of this clade (Figure 2.9). During the long interval from about 38 Ma to 30.8 Ma, there is only a slight additional increase in the mean HI for this group. At 30.8 Ma, there is a signiﬁcant increase in the mean HI for the family with the appearance of Archaeohyrax, a taxon that persists in Patagonia through the Deseadan. The next notoungulate clade to evolve hypsodonty, that is, the next family-level group of Notoungulata to achieve mean HI>1 was the Interatheriidae, a group that was long resident in Patagonia. The oldest known hypsodont interatheriid in the Patagonian fossil record is cf. Eopachyrucos with an HI¼1.58 at a level dated to 38.0 Ma. This occurrence marks the moment the Interatheriidae passed the mean HI rubicon and it occurred in the late middle Eocene. The Interatheriidae show a slight increase in mean HI at 33.6 Ma with the appearance of Proargyrohyrax, Santiagorothia, and Eopachy- rucos pliciferus. The decrease in mean HI of interatheres at Tinguiririca is noteworthy. Between 30.8 Ma and 20.9 Ma, the crown height of advanced interatheres increases steadily. The third monophyletic group to achieve a mean HI>1 was among taxa in the family Notohippidae (Figures 2.9 and 2.10), and this occurred some time between 33.6 Ma and 30.8 Ma, possibly either during the later part of the EOT or just subsequent to Oi-1, the oldest glacial stage in the middle Cenozoic. The oldest hypsodont notohippid is Eomorphippus obscurus (HI¼1.01); it occurs at a level at Gran Barranca (GBV-4 La 2.3 Hypsodonty in the middle Cenozoic of Patagonia 35

100

25 Notoungulate hypsodonty (%) 0

4.0 Archaeohyracidae

Oldfieldthomasiidae

Notostylopidae 3.0 Toxodontidae

Interatheriidae

Notohippidae 2.0 Hypsodonty index (HI) 1.0

0.0 45 40 35 30 25 20 Time (Ma)

Figure 2.8 Evolutionary trends of increasing prevalence of taxa with high-crowned molars (top) and molar crown height (hypsodonty index, HI) in middle Cenozoic clades of Notoungulata (bottom). Top, percentage of notoungulate taxa that are hypsodont. Bottom, mean HI in six clades of notoungulates.

Cancha) dated to Chron 13n or 33.6 Ma (where it occurs along with at least three other taxa of non-hypsodont notohippids). The Notohippidae were long resident in Patagonia and first appear in the fossil record there at about 38.0 Ma (Puelia sp.), but are as yet unknown from older assemblages there. Of these three examples of family-level groups evolving hypsodonty, the two oldest (Interatheriidae and Notohippidae) plausibly evolved hypsodonty in Patagonia, as they have evolutionary histories in Patagonia prior to the first appearance of hypsodont species, and their phylogenetic relationships do not contradict this by revealing a more derived sister-group with higher-crowned teeth at an older level in a locality outside Patagonia (Shockey, 1997a; Hitz et al., 2000). In these two groups, the oldest hypsodont taxon first appears in Patagonia in assemblages including other taxa of the same group that are not hypsodont. Of special note, in the stratigraphic level immediately following 36 Hypsodonty in the South American fossil record

Ting Casamayoran Deseadan-Colhuehuapian

Casamayoran Deseadan–Colhuehuapian

0.60 1.71

Tinguirirican 0.96 Pleurosylodon modicus arenalesi Pampahippus complicatissimus Plexotemnus Puelia coarctatus Eomorphippus obscurus boliviensis Pascualihippus equinus Rhynchippus pumilus Rhynchippus Rynchippus brasiliensis Eurygenium pacegnum Eurygenium latirostris Argyrohippus praecox Argyrohippus fraterculus Pleurosylodon modicus arenalesi Pampahippus complicatissimus Plexotemnus Puelia coarctatus Eomorphippus obscurus boliviensis Pascualihippus equinus Rhynchippus pumilus Rhynchippus Rynchippus brasiliensis Eurygenium pacegnum Eurygenium latirostris Argyrohippus praecox Argyrohippus fraterculus

M1 crown height brachydont (HI<1) mesodont (HI=1) A B hypsodont (12) equivocal

Deseadan– Casamayoran Colhuehuapian

Tinguir.

1.351.75 to >2.25 2.25 Oldfieldthomasia Acropithecus Eohyrax Pseudhyrax Archaeotypotherium Protarchaeohyrax Archaeohyrax Hegetotherium Oldfieldthomasia Acropithecus Eohyrax Pseudhyrax Archaeotypotherium Protarchaeohyrax Archaeohyrax Hegetotherium

M1 crown height D E brachydont (HI<1) F moderately hypsodont (1< HI<1.75) very hypsodont (HI>1.75) rootless equivocal

Figure 2.9 Phylogeny and molar crown height in middle Cenozoic Notohippidae and Archaeohyracidae. (A) Phylogeny of notohippid species according to Shockey (1997) with unresolved Casamayoran and Deseadan polytomies. (B) Maxillary ﬁrst molar crown height character trace on Shockey’s phylogeny. (C) Mean HIs for notohippid species in Casamayoran and Deseadan-Colhuehuapian polytomies, and HI for Tinguirirican Eomorphippus obscurus. (D) Phylogeny of archaeohyracid genera according to Croft et al. (2003). (E) Maxillary ﬁrst molar crown height character trace on the phylogeny. (F) Mean HIs for archaeohyracid genera in the Casamayoran, Deseadan–Colhuehuapian, and for Archaeotypotherium and Protarchaeohyrax.

or subsequent to the first appearance of hypsodont species, all species in these two clades are hypsodont. Four family-level groups of Notoungulata are hypsodont at their first appearance in the Patagonian fossil record: the Archaeohyracidae, the Toxodontidae, the Hegetotheriidae, and the Mesotheriidae. The oldest known Archaeohyracidae in the Sarmiento Formation is Eohyrax rusticus with an HI of 1.25. Still higher-crowned archaeohyracids appear at 38.5 Ma, and increase in diversity to four taxa at 33.6 Ma and five taxa at 30.8 Ma. The oldest known Toxodontidae in Patagonia (Proadinotherium leptognathum) has an HI of 1.98. Like the Archaeohyracidae, the family-group Toxodontidae is fully hypsodont when it first appears in the Patagonian fossil record in the Deseadan between about 24 Ma and 26 Ma. The oldest known Hegetotheriidae in Patagonia are the five taxa that appear in the Deseadan at Cabeza Blanca. Of these five, the HI can be measured in Prosotherium garzoni, Medistylus dorsatus, Prohegeotherium sculptum, and Propachyrucos smithwoodwardi, all with HI>2.2. The oldest Patagonian record of Mesotheriidae (Trachytherus) is at 30.8 Ma, and this taxon is fully hypsodont when it first appears in 2.3 Hypsodonty in the middle Cenozoic of Patagonia 37

Figure 2.10 Evolutionary increase in mandibular premolar and molar crown height in Notohippidae from Patagonia. Specimens arranged in temporal sequence from oldest (C, bottom) to youngest (A, top). (A) Rhynchippus equinus AMNH 14152 from the Deseadan of Cabeza Blanca; (B) Eomorphippus obscurus MLP 12-1508 from the Tingurirican at Cañadon Blanco; (C) Eomorphippus pascuali AMNH 29474 from the Tinguirirican at Gran Barranca.

Patagonia. Precisely when and where these groups evolved hypsodonty cannot be determined from the known fossil record in Patagonia. Interestingly, outside Notoungulata, one species of Astrapotheriidae (Order Astrapotheria) became hypsodont (HI¼1.0) in Patagonia at 20.9 Ma (Astrapotherium? ruderarium) as evident by their fossil record at Gran Barranca (Kramarz and Bond, 2009). This trend to higher crowns in Astrapotheriidae is ﬁrst evident in the Mustersan (Figure 2.11). 38 Hypsodonty in the South American fossil record

Albertogaudrya (?Astraponotus)

Albertogaudrya unica

Figure 2.11 Mandibular molars of Astrapotheriidae (Astrapotheria) from the middle Cenozoic of Gran Barranca, arranged from youngest (top) to oldest (bottom): Albertogaudrya unica right m1 or m2 MACN 12001; Albertogaudrya (¼?Astraponotus) left m1 or m2 AMNH 28637; Astraponotus sp. left m1 or m2 AMNH 29449 from Coley’s Quarry.

There is also an example of the evolution of high-crowned teeth among marsupials in the Patagonian fossil record at Gran Barranca, beginning with the appearance of rather more high-crowned taxon Epiklohnia verticalis among Argyrolagoidea at 33.6 Ma (Goin et al., 2010). With regard to precocious hypsodonty among Notoungulata, there is a brief interval of coincident and coordinated increase in mean HI in three families or clades between 39.1 Ma and 38.0 Ma at Gran Barranca. It involves the Notostylopidae (HI increases from 0.53 to at least 0.70), the Interatheriidae (mean HI increases from 0.65 to 1.02), and the Archaeohyracidae (mean HI increases from 1.25 to 1.60). This coincident increase in crown height occurs over a one-million-year interval in the late middle Eocene (Figure 2.8). What about the evolution of hypsodonty in Patagonia in terms of faunal hypsodonty? Considering only Notoungulata (Figure 2.8), from 43.0 Ma until about 39.1 Ma there was only one hypsodont notoungulate in Patagonia, the archaeohyracid Eohyrax. 2.3 Hypsodonty in the middle Cenozoic of Patagonia 39

Between 39.1 Ma and 38.0 Ma, the proportion of hypsodont taxa among notoungulates increased to 25%. Hypsodonty among notoungulates reached 53% by 33.6 Ma, and 69% by 30.8 Ma, about as high a measure of notoungulate hypsodonty that one ever finds in the South American fossil record. Unfortunately, we do not know precisely at what moment or in what interval between 38.0 Ma and 33.6 Ma notoungulate hypsodonty increased from 25% to 53%; all we know is that by 33.6 Ma, over half of the notoungulates in the Patagonian fauna were hypsodont. In summary, the oldest hypsodont notoungulate in the Patagonian fossil record (Eohyrax rusticus, Archaeohyracidae) appears at about 43 Ma without antecedents, although the typotherian Kibenikhoria, by far the most common species in the Riochi- can at Cañadon Hondo, has high but not hypsodont crowns. During the Barrancan, there is little conspicuous increase in crown height. Then abruptly, in the brief interval between 39.1 Ma and 38.0 Ma in the late middle Eocene, there is coincident increase in mean HI involving the clades Notostylopidae, Interatheriidae, and Archaeohyracidae. This event of coincident increase in mean HI in these three clades is explained by the appearance of Protarchaeohyrax and Pseudhyrax among Archaeohyracidae, Eopachyrucos and Guilielmoscottia among Interatheriidae, Homalostylops among Notostylopidae, and the first appearance of Notohippidae (Puelia). As such, this event represents a departure from the relative stasis of the Barrancan, and also contrasts with the subsequent interval of relative stasis among these same clades between 38.0 Ma and 33.6 Ma. This one-million-year long evolutionary event between the end of the Bar- rancan and the Mustersan is underway at 38.5 Ma (Cifelli, 1985; Level 15, Section V) and is completed by 38.0 Ma. During the interval between 38 Ma and 33.6 Ma in Patagonia, while mean HI for notoungulate clades remains almost constant (Figure 2.8), there occurs a remarkable proliferation of hypsodont taxa within Notohippidae, Archaeohyracidae, and Interather- iidae such that notoungulate hypsodonty increases from 25% to over 50% (Tables 2.2 and 2.3). The accumulation of hypsodont taxa in these three clades is an important event in South American mammal evolution, and is coincident with Goin’s “Patagonian hinge” (Goin et al., 2010), a moment of transcendant change in the composition of the marsupial fauna of Patagonia. The Notohippidae first appear in the Patagonian fossil record at about 38.0 Ma but the first hypsodont notohippid Eomorphippus obscurus appears nearly four million years later at about 33.6 Ma. Among Notohippidae at GBV-4 La Cancha (Puelia and Eomorphippus), both genera undergo a phyletic increase in crown height. Diversifi- cation in Puelia gives rise to Puelia plicata (HI¼0.75) and Puelia coarctatus (HI¼0.81), and in Eomorphippus we find phyletic increase in crown height between E. pascuali (HI¼0.72) and E. obscurus (HI¼1.01). Precisely when this occurred is not known, but it may have occurred rapidly around 33.6 Ma, as suggested by the fossil record of Eomorphippus at Gran Barranca (Simpson, 1967). Proliferation is also evident in Archaeohyracidae and Interatheriidae during this interval. Diverse Interatheriidae (Proargyrohyrax, Eopachyrucos, and perhaps Santiagorothia) and Archaeohyracidae (Archaeotypotherium, Protarchaeohyrax,andPseudhyrax) occur together at 33.6 Ma. Exactly when this proliferation occurred is also not known. 40 Hypsodonty in the South American fossil record

Hypsodont Toxodontidae, Mesotheriidae, and Hegetotheriidae appear abruptly in the fossil record in Patagonia, the Mesotheriidae at about 30.8 Ma and the Toxodontidae and Hegetotheriidae somewhat later by about 24.1 Ma. These three groups appear without local antecedents, indicating their evolutionary transition to high crowns probably occurred outside Patagonia. At about this same time, caviomorph rodents begin to show a significant increase in crown height (Wood and Patterson, 1959). Some Deseadan caviomorphs from Patagonia (from La Flecha and Cabeza Blanca) display higher-crowned molars than their closest phylogenetic relatives at Salla in Bolivia (Patterson and Wood, 1982). New dates for the type Deseadan at La Flecha suggest the two best-known Patagonian Deseadan local faunas may be as much as two million years younger than the most fossiliferous levels at Salla (Kay et al., 1998). Whether this rodent crown height evolution took place in Patagonia or elsewhere is still a mystery. Did any of the process of the evolution of higher tooth crowns among notoungulates happen in Patagonia? Or could they plausibly have evolved high-crowned teeth elsewhere in South America or Antarctica, from where they subsequently migrated into Patagonia? This question is important with regard to a search for an explanation. Of all the changes in HI, the coincident “events” between 39 Ma and 38 Ma and between 33.6 Ma and 30.8 Ma, appear to involve taxa with antecedents in the Patagon- ian fossil record. All the other parts of the story, including the first appearances of hypsodont Archaeohyracidae (Eohyrax at 43 Ma), mesodont Notohippidae (Puelia at 38 Ma), hypsodont Toxodontidae (Proadinotherium at 24 Ma), euhypsodont Mesotherii- dae (Trachytherus at 30.8 Ma), and diverse Hegetotheriidae in the Deseadan at 24 Ma, involved unheralded appearances in the Patagonian fossil record without clear and plausible resident antecedent or ancestral groups. All these clades may have evolved their initial hypsodonty elsewhere. How do we establish that an evolutionary increase in crown height occurred in situ in Patagonia, or any geographic area, in essence, in a direct ancestor–descendant relationship? Given a set of two or more closely related taxa from the same geographic area, each with their first appearances (FAPs) in a different stratigraphic level, how do we conclude they represent an evolving lineage? The hypothesis requires a character-based phylogeny in which each taxon appears as a separate branch and each other’s nearest neighbor (Figure 2.9). In addition, the order of the branches must agree with stratigraphic superposition; that is, the branching pattern reproduces the chronologic sequence of strata, and for all characters supporting the phylogeny, the character-state transformation is unidirectional and consistent with stratigraphy or geochronology. Such a hypothesis can be falsified by the simple discovery of a third taxon from a different geographic area that character analysis places on the branching diagram between the original two taxa. For example, Eopachyrucos, only known from Patagonia, is at the base of a clade of more derived interatheres the basal node of which is itself part of a trichotomy with Johnbell and Ignigena, two taxa from farther north in central Chile (Hitz et al., 2006). At Gran Barranca, Eopachyrucos occurs at GBV-3, GBV-4, and GBV-19, and is the oldest and most primitive taxon in a clade supported by three (Hitz et al., 2006)orfive 2.3 Hypsodonty in the middle Cenozoic of Patagonia 41

(Reguero et al., 2003b) characters. Among the most primitive members of this clade, Proargyrohyrax occurs at GBV-4 and Santiagorothia occurs at GBV-4 and GBV-19 at Gran Barranca, and the same phylogenies agree in showing that these taxa are derived with respect to Eopachyrucos (Reguero et al., 2003b). Judging by their first appearances at Gran Barranca, there is a chronologic sequence of FAPs from Eopachyrucos– Proargyrohyrax–Santiagorothia. Is this an evolving lineage with increasing crown height? Assuming published measures of HI are comparable, Eopachyrucos pliciferus (HI¼1.58) is derived with respect to Proarchyrohyrax (HI¼1.2) and Santiagorothia (HI¼1.26) (Reguero et al., 2003b), yet represents a significant increase over its primitive cladistic sister-group comprising Johnbell (HI¼0.85) and Ignigena (HI¼0.79) (Hitz et al., 2006). What are we to make of this? That Eopachyrucos might be descended from taxa in Patagonia is contradicted by the discovery of Johnbell and Ignigena in central Chile and Punapithecus in northwestern Argentina (Hitz et al., 2006). If Eopachyrucos is descended from taxa outside Patagonia, the first significant increase in crown height among interatheres did not happen in Patagonia, and is not well documented anywhere. However, the proliferation of high-crowned interatheres seems to have occurred in Patagonia, at least until something like Santiagorothia or Proargyrohyrax are found in deposits elsewhere that antedate 30.8 Ma, the age of GBV- 4 La Cancha. Archaeohyracidae provide another example. Eohyrax (HI¼1.25) is only known from Patagonia, and occurs at Cañadon Vaca and in the Barrancan. Protarchaeohyrax (HI¼1.70), Pseudhyrax (HI¼1.6), and Archaeotypotherium (HI¼2.25) are relatively derived and have their first appearances at Gran Barranca at GBV-60, GBV-3, and GBV-4, respectively. The family Archaeohyracidae makes its first appearance in the fossil record in Patagonia (at Cañadon Vaca), and the clade of more derived taxa also has its first appearance in Patagonia at GBV-60. Thus, the proliferation of archaeohyracids appears to have occurred in Patagonia, at least until these taxa are found in older deposits elsewhere. Until then, their progressive evolution in crown height also appears to be in response to local environmental change, and little if any of their crown-height evolution or diversification is related to the Eocene–Oligocene climatic deterioration, as posited by Croft et al. (2003).

2.3.3 Evolving lineages at Gran Barranca

A cladogram that reveals a series of closely related taxa (nearest neighbors in the branching order) found in stratigraphic sequence within a restricted geographic area (say Patagonia), the morphological differences of which relate only to hypsodonty (and characters that co-vary with hypsodonty), would constitute prima facie evidence for an evolving lineage. This amounts to using fossils as tests of phylogenetic estimation through consistency metrics (e.g., the stratigraphic consistency index) that compare branching order with appearance in the fossil record (Huelsenbeck, 1994). Stratophenetics (Gingerich, 1979) is a more traditional approach to establish species- level lineages when stratigraphic completeness convincingly demonstrates evolutionary continuity; for example, in the condylarthran Hyopsodus, where stratophenetics reveals 42 Hypsodonty in the South American fossil record

trends in tooth size commonly used as a proxy for body size. Conceptually similar graphical depictions of lineages demonstrating gradually increasing hypsodonty (or directional change in some other morphological character) was the classic approach used by Marsh (at the time of Darwin) for horses, and Stirton for beavers. Another approach using stratocladistics (Fisher, 1994) looks at the congruence between phylogeny and stratigraphy, whereby high congruence supports the identity of lineages and low congruence weakens the evidence. For example, consider the Notohippidae (Figure 2.9, top panel). Character analysis and phylogenetics, including crown height as an unordered character, reveals a branching pattern in which a taxon of intermediate crown height (Eomorphippus) is interposed between a group of basal taxa with low crown height, and a clade with high crown height in unresolved polytomy. This same pattern is found among Interatheriidae, where a taxon of intermediate crown height (Santiagorothia) is interposed between a group of basal interatheres with brachydont cheek teeth (formerly called Notopithecinae) and a monophyletic clade with hypselodont cheek teeth in unresolved polytomy. A broadly similar pattern where increasing crown height is consistent with branching order is found in Archaeohyracidae. An evolving lineage will have a plausible ancestor in the next immediately lower stratigraphic level. The longer the stratigraphic sequence, the more robust the hypothetical lineage becomes. Such propositions are testable hypotheses; that is, can be refuted by (1) the discovery of unexpected morphological affinity with a more distantly related group or the discovery of a more closely related taxon (by synapomorphy) in a geographically distant location; (2) by the discovery of a richly fossiliferous intermediate level without a suitable morphological intermediate, thereby increasing the temporal space between purported ancestor and descendant; and (3) the sudden unheralded first appearance of elements in the assemblage (indicating a migration event). Any proposition that Species A is ancestral to Species B (they differ only in a unidirectional morphological transformation) is a testable or falsifiable proposition refuted by the discovery of a plausible ancestor (or more closely related sister-taxon) of greater antiquity elsewhere, displaying intermediate condition between the purported two end- points of a hypothetical sequence. Just finding the same taxon elsewhere is not a complete refutation; it must also be intermediate in the character transformation. It might be said that without benefit of modern cladistics and geochronology, Simpson (1967, p. 140) struggled to make sense of morphological succession among notoungulates in Patagonia. However, I think, in retrospect, Simpson’s approach had a lot of practical merit. For example, he expressed “doubt about supposed cases of genera common to the Casamayoran and Mustersan, and there are no species common to the two, but there are species so similar that their generic separation is dubious at least. Casamayoran Thomashuxleya versus Mustersan Periphragnis and Casamayoran Anisotemnus versus Mustersan Rhyphodon are examples.” Casamayoran Notoungulata seemed to present a special problem for Simpson. “It is again clear that in the Casamayoran we are very near the base of notoungulate differentiation. Forms that must be placed in different families, when account is taken of the later lines, and that could even be placed in different suborders from this point of view, are here really quite 2.3 Hypsodonty in the middle Cenozoic of Patagonia 43

closely related from the point of view of their horizontal and immediately ancestral relationships” (Simpson, 1967, p. 62). Whether the Casamayoran at Gran Barranca is a time near the base of notoungulate differentiation, or only near the base of an important episode of evolutionary radiation following the appearance of morphological novelty, is an important question. It implies that the task of making sense of phylogenetic affinities at a time of rapid evolutionary change will be difficult because of the experimental nature of the events. In the following, I present more details about the evolutionary transformations to higher tooth crown height among archaic ungulates of Patagonia, and attempt to identify evolving lineages more carefully and explicitly, to determine whether first appearances represent in situ evolutionary change or immigration events. Readers satisfied with the previous summary of the important features of the record of “precocious” hypsodonty, should move on directly to the last two sections of this chapter, and then to the next chapter.

2.3.3.1 Isotemnidae Among Isotemnidae, Periphragnis (Mustersan) is closely similar to Thomashuxleya (Casamayoran), but the otherwise brachydont teeth have slightly higher crowns; and five less conspicuous differences are (1) parastyle and paracone folds of upper molars are less prominent and less sharply separate, (2) parastyle folds of upper cheek teeth are strongly interlocking or imbricate, (3) p2 is more complex, with well-developed posterolingual sulcus, (4) lower premolars generally are shorter and relatively broader, and (5) incisor series are more transverse, suggesting a slight increase in crown height and other adaptations to herbivory or a more grazing habitus (Simpson, 1967; p. 162). If this is an evolutionary transformation, it probably occurred in Patagonia. Peri- phragnis has its stratigraphic FAP at GBV-60 El Nuevo, in an assemblage otherwise characterized by archaic taxa. The identification of material of Periphragnis was made by Cifelli (1985), but the presence of this taxon at this level has not been confirmed by later collections. Among newer material from this locality are remains of Thomashux- leya and material comparable to Pleurostylodon. Remains of Periphragnis have been found at GBV-3 El Rosado and GBV-4 La Cancha. There may be another lineage among Patagonian Isotemnidae, where Rhyphodon (Mustersan) differs from Anisotemnus (Casamayoran) in having more nearly hypsodont upper premolars, and more transverse and less quadrate upper premolars and less distinct ectoloph folds (Simpson, 1967, p. 71). Yet a third evolutionary lineage involving Isotemnidae was suggested to Simpson by Acoelohyrax (including Plexotemnus) (Casamayoran) and ?Acoelohyrax (Mustersan). Simpson speculated that this lineage might end among archaeohyracids. Acoelohyrax has higher cheek tooth crowns than usual in Isotemnidae, “its cheek teeth could be simply a somewhat more complex and higher-crowned version” of Pleurostylodon (Simpson, 1967) or a higher-crowned sister-taxon to Pleurostylodon. In Simpson’s opinion, differences between Isotemnidae and Archaeohyracidae relate to greater hypsodonty, more transitory fossettids with wear, and crown proportions (the length of trigonid less than or subequal to talonid). However, later studies of the ear region by 44 Hypsodonty in the South American fossil record

Table 2.4 Temporal succession of genera and species among middle Cenoizoic Archaeohyracidae (Notoungulata) in Patagonia, in approximate order from oldest (bottom) to youngest (top)

Maxillary/ SALMA, locality or Specimen Taxon mandibular teeth level

AMNH 29609 Archaeohyrax ? Upper molar, lower molar Deseadan, Scarritt patagonicus Pocket MACN Archaeohyrax Upper and lower dentition Deseadan, Punta A52–617 patagonicus Nava MACN Archaeohyrax? Upper dentition Deseadan, unknown A52–625 propheticus MACN A Bryanpattersonia M1 or 2, m1, m1 or 2 Mustersan 10905 nesodontoides MLP 67-II-27- Pseudhyrax (Degonia) M2–3; m3 Mustersan, Gran 40, 41 sp. Hondonada AMNH 28883 M1–3 No label AMNH 29410 Pseudhyrax m2–3 Mustersan, Cerro eutrachytheroides Blanco AMNH 29458 ?Pseudhyrax sp. P3–4, M1 Mustersan, Cerro del Humo AMNH 29487 Acoelohyrax exponens P2–4, M1–2 Mustersan, Cerro Blanco AMNH 28844 Eohyrax isotemnoides M1 and M2 Barrancan, Gran Barranca AMNH 28665 Eohyrax isotemnoides p1–4, m1–3 Barrancan, Gran Barranca AMNH 28628 Eohyrax isotemnoides Mandibular rami p1–4, Barrancan, Gran m1–3 Barranca MACN 10777 Eohyrax praerusticus Maxillary and mandibular Barrancan, Gran cheek teeth Barranca

Patterson (1936) convinced Simpson that Archaeohyracidae should be included in Hegetotheria, and Cifelli (1993) presented evidence for a sister-group relationship between Archaeohyracidae and Hegetotheriidae. This is an example of the refutation of an ancestor–descendant relationship by the discovery of morphological afﬁnity with a more distantly related group.

2.3.3.2 Archaeohyracidae According to the most recent revisions (Croft et al., 2003; Reguero et al., 2003b), there are ﬁve valid genera among Patagonian Archaeohyracidae: Archaeotypotherium (GBV- 4, GBV-19), Protarchaeohyrax (GBV-60, GBV-4, GBV-19), Pseudhyrax (GBV-3), Eohyrax (GBV-60), and Archaeohyrax (Deseadan). This succession of genera in Patagonia demonstrates a long and rather continuous evolutionary trend in increasing crown height (Table 2.4). Within this succession of Archaeohyracidae, several hypothetical evolutionary lineages have been proposed in the literature. The ﬁrst of these, Archaeotypotherium propheticus–Archaeohyrax patagonicus, are relatively large archaeohyracids. 2.3 Hypsodonty in the middle Cenozoic of Patagonia 45

Archaeotypotherium propheticus is known from GBV-4 and GBV-19 at Gran Barranca and Archaeohyrax patagonicus occurs in the Deseadan at La Flecha and Cabeza Blanca. Archaeotypotherium and Archaeohyrax differ principally in cheek tooth crown height, with Archaeotypotherium having hypsodont but rooted cheek teeth (HI¼1.75–2.25) and Archaeohyrax rootless cheek teeth (HI>2.5) (Figure 2.9, bottom panel). Some of the other diagnostic characters may be correlates of increasing crown height; for example, more or less persistent accessory fossettes/fossettids. However, certain other diagnostic characters suggest this may not be a case of a simple evolving lineage or sequence; for instance, larger lower premolars, and M3 posterior lobe. A second hypothetical lineage may be Eohyrax (Casamayoran) and Pseudhyrax (Mustersan). Simpson (1967, p. 105) established that Eohyrax is generally less hypsodont that Pseudhyrax and otherwise “Pseudhyrax is closely similar to Eohyrax and probably directly derived from and intergrading with that genus,” and Patterson (unpublished notes) considered Pseudhyrax eutrachytheroides to be plausibly ancestral to Deseadan Archaeohyrax. A third evolving lineage among archaeohyracids may be found in Protarchaeohyrax. Protarchaeohyrax occurs at Gran Barranca at three distinct levels (GBV-60, GBV-4, and GBV-19). A very small archaeohyracid, there are three recognized species: P. gracilis from Cañadon Blanco and Gran Barranca; the smallest known archaeohyracid P. minor from Cañadon Blanco; and a third species, P. intermedium, so far only known from Tinguiririca in Central Chile. All of the characters identiﬁed as distinguishing Hegetotheriidae from Archaeohyr- acidae (elodont I1, straight lingual face on lower molars, absence of fossettes/fossettids, and prismatic ever-growing cheek teeth) are all plausibly correlated with increasing crown height. Thus, Hegetotheriidae may have evolved from Archaeohyracidae in Patagonia and may not represent immigrants into Patagonia from elsewhere. Prohegetotherium, a Deseadan species P. sculptum, is the oldest known material of the family Hegetotheriidae, the oldest occurrence in Patagonia of which is at GBV-19 La Cantera (although the family may occur at Cañadon Blanco). The same is true for the mostly Deseadan taxon Trachytherus (Mesotheriidae), now known at GBV-19 La Cantera. Thus, sometime between GBV-4 La Cancha (33 Ma) and GBV-19 La Cantera (31 Ma), these two clades (Hegetotheriidae and Mesotheriidae) appear in Patagonia. They are understood to be sister-taxa of Archaeohyracidae (and along with archaeohyracids, the most recent common descendants of Campanorco), together comprise the Typotherioidea Reguero and Castro 2004 and arise phylogenetically out of the para- phyletic taxon Archaeohyracidae. Thus, these two families both could have differenti- ated in Patagonia.

2.3.3.3 Interatheriidae Cifelli (1993) recognized nine genera of Interatheriidae, included in two subfamilies the Notopithecinae (Riochican–-Mustersan) and Interatheriinae (Deseadan and later). To these must be added the new taxa described or given emended diagnosis (Hitz, 1997; Hitz et al., 2000, 2006). The family occured in the Itaboraian (Bond et al., 1995) and persisted into the Huayquerian. Establishing the identity of evolving lineages among 46 Hypsodonty in the South American fossil record

Interatheriidae in Patagonia is difﬁcult because of their remarkably constant general similarities. Simpson (1967) collected three species in the Barrancan at Gran Barranca: (1) Notopithecus adapinus (with two fairly well-distinguished subspecies), (2) Antepithecus brachystephanus (a possible second species A. innexus with slightly longer and markedly more tranverse upper molars occurs at Gran Barranca), and (3) Transpithecus obtentus;but only one species from the Mustersan, Guilielmoscottia plicifera.Thisbottleneckimplies that the evolutionary continuity of lineages may have been truncated. As Simpson (1967) noted with regard to the Notopithecinae, “these earliest interatheriids form a rather compact group in themselves, that there is a profound phylogenetic gap between them and the typical interatheres of the Deseadan.” This profound gap relates only to the evolutionary change in crown height from the condition in the “notopithecines” (Transpithecus obtentus, Notopithecus adapinus, and Antepithecus brachystephanus in the Barrancan) and the elodont condition in the more advanced “interatheriines” (Archaeophylus patrius, Plagiarthrus clivus, Cochilius fumensis, and Progaleopithecus tournoueri from the Deseadan). For Hitz et al. (2000), synapomorphies shared among the advanced taxa of Interatheriinae include a deep parastyle and paracone groove on P2–4, a very shallow parastyle/paracone groove on M1–3, a smooth posterior ectoloph on M1–3, very high- crowned cheek teeth, and distinctly bilobed p3–m3 with persistent labial and lingual sulci. These dental characters can plausibly be correlated with increasing crown height. In the Mustersan at GBV-3 (38.0 Ma) occur Guilelmoscottia, Antepithecus, and something similar to Eopachyrucos. It is the material of Eopachyrucos at GBV-3 that indicates that the evolutionary increase in crown height in interatheres started at about 38.0 Ma in Patagonia. At GBV-4 La Cancha (33.6 Ma), Guilelmoscottia, Santiagor- othia, Proargyrohyrax, and Eopachyrucos all occur. Eopachyrucos and something similar to Santiagorothia have been found at GBV-19 La Cantera (30.8 Ma). All Deseadan and Colhuehuapian interatheriine genera (e.g., Archaeophylus, Plagi- arthrus [includes Argyrohyrax], and Cochilius) have cheek teeth that do not form closed roots (i.e., are fully ever-growing), have more prismatic cheek teeth that do not change proportions or become more equidimensional with wear, and have ephemeral labial fossettes on the upper molars.

2.3.3.4 Notohippidae Among Notohippidae, there are two plausible evolutionary lineages in Patagonia that demonstrate increasing crown height (Table 2.5). The ﬁrst is the series of small taxa in temporal succession based on a comparison of maxillary molars: Eomorphippus pascuali (AMNH 29405 fn 147 from 2’ under U Channel beds at M), Patagonhippus dukei from GBV-19, and Rhynchippus pumilus (AMNH 29579 Scarritt Pocket), without any accompanying change in size. In the upper cheek teeth, an increase in the disparity between enamel height on the buccal and lingual sides of the crown (“unilateral hypsodonty”) is observed, whereby the buccal enamel of the ectoloph becomes much higher than the lingual enamel (Figure 2.10). Part of this process of increasing crown height with more pronounced disparity in the height of the buccal and lingual enamel is 2.3 Hypsodonty in the middle Cenozoic of Patagonia 47

Table 2.5 Hypothetical temporal successions of a small-sized and medium-sized lineages among Notohippidae at Gran Barranca and elsewhere in central Patagonia in approximate temporal order from oldest (bottom) to youngest (top)

Sequence Small-sized lineage Medium-sized lineage

Scarritt Pocket Rhynchippus pumilus AMNH 29579 Cabeza Blanca Rhynchippus equinus AMNH 14152 GBV-19 La Cantera Patagonhippus dukei Patagonhippus canterensis Cañadon Blanco Eomorphippus obscurus (“Eurystomus stehlini”) MLP 12–1508 La Cancha level ?Eomorphippus Eomorphippus obscurus at Gran Barranca Proﬁles M and K AMNH 29462 AMNH 29474 (148) Below Discontinuity 6 at Proﬁle M “Eomorphippus” pascuali AMNH 29405 GBV-3 El Rosado Puelia plicata Barrancan SALMA at Gran Plexotemnus complicatissimus Barranca MACN A55–1

a corresponding diminution in the anterolingual cingulum, early isolation and loss of the fossettes, and early closure of the lingual fold. In this hypothetical lineage, the morphological evidence of temporal succession hinges on the relative stratigraphic position of fn 147 (AMNH 29405) from 2’ under U Channel beds at M and fn 146 (AMNH 29462) from the “pink beds” just under U Channel at M. The ﬁrst specimen 29405 is much lower crowned than the second 29462, suggesting that this was a rapid pulse of increasing hypsodonty. Perhaps bearing on this is the stratigraphic position of fn 148 (AMNH 29474) from the U Channel beds at M collected by Coley S. Williams on November 20, 1930 and the provenance of “Pseudostylops subquadratus” in the Feruglio collection. There are casts of “Pseudo- stylops subquadratus” (¼Eomorphippus obscurus) from the Feruglio collection at the University of Padova, Italy, in the AMNH. This specimen (a maxilla with P2–4 and M1–2, with P3 and P4 broken) is from GBV-4 La Cancha as reconstructed from Feruglio’s section. The anterior dentition, in its preserved parts, is reminiscent of the anterior dentition of Argyrohippus fraterculus (AMNH 29685h fn 28) in general conformation, thus establishing that this is indeed a notohippid. It is otherwise very different from A. fraterculus, in having an erupting maxillary canine (there is no canine in A. fraterculus), a short diastema between the C and P2 (much shorter than the I3–P2 diastema in A. fraterculus), and none of the teeth in the Padova specimen are covered with external cementum. A comparison of the upper molars of “Pseudostylops subquadratus” to those of AMNH 29462 reveal important differences in crown pattern and crown height. These were enigmatic times of rapid evolutionary radiation for the Notohippidae. Thus, at the GBV-4 La Cancha level, there were two different 48 Hypsodonty in the South American fossil record

notohippids, “Pseudostylops subquadratus” (an adult) and another AMNH 29462, both of which have been called Eomorphippus obscurus. AMNH 29405 (fn 147) is one of the “Eomorphippus” remains collected by Coley Williams at Profile M. This is labeled “?Eomorphippus” pascuali and it is an unusual animal in that M2 and the three premolars have much higher-crowned ectolophs than M1, making M1 the lowest crowned cheektooth position. There is a world of difference between the crown height on this specimen (?E. pascuali) and that of AMNH 29462 (E. obscurus), even though AMNH 29462 is a juvenile with unworn encrypted crowns of P3 and P4 (although shatterred), and one might think it would be tricky to compare to AMNH 29405 (an adult). It is not at all difficult to compare. The M1 and M2 in this juvenile specimen are so high-crowned as to show no evidence for root formation. In addition, the evidently hypselodont crowns of M1 and M2 have completely lost the anterolingual cingulum, which is very prominent on AMNH 29405. Most conspicuously, besides the difference in height of the ectoloph enamel, the central lingual fold extends downward less than half the instantaneous crown height, whereas in AMNH 29405, the lingual fold extends nearly to the base of the crown at the cementoenamel junction on both M1 and M2 in AMNH 29405. Thus, these are two very different animals, and if they comprise a phylogenetic series, there is a whole world of difference in their crown height. One possibility is that AMNH 29405 could be a primitive antecedent of Rhynchippus pumilus (AMNH 29579 from Scarritt Pocket), whereby R. pumilus is a little more hypsodont. While these two specimens are very similar in size, they differ markedly in crown height. If this is an example of an evolving lineage, there is a significant evolutionary increase in crown height between the level of La Cancha (early Tinguir- irican) and Scarritt Pocket (Deseadan). The second hypothetical lineage of larger-sized Patagonian taxa in temporal succession is based on a comparison of mandibular dentition; Eomorphippus obscurus (AMNH 29474 fn 148 Profile M), E. obscurus (MLP 12–1508 from Cañadon Blanco), Patagonhippus canterensis from GBV-19, and Rhynchippus equinus from Cabeza Blanca (AMNH 14152), with a noteworthy evolutionary increase in size between Cañadon Blanco and Cabeza Blanca (Table 2.5). In the lower cheek teeth, one of the salient features is the increase in unilateral hypsodonty, where the relative height of the buccal enamel in E. obscurus at Profile M becomes greater in E. obscurus from Cañadon Blanco, then much greater than the height of the lingual enamel in Rhynch- ippus equinus. AMNH 29474 (fn 148) is a mandible with complete cheek tooth dentition that almost certainly represents a larger animal than AMNH 29405. MLP 12–1508 (the type of Eurystomus stehlini Roth) from Cañadon Blanco that is labeled Eomorphippus obscurus could very well be a younger individual of the same taxon as AMNH 29474. Both are right mandibular rami, and both preserve p2–m3, which can be compared directly. In most particulars, they are comparable, except that the p4 of AMNH 29474 is much less high-crowned than the p4 of MLP 12–1508, suggesting the specimen from Profile M is a more primitive species. While it is more difficult to compare, it would appear that the buccal enamel is higher (there is more unilateral 2.3 Hypsodonty in the middle Cenozoic of Patagonia 49

hypsodonty) in m1 (and may also be in m2 of MLP 12–1508, but most of the m2 and m3 crowns of MLP 12–1508 are embedded in the alveolar bone and not visible. If this is an example of an evolving lineage, there is a noteworthy increase in crown height between La Cancha and Cañadon Blanco. Rhynchippus equinus (AMNH 14152 collected by the Amherst party from Cabeza Blanca) is still more unilaterally hypsodont than MLP 12–1508, with greater contrast between the height of the lingual and buccal sides in the lower molars. If this is an evolving lineage, there was a further increase in hypsodonty between Cañadon Blanco (Tinguirirican) and Cabeza Blanca (Deseadan) in Patagonia.

2.3.3.5 Oldfieldthomasiidae Simpson (1967) recognized five genera: Kibenikhoria (Riochican), Oldfieldthomasia (Barrancan), Ultrapithecus (Barrancan), Maxschlosseria (Vacan), and Tsamnichoria (Mustersan), plus an additional two (?Acoelodus and ?Paginula) with doubt. A hypothetical slight evolutionary trend toward somewhat increased crown height may be seen in the closely related and temporally successive oldfieldthomasiid species Maxschlosseria consumata at Cañadon Vaca and Ultrapithecus rutilans at Gran Barranca. Is it also possible to discern crown height increase in Oldfieldthomasiidae between either Barrancan Oldfieldthomasia debilitata or Ultrapithecus rutlians and Mustersan Tsamnichoria? Tsamnichoria cabrerai (the Mustersan taxon) had not been recorded from Gran Barranca at the time Simpson (1967) monographed the group, although in unpublished notes on the biostratigraphy and on museum labels, Simpson appears to have tentatively identified material of Tsamnichoria at GBV-60 El Nuevo. There is no obvious increase in crown height among Oldfieldthomasiidae from Gran Barranca; that is, between O. debilitata from the Barrancan and the material of ?Tsamnichoria from GBV-60 El Nuevo based on AMNH material. Nor is there any obvious increase in crown height between Ultrapithecus rutilans material from the Barrancan and the material of ?Tsamnichoria from GBV-60 El Nuevo that was tentatively referred to as U. rutilans by Cifelli (1985).

2.3.3.6 Notostylopidae Documenting increasing crown height among Patagonian Notostylopidae is problem- atic. There are two specimens with relatively unworn lower molars of Notostylops pendens from Cañadon Vaca (AMNH 28772 fn 68 of 1930 with an erupting m1 and AMNH 28733 fn191 of 1931 with little worn p4 and m1). There are also two relatively unworn specimens of N. murinus from Gran Barranca (AMNH 28727 [fn 215] and 28814 [fn 204]) at a similar stage of wear that substantiate what Cifelli (1985) claimed about somewhat increased crown height in Notostylops between these two localities. In addition, between the Barrancan and Mustersan there is a suggestion of evolutionary increase in crown height between Notostylops pendens (Vacan), N. murinus (Bar- rancan), and material of Notostylops from GBV-3 El Rosado. Comparing AMNH 28582 (fn 82) with AMNH 28592 (fn 236) from GBV-3 El Rosado, which are both maxillary cheek teeth preserving the lingual aspect of the crowns at a comparable stage of wear, there is only a suggestion of an increase in crown height involving the 50 Hypsodonty in the South American fossil record

appearance of a lingual groove on P3, P4, and M1 (see earlier note re AMNH 28961). Thus, by this comparison, there is only a subtle evolutionary increase in crown height between Barrancan Notostylops murinus and the specimen (Notostylops sp.) from El Rosado.

2.3.3.7 Astrapotheriidae Astrapotheriidae experienced a subtle evolutionary increase in crown height during the same interval at Gran Barranca (Figure 2.11). There is a plausible evolutionary lineage that documents a slight but important increase in molar crown height between Albertogaudrya in the Barrancan and Astraponotus in the Mustersan. Since its ﬁrst description, Albertogaudrya (the largest mammal in Casamayoran faunas) has had uncertain status as an astrapotheriid. Ameghino (1904) placed Albertogaudrya into a separate family Albertogaudryidae, and Astraponotus and later genera into Astrapother- iidae. Scott (1937b) thought Albertogaudrya to be the primitive direct ancestor of Astrapotherium, whereas Simpson (1945, 1967) included Albertogaudrya in Trigonostylopidae. Beneﬁtting from larger museum samples of the genus collected in Patagonia between 1956 and 1969, especially at Gran Hondonada, and the partial mandible of a new species from northwestern Argentina, Carbajal et al. (1977) refer Albertogaudrya to the Astrapotheriidae. They argued that the Albertogaudrya dental morphology is what one would expect in the immediate ancestor of Astraponotus. The increase in lower molar crown height between the Casamayoran and Mustersan at Gran Barranca is suggested by a three-taxon hypothetical evolutionary lineage: (1) the type of A. unica (locality unknown?), (2) AMNH 28637 from below Simpson’s Y, which is nearly identical to the type of A. unica, and (3) AMNH 29449 from Coley’s Quarry, referred to as Astraponotus. The increase in crown height occurs between AMNH 28637 and 29449, or between Simpson’s Y and the level of Coley’s Quarry at the base of Simpson’s lower channel series.

2.4 Crown height and the single-chamber stomach in notoungulates

Why is this question important? Hindgut fermenting ungulates have simple single- chamber stomachs for protein and sugar digestion and an enlarged cecum where microorganisms break down and ferment cellulose. The food is chewed only once. It is not as efﬁcient as the ruminant method of digesting cellulose, as evident by the undigested plant material seen in fecal material. By contrast, foregut-fermenting or ruminant artiodactyls (goat, cattle, sheep) have a multichamber stomach. They take in a lot of food in a short time and digest it more slowly and fully. After a quick ﬁrst chewing, food passes into the rumen where it is partially broken down and then regurgitated in small balls, chewed again, and reswallowed. It then passes through the other stomach chambers and intestines for further digestion. The chambered stomach enables smaller food particles to pass through, whereas larger particles of undigested food get re-fermented (Gordon and Illius, 1989; Duncan et al., 1990; Bodmer, 1991; Illius and Gordon, 1992; Pérez-Barbería and Gordon, 2001; Forsyth et al., 2002). 2.4 Crown height and the single-chamber stomach in notoungulates 51

Notoungulates were probably hindgut fermenters, more like Suina (pigs, peccary), which have simple single-chamber stomachs. Two arguments can be made in support of this assertion: phylogenetic afﬁnity and functional or ecological morphology.

2.4.1 Phylogenetic afﬁnity

Many ideas have been expressed in the literature about the outgroup of South American native archaic ungulates, the notoungulates. Crown Notoungulata, as presently consti- tuted, appear to be a coherent monophyletic group. Crown notoungulates including Typotheria (Oldfieldthomasiidae, etc.) and Toxodontia (Isotemnidae, etc.), share a more recent common ancestor. This common ancestor plausibly resides among Henricosborniidae, and as such, Notostylopidae belong among Notoungulata. For the most part, notoungulates are characterized on the basis of a fossil record that is middle Eocene and younger in age. There are no notoungulates in the South American Cretaceous and few if any in the South American Paleocene. Both Itaborai and Rio Chico have notoungulates, but both could be easily accommodated in the early and middle Eocene. On faunal composition and the close phylogenetic affinity with Casa- mayoran notoungulates, Rio Chico and Itaborai faunas are not that much older than the Vacan, but their faunas differ significantly in composition from both Rio Loro and Tiupampa; two faunas that are more legitimately Paleocene in age. On the one hand, the notoungulates from Rio Chico and Itaborai present no problems whatsoever for phylogenetic affinities with later notoungulates. On the other hand, the “ungulates” from Rio Loro and Tiupampa are either bizarrely primitive (Alcideorbignya, Eoastrapostylops)or conventionally primitive mioclaenine condylarthrans. Consequently, we have a huge hole between the earliest Cenozoic faunas (Rio Loro, Tiupampa) and the oldest Eocene faunas (Rio Chico, Itaborai, Vacan, and Barrancan), into which evidence for the broader affinities of notoungulates seems to evaporate. Among native South American “meridiungulates,” possible outgroups to Notoungu- lata include Litopterna (plus Didolodontidae), a coherent monophyletic group with close affinities to Mioclaenidae (Hyopsodontidae, condylarthran). If “meridiungulates” include Litopterna (and their plausible allies), Pyrotheria, and Astrapotheria (Trigonostylopidae plus Astrapotheriidae), meridiungulates are probably not monophyletic. As a more restricted monophyletic group including Notoungulata, Litopterna, and Astrapotheria, probably not either, as Litopterna have a close relationship with Mio- claeninae, but the relationship of Astrapotheria and Notoungulata to that particular group of condylarthran-like mammals is not nearly as well established. However, the most morphologically primitive notoungulate group is the Henricosborniidae, plausibly derived from a condylarthran ancestor. Thus, Meridiungulata (M) ¼ Notoungulata (N) þ Litopterna (L) is more plausible than M¼NþLþA (Astrapotheria). However, the transformation out of condylarthrans is not clear. For Astrapotheria, there is no obvious or convincing ancestral group. There is still no consensus on the phylogenetic position of Notoungulata among other eutherian mammals. Florentino Ameghino (and Stromer and Zittel) proposed a special relationship between notoungulates and hyracoids (Ameghino, 1897; Stromer, 1926). 52 Hypsodonty in the South American fossil record

Gregory (1910) placed Notoungulata among Ungulata along with Protungulata (including Condylarthra), Amblypoda (including Coryphodontidae, Uintatheriidae), Barytheria, Sirenia, Proboscidea, Hyraces, Embrithopoda, Mesaxonia (includes Perissodactyla), and Notoungulata (for Gregory, Notungulata ¼ Homalodotheria, Astrapotheria, Toxodontia, Pyrotheria, plus Litopterna). Simpson (1945) included Notoungulata in his Protungulata along with Tubulidentata, Condylarthra, Litopterna, and Astrapotheria. In Paenungulata, he included Proboscidea, Hyracoidea, Sirenia, Desmostyliformes, Pantodonta, Dinocerata, Pyrotheria, and Embrithopoda. Into an unresolved six-clade polytomy, McKenna (1975) included Tethytheria (¼ Proboscidea, Sirenia, Desmostylia), Phenacodonta (¼ Hyracoidea, Perissodactyla, Condylarthra [emended]), Meridiungulata (¼ Litopterna, Notoungulata, Astrapotheria), and Eparctocyona (¼ Tubulidentata, Arctocyonia, Tillodontia, Dinocerata, and Embrithopoda), but among these resolved no notoungulate sister-group. Szalay (1977) included Meridiungulata in Mesaxonia along with Perissodactyla, Dinocerata, Embrithopoda, Hyracoidea, Proboscidea, Sirenia, and Desmostylia. In his recent phylogenetic analysis of Notoungulata, Billet (2011) resorts to using two a priori out-groups from among nonplacental eutherians Leptictis and Zalambdalestes, and also included non-South American condylarthrans Meniscotherium and Phenacodus. Accommodation for Notoungulata has also been found among Afrotheria (Asher et al., 2009; Agnolin and Chimento, 2011). As suitably primitive ancestors to all “ungulates,” one can find evidence and arguments to recommend Protungulatum for Ungulata. In the same way, a suitably primitive taxon such as Andinodus could be ancestral to all Meridiungulata. One possible approach to the broader affinities of Notoungulata might use the oldest and/or best- known taxa of each of the following six groups as outgroups: GROUP 1, a set of odd archaic ungulates from South America, including Pyrotheria (Carolozittelia), Panto- donta or Uintamorpha (Alcideorbignya, Eoastrapostylops, Etayoia), or Xenungulata (Carodnia); GROUP 2, the condylarthran descendants among South American “ungulates” including Litopterna (encompassing Sparnotheriodontidae, Proterotheriidae, Macraucheniidae, Protlipternidae, and Adianthidae), Hyopsodontidae (Hyopsodonti- dae), and Periptychidae; GROUP 3, the conspicuously similar and the most suspicious from among better known “ungulates” elsewhere, including Paenungulata, Hyracoidea (including Seggeurius from the Eocene of Africa), Perissodactyla, and Phenacodontidae (including Ocepeia from the Eocene of Africa); GROUP 4, primitive African “ungulates” including Tethytheria, Proboscidea (Phosphatherium, Daouitherium, Numi- dotheriidae, three Eocene African taxa), and Sirenia (Pezosiren, Prorastomus are early Sirenians from the Eocene of Jamaica); GROUP 5, archaic “ungulates” with superficially similar dental morphology that often pose as leading candidates for a notoungulate outgroup including North American Arctostylopidae and Asian Paleostylopidae; and/or GROUP 6, the oldest and most primitive known “ungulates” among the Zhelestidae. Another approach would be to look for fossils. What seems true about all these speculations is that notoungulate phylogenetic affinities are not with foregut-fermenting ungulates, as most of the members of these 2.4 Crown height and the single-chamber stomach in notoungulates 53

six out-groups appear to have been herbivores with single-chamber stomachs. Did any South American native ungulates evolve foregut fermentation?

2.4.2 Functional and ecological morphology

Unless there is a clear and unambiguous correlation between the foregut and hindgut fermentation expressed in tooth morphology or the morphology of the masticatory apparatus, there is no way to establish convincingly whether notoungulates were fore- or hindgut fermenters. The literature speculating on the digestive fermentation system in notoungulates is not voluminous. Reguero et al. wrote that “Based on dental morphology, astrapotheres and sparnotheriodontids probably were hindgut fermenters like non-ruminant artiodactyls and perissodactyls” (2013, p. 86), arguing on the basis of the similarity between astrapothere and rhinoceros teeth. However, neither astrapotheres nor sparnotheriodontids are notoungulates; Astrapotheres are a distinct order, the broader afﬁnities of which are as obscure as those of notoungulates, although they may be a proximal sister-group of notoungulates. Sparnotheriodontids seem to be more like litopterns, but they appear early in the Cenozoic and quickly die out without issue. The distribution of fermentation systems among living ungulates reveals that most of the living ungulates, among which are found the best analogues for understanding notoungulate morphology, are hindgut fermenters; for example, rhinos, lagomorphs, hyraxes, sirenians, etc. Foregut fermenters basically are the ruminants (although sloths and kangaroos are included here as well), but these groups provide little in the way of analogous morphologies to notoungulates. Phylogenetically, hindgut fermentation seems primitive among ungulates, and among the out-groups most often explored as sister-taxa to notoungulates. Langer (1987) shows how hindgut-fermenting artiodactyls and perissodactyls dominated herbivore faunas in Europe, Asia, Africa, and North America through the Eocene and Oligocene, with forestomach-fermenting artiodactyls only coming into dominance in the Miocene (in terms of the absolute number of species). The Oligocene was a time of transition, but for that time there are many fossil taxa for which the fermentation system cannot be assumed. Many structures on the occlusal surface of notoungulate teeth probably served for food particle fragmentation. In addition, notoungulates display other mechanisms for increasing the number of shearing blades brought into occlusion during each masticatory stroke, such as crown imbrication. Evolutionarily, as notoungulate cheek teeth become ever-growing and the number of shearing blades decreases because of develo- mental constraints, imbrication and anisodonty seem to increase. Therefore, again, food particle fragmentation is maintained and this emphasis on oral processing suggests that notoungulates may have been relatively inefﬁcient fermenters of vegetable matter. If you accept Janis’ (1995) generalization that hindgut fermenters pass volumes of food, and foregut fermenters can utilize more limited quantities of herbage, and if you accept that the shape of the rostrum and incisor cropping battery correlates with these two modes of feeding (bulk feeders ¼ broad muzzles, selective feeders ¼ narrow or 54 Hypsodonty in the South American fossil record

pointed muzzles), you could not generalize for notoungulates because the diversity of muzzle morphology is a particularly striking feature of notoungulates. Fortelius (1985) points out that ruminant artiodactyls process their food largely as cud, which is soft. Therefore, their teeth are uniformly selenodont, and their cheek muscles are smaller than those of hindgut fermenters that really grind their food before swallowing (3–4 difference for equivalent-sized animals). Hence, these two features provide a morphological distinction between foregut and hindgut fermenters; that is, selenodont versus non-selenodont, and smaller versus larger jaw musculature. Ruminant artiodactyls display relatively little increased crown height, and only in some restricted groups of taxa where it relates to low feeding height above the ground. While ruminants have uniformly lower-crowned molars, they occasionally evolved high incisor crowns, but this feature is related to food acquisition at the soil surface and ingested soil, not to phytoliths. Measurements and observations bearing on the ecological morphology of a suite of diverse living herbivores scored by the fermentation system (foregut, hindgut, or unknown) include variables that may be construed to reflect masticatory muscle mass. For example, temporal fossa width may be understood as an estimator of the mass of the temporalis muscle. In general, notoungulates have very large and conspicuous areas of muscle attachment and muscle scars for masticatory muscles. Additionally, notoungulates have a fused mandibular symphysis. There appears to be some correlation between these features and diet quality. Insofar as hindgut fermenters consume poorer-quality food with shorter retention times, they have larger masticatory muscle mass, whereas foregut fermenters make do with smaller muscles. Hindgut fermenters tend to have higher values for temporal fossa width. Interestingly, this relationship seems to break down for kangaroos (foregut fermenters, albeit non-ruminants) because they consume very poor quality food, and some hindgut fermenters (e.g., the leporids) are more selective feeders. Probably the best argument for whether notoungulates were foregut or hindgut fermenters would note that notoungulates evolved really high crowned teeth, in fact, many evolved rootless ever-growing cheek teeth and ever-growing incisors. Unlike nearly all living and fossil ruminants and most living and fossil ungulates, notoungulates have an evolutionary history that is notorious for the frequency of the appearance of ever-growing teeth. Some living ruminants have fairly high crowned molars (the dry grass grazers), but with only one exception, all living ruminants have low-crowned incisors, even the dry grass grazers. Incisor and molar crown height is low in ruminants because mineral particles rarely come between occluding tooth surfaces, even in ruminants that eat grasses laden with phytoliths. By contrast, herbivores with single-chamber stomachs (or hindgut fermenters) require and rely on the active mechanical processing and comminution of vegetable foods in the oral cavity. This emphasis on oral processing (the cutting of plant food into fine particles) means these animals chew and re-chew grit and phytolith-laden plant material (not grit and largely phytolith-free regurgitated cud). Hindgut fermenters do not chew as much as ruminants. The relatively inefficient mastication and digestion requires 2.5 South America exceptional? 55

them to ingest a larger volume of plant material, and masticate it more thoroughly in the buccal cavity, and consequently, they get more abrasive minerals, especially soil abrasives, between their teeth. This is why perissodactyls that graze and feed close to the ground have higher tooth crowns than ruminants, which have the same feeding habits. Their reliance on oral processing means they pass more abrasives (both intrinsics and extrinsics) between the teeth and in higher concentrations. Any differences between the height of the incisor crowns and molars should reflect the balance between incisor acquisition and molar processing. Foregut (multichamber stomach) and hindgut (single-chamber stomach) herbivorous mammals differ in one feature of skull architecture: foregut fermenters have a smaller masticatory muscle mass than hindgut fermenters (Figure 2.12, top). Temporal fossa width as an expression of masticatory muscle mass, after controlling for body size (total skull length), reveals this essential difference in design. This generalization applies to many different clades of mammals across a broad spectrum of evolutionary history (Figure 2.12, bottom). Typotherian notoungulates (and presumably all other notoungulates) have a skull architecture that is similar to living mammals with single-chamber stomachs (Figure 2.12, bottom). Among Litopterna, proterotheriids have a similarly proportioned skull, whereas Macraucheniidae appear to have a masticatory muscle mass more like foregut-fermenting ruminants. Because ever-growing cheek teeth and incisors evolved so often among notoungulates, notoungulates are unlikely to have been foregut fermenters or ruminators. This feature of notoungulate evolution, the frequency of the evolution of ever-growing teeth, seems to suggest that mineral abrasives were important for the incisor and molar evolution. As an explanation for this evolutionary pattern, both incisors and molars probably encountered soil mineral abrasives. Just as for living ungulates, soil minerals were probably significant for incisor wear in those notoungulates that harvested close to the soil surface, and soil minerals, once ingested and taken into the oral cavity, were probably significant for the molars.

2.5 South America exceptional?

Having established the facts about the prevalence of hypsodonty and its evolution among the native ungulates of South America, we now ask: is there anything exceptional about the prevalence or either geographic or temporal distribution of high crowns among fossil and living South American mammals compared with mammalian faunas on other continents? The oldest high-crowned mammals in South America, the Paleocene Sudamerica and Ferugliotherium, appear to be no older than the oldest records of the evolution of high- crowned teeth in North American Stylinodontidae (Taeniodonta) and in Asian and North American Trogosinae (Tillodontia) (Lucas and Schoch, 1998; Lucas et al., 1998). The oldest occurrence of noteworthy increase in molar crown height among notoungulates in the late Eocene (Patterson and Pascual, 1968; Simpson, 1967; Kay et al., 1999) does not seem to antedate the appearance or evolutionary history of clades in the Asian and North ebvru aml)apa ohv ensml igecabrsoahfretr,smlrto similar fermenters, Perissodactyla. stomach and single-chamber rabbits American simple living South been have archaic to (extinct appear litoptern mammals) herbivorous proterotheriid and notoungulate typotherian the iue2.12 Figure ( eghi ies aiiso xatadetnthrioosmmas otm apeszsas sizes Sample bottom. mammals, herbivorous extinct N and skull Cervidae extant width/total follows: of fossa families Temporal diverse top. in mammals, length herbivorous other with compared mammals rgldeN Tragulidae brasiliensis hooo garrettorum Theosodon TFW/skull length TFW/skull length 0.1 0.2 0.3 0.4 0.5 0.6 0.1 0.2 0.3 0.4 0.5 0.6 0 0 atctr ucems setmtdb eprlfsawdh(F)i ruminant in (TFW) width fossa temporal by estimated as mass muscle Masticatory ,Tptei N Typotheria ), Cervidae ¼ 1(

rglsjavanicus Tragulus Bovidae ¼

,BvdeN Bovidae 4, Caviomorph oeu idu Unknown Hindgut Foregut N=19 ,Poeohria N Proterotheriidae ), ¼

1( Leporidae icciisanamopodus Miocochilius

Typotheria ¼ ,CmldeN Camelidae ), ,Cvoop N Caviomorph 8,

Procaviidae ¼ 1( N=6

rtrteimcavum Proterotherium Suidae

¼ Tragulidae 1( ¼ ,LprdeN Leporidae 4, Vicugna ,PoaideN Procaviidae ), Camelidae Macraucheniidae ,McaceideN Macraucheniidae ), Proterotheriidae N=8 .B hslmtdsample, limited this By ). ¼ 1( ¼ ,Sia N Suidae 2, Sylvilagus ¼ ¼ 1 2, 2.5 South America exceptional? 57

American fossil records; for example, Leporidae, Leptocheniinae (Mericoidodontidae), Castoridae, Geomyidae, and Heteromyidae (Lander, 1998; Lopez-Martinez, 2008). Thus, in terms of oldest temporal occurrences and examples of the evolutionary transformation, South America does not appear to be unique. If not antiquity, is the prevalence of hypsodonty among South American mammals exceptional geographically? Most of the area of South America presently is covered by humid and wet forest at tropical latitudes, and presumably was so during much of the Cenozoic (Burnham and Johnson, 2004). Moreover, the total area of natural grasslands is less than in other continents (Gibson, 2009). However, a portion of South America’s open-habitat is mountainous, and almost all of the area of open-habitat in the Andes is under the influence of active erosion and volcanism. In part, the myopic perspective of this book is its use of the evolutionary history of South American mammals as exemplars. South American mammals evolved in relative geographic isolation and their evolutionary history, therefore, is largely a response to changing climates and environments and not an artifact of the immigration of new taxa. Furthermore, middle Cenozoic immigration events (caviomorph rodents and primates) and the Great American Biotic Interchange (GABI) introduced many clades that adapted to South American environments by evolving high tooth crowns. While the prevalence of hypsodonty was noted in the early literature on South American paleontology (Ameghino, 1904; Scott, 1913), the search for the cause of evolutionary hypsodonty was first commented on in the European scientific literature by Kovalevsky, Owen, and Huxley, and the most important examples from the Holarctic fossil record are horses and beavers described by Matthew, Stirton, and MacFadden, among a host of other authorities. In addition, excess tooth wear in living mammals was first reported and studied in New Zealand, not South America, indicating that this particular problem is certainly not unique to South America, where it may not be as economically important to the domestic animal industry as it is elsewhere. The introduction of “European” domestic livestock into South America was also rapid and their success was established in early colonial times. Prior to the arrival of the Spanish, the interior area of the Pampas of Argentina was inhabited by nomadic Amerind hunters, exploiting deer and guanaco. Both these mammals arrived into South America during the Great Biotic Interchange, sometime around the Uquian. Spanish cattle were not successful immediately in the Pampas. The well-equipped expedition of Pedro de Mendoza established a colony at Buenos Aires in the first half of the sixteenth century (1535–1536), but this attempt was an utter failure and abandoned by 1541. A second attempt in 1580 proved more successful and Buenos Aires existed thereafter for two centuries as a small settlement separated from the interior by the Rio Salado. During this period, stock raising supported a very sparse population of 400 houses in 1657 that only slowly increased to 13 000 rural and 25 000 inhabitants in town in 1778. Great herds of horses and criollo cattle developed much later (McCann, 1852). One hypothesis for the delayed development of a domestic grazing ecosystem is that only following the introduction of European plants, could cattle and horses achieve 58 Hypsodonty in the South American fossil record

success in the Pampas. Why this might be the case is an interesting question. Members of Pedro de Mendoza’s expedition, the first Europeans to see the Pampas, described it as a treeless prairie. The original grasses were tall pasto duro in which species of the grass genus Stipa predominated. Referred to as pastos altos y pajonales, the grasses were burned initially to obtain fresh sprouts as feed for the cattle. The plant association of pasto agrio sour reed grass on swampy soils combined with high pampas grass Cortaderia argentea occurred in cortaderales, areas burned by travellers to open a pathway. It is thought that the persistent root smoldering of these fires contributed to produce the tierra cocida of the upper levels of the Pampa Formation. The dramatic alteration of the natural grasslands of the Pampas into cattle pasture occurred a pata y diente, and was accompanied by plant introductions from Europe. The grasslands that developed were short-grass prairies composed of introduced pastos tiernos or pasto blando that formed a low dense sod. These short-grass praries were composed almost exclusively of introduced European plants such as the grasses Poa, Lolium, Avena, Hordeum, Cynodon, soft herbs, clover, hemlock, fennel, and others. Darwin noted the difference between tall (original) and short (introduced) grass pampas upon crossing the Rio Salado and was “very much struck” with the marked change in the aspect of the country and noted that “from a coarse herbage we passed on to a carpet of fine green verdure...attributed to the manuring and grazing of the cattle.” Hence, what is unique about South American hypsodonty? The available fossil record suggests that hypsodonty arose in South America among many terrestrial mammalian herbivore clades, and the record of independent evolutionary events of hypsodonty continued through the Cenozoic. The gradual accumulation of hypsodont mammals increased through the middle Tertiary and into the late Miocene. Hypsodonty also evolved in mammals that arrived to South America during the GABI. While this is just a suspicion, the prevalence of hypsodonty and fully elodont mammals is unequaled on any other landmass. Moreover, their accumulation in the fauna occurred relatively early and high faunal hypsodonty was maintained throughout the Cenozoic; a record of continuity not matched elsewhere. If South America is exceptional as a geographic area of high hypsodonty, is there anything unique about South American geography that might suggest an explanation? If South America is exceptional as a geographic area of high hypsodonty, to what can it be attributed? Given what has been speculated in the literature, it might be attributed to any or all of the following: (1) high phytolith abundance in especially coarse grasses; (2) prevalence of plant life-forms and leaf surface properties; (3) high levels of soil exposure, disturbance, or susceptibity to erosion; and (4) prevalence and wide distribution of sources of mineral sediment, such as continuously available accumulations of volcanic ash and dust subject to erosion–entrainment–transport–deposition cycles sustained over evolutionary timescales. 3 South America and global hypsodonty

3.1 Mammalian hypsodonty in South America

3.1.1 Introduction and approach

To explore the environmental correlates of hypsodonty in South American mammals and analyze the strength of association between hypsodonty and the environmental variables that have been proposed to explain the precocious hypsodonty of the late Eocene, frequency distributions, bivariate linear regression, and unimodal multivariate methods are used here to analyze patterns of hypsodonty among living mammals of South America. For this exploration, the diet of 559 non-volant South American mammal species have been compiled and classified, based on published studies. Although the diet has been described for only 259 of 559 (or 46%) of the species used in this analysis, and the range of methods, quality, and completeness of the descriptions of diet are highly variable (see later), as an expedient partial remedy for this deplorable ignorance about the foods mammals eat (the basic facts of the trophic pyramid), all species of a genus are assumed to have the same diet. This expedient enables 530 species (about 95%) to be classified. For mono-specific genera where diet is unknown, the species is excluded from analysis. [At this point, I expect serious zoologists will close the book and turn to other tasks. After all, who but a nut would ever build a meaningful theoretical edifice on such inadequate data? But, I implore you to suspend judgment and continue reading, as I hope to convince you that diet is rather meaningless to this inquiry, and that what might matter more than food in the evolution of tooth crown height and enamel volume are the mineral particles ingested with the food.] Each species was also classified into low- or high-crowned tooth classes. Crown height could be classified for only 474 (or 85%) of the total number of species. Of these, 191 species (or 40%) were classified as hypsodont (including all xenarthrans). Of the 121 species of Sigmodontine rodents classified by crown shape, 24 (or 20%) are considered hypsodont here. Sigmodontines were scored as “hypsodont” if they are reported to display greater cheek tooth crown height than found in oryzomyins, the living group most closely related to the presumptive ancestral group. Braun (1993) scores upper molar crown height in 40 species of Sigmodontinae (principally

59 60 South America and global hypsodonty

phyllotines) as either 0¼brachydont or 1¼hypsodont (relatively high-crowned). Within the “subhypsodont to mesodont” Akodontini, Reig (1987) described the molars of Bolomys as “mesodont,” Geoxus as “brachyodont,” Chelemys as “relatively hypsodont,” Abothrix with “moderately well-developed tubercular hypsodonty and a slight crown hypsodonty,” and Akodon with “moderately developed hypsodonty.” From these basic data, summary variables were compiled, including (1) the percentage of mammal species that are hypsodont in each of nine diet categories for each of 80 sites, (2) the number and percentage of South American sigmodontine species that are hypsodont, (3) the number of mammal species that are brachydont, (4) the number that are hypsodont, and (5) the proportion (%) that are hypsodont. The number of hypsodont species at any site is either the result of in situ evolution or immigration, and the likelihood of each of these changes with the phylogenetic antiquity of its first evolutionary appearance. On the assumption that active evolution of hypsodonty is more likely to still be occurring among more recent arrivals into South America, the distribution of hypsodonty among sigmodontines may be a more sensitive indicator of geographic or environmental causation. Mammal species occurrences were then compiled from faunal inventories at 80 sites or localities across South America (Figure 3.1). For each site, 26 environmental variables (20 continuous, 6 nominal) were also compiled. The environmental variables include those associated with plant tissue toughness (seasonality, dry days, summertime rainfall, severity of winter), general aridification (mean annual precipitation, precipitation seasonality, water balance, potential evapotranspiration), proximity to sources of environmental abrasives (volcanic ash soils, altitude, topographic relief), climate features that influence mineral particle mobility (windspeed, vegetation cover), and environmental variables that are either preserved in the marine and terrestrial rock record or discussed in the climate modeling literature (mean annual temperature, temperature seasonality, latitude, photoperiod, solar radiation). Continuous environmental variables include: latitude (LAT), altitude (ALTITUD), mean annual temperature (MAT), coldest month mean monthly temperature (MINMMT), annual amplitude of the mean monthly temperatures (TEMPAMP), mean annual precipitation (MAP), annual amplitude of mean monthly precipitation (AMPMMP), dry days (DRYDAYS), annual potential evapotranspiration (ANNPET), amplitude of monthly PET (PETAMP), total annual radiation (ANNRAD), amplitude of mean monthly radiation (RADAMP), average annual windspeed (WIND), diurnal temperature amplitude (DTEMPAMP), growing degree days above 5 C (GROWDD), summertime rainfall rate (JANRRATE), water balance surplus (SURPLUS), total relief within 100 km radius (RELIEF), photoperiod (SDPHOTO), and water balance deficit (DEFICIT). The nominal variables include: open, closed canopy, trees dispersed, woodland mosaic, trees present, and volcanic ash soils (ANDISOLS). The distribution of andisols (or andosols) in South America closely agrees with areas of active pyroclastic volcanism (Leamy, 1984; Shoji et al., 1993), as indicated by the mapped distribution of andisols in South America (Eswaran et al., 1992; FAO (Food and Agriculture Organization), 2003) and the andisols of Moscatelli and Pazos (2000). Other areas where volcanic ash or glass comprise a significant proportion of soil parent 3.1 Mammalian hypsodonty in South America 61

Figure 3.1 Mammal fauna inventory sites (right) and the geographic distribution of active volcanoes (left) in South America. Andean elevations >1000 m in solid black.

material include central Patagonian aridisols, Puna soils of NW Argentina, the western Cordillera and Altiplano of Bolivia and southern Peru; and soils derived from the Pleistocene cangagua aeolica of highland Ecuador. These are all considered “andisols” here. Of the 80 sites, fifteen are on volcanic ash soils in areas of the Andes under the direct influence of active volcanism. These sites include Los Glaciares, Perito Moreno, Bosque Petrificado, Los Alerces, Lago Puelo, Nahuel Huapi, Los Arrayanes, Lanin in Patagonia in the Southern Andean Vocanic Zone; Salta Puna, Eduardo Abaroa, Huajara, Bolivia Puna, and Peru Puna in the Central Andean Volcanic Zone; and Ecuador Temperate, Ecuador Andean in the North Andean Volcanic Zone. 62 South America and global hypsodonty

Covariables express some of the obvious sources of variation or noise underlying the sampling of species richness in faunal inventories, including the area sampled and the intensity of the sampling effort. The surface area inventoried or included in the elaboration of mammal species lists varies across the 80 sites, as does the kind and relative intensity of sampling during the elaboration of the faunal inventories. Sampling effort was summarized using four categories that describe the intensity and diversity of methods used: (1) rapid survey (such as undertaken during the Rapid Assessment Program), (2) inventories undertaken by government ministries using a combination of museum and published records supplemented by usually limited fieldwork, (3) intensive inventories that devote more time and a wider diversity of field methods to the elaboration of a species list, and (4) exhaustive efforts the goal of which is a comprehensive and definitive list of mammal species elaborated during extended multiyear fieldwork. As local climate is rarely measured at inventory or survey sites, meteorological or agrometeorological station data is substituted. The selection of a meteorological station from among the nearest or closest stations to sample sites introduces geographic error expressed here as a combination of the distance in latitude and difference in altitude between the site and station. Area and error are continuous covariables, whereas sampling intensity (rapid, inventory, intense, and exhaustive) is a nominal covariable. Before presenting the results of this analysis, it is sobering to consider how the diet of mammal species is described in conventional zoology and how this is thought to relate to tooth shape.

3.1.2 Diet classiﬁcation

The ecological structure of biota or communities of living organisms is often depicted as a trophic pyramid with plants at the base and above which are primary consumers, secondary consumers, and at the apex, top predators. The pyramid rests on the Earth’s surface. The ﬂow of energy and nutrients through the living world begins with soil minerals and sunlight, and through photosynthesis to sugars, structural carbohydrates, and plant proteins at the base of the pyramid, and from here ascends to animal tissues through the consumption of plant parts by animals. This wider web describes the interaction between the planet (geosphere) and components of the biosphere (plants and animals). A fundamental part of the description of nature in botany and zoology is the study of the interaction between levels of the trophic pyramid. It is not possible to understand the interdependency, or movement of energy through the living world without studying these interactions or transformations, and without knowing what passes from one level of the pyramid to another. The study of animal ecology is essentially the study of the ﬂow of energy from plants to animals or the interactions between an animal and its surroundings mediated by foods, the distribution, availability, variety, and changes in foods across the seasons and from year to year. In zoology, there are 10 general categories of mammal diet, including: carnivory (vertebrate muscle and soft tissues), insectivory (the digestible portions of insects and arthropods), animalivory (which includes all forms of secondary 3.1 Mammalian hypsodonty in South America 63

consumption), omnivory (when diet includes both plant and animal components), herbivory (the consumption of all kinds of plant parts), folivory (mostly leaves), and grazing (mostly leaves of grasses). These categories are not mutually exclusive, as there are few if any mammals that eat one broad type of food solely and exclusively, unless, of course, we make the generalization so broad as to be almost meaningless (such as primary or secondary consumer). Some examples of studies of mammal diets taken from the scientific literature illustrate something of the variety of approaches used in the study of mammal diets. The two examples illustrate one important thing. Despite the fact that the study and description of animal diet has long been part of animal ecology, the techniques or methods used in the study of animal diet have become standardized only recently (but are still heterogeneous in practice), and categorization is an often misleading way of understanding diet. For example, M.G.M. Van Roosmalen spent three years studying the diet of the monkeys in a national park in Surinam and wrote inspiring and influential books describing the plants, leaves, flowers, buds, and fruits consumed by the monkeys (1980, 1985). This work is among the most important publications ever produced about the patterns of tropical forest food availability and plant phenology in relation to mammal diets. It is probably the best description of the diet of any tropical forest primate or mammal. While there is a lot of interest about primate diets, rodents comprise the largest portion of total non-volant mammalian species richness in South America, from 19% to 79% of total richness (mean 35%), and within the dietary classes of herbivory, insectivory, omnivory, and especially granivory, rodents comprise a significant part of total richness. Sigmodontinae (Muridae) comprise 41% of all rodent species in South America, and the proportion ranges from 14% to 93%. Some Sigmodontine (Muridae, Rodentia) clades have strong associations with major altitudinal biomes in Andean South America; for example, Oryzomyini and Echimyidae are usually restricted to tropical and subtropical elevations, Thomasomyini to intermediate montane elevations, and Akodontini and Phyllotini to highland Andean environments. Hershkovitz’s(1962, 1969) association of sigmodontine clades with sylvan and pastoral biomes is based on his perception of a relationship between environment and tooth morphology. While rodents comprise the largest portion of total non-volant mammalian species richness in South America, they are among the least well known in terms of their dietary habits. In particular, South American Muridae, after their dispersal into South America, have come to occupy most all geographic areas of the continent and have radiated into nearly all modern ecological life zones. Their most conspicuous dental specializations are thought to reflect these diverse habitats and diets (Hershkovitz, 1962). In tooth shape, Sigmodontinae range from bunodont (Calomys) to hypsodont (Punomys, Chinchilulla). By virtue of their relatively recent introduction into the continent, Muridae present a pattern of adaptive response less masked by subsequent evolutionary change, and thus are a more useful model for the study of geographic or ecological variation in dental and masticatory morphology. 64 South America and global hypsodonty

Table 3.1 Characteristics of the three study sites represent contrasting environments in terms of general climate, soil type, modern plant community, and potential sources of environmental abrasives

Study site LAT ALT MAP MAT MMT Amp

Peru 16 3800 89–554 <8.4 3.4 Chile 41 710 >3000 <10.3 7.6 Argentina 36 66 953 16.4 14.5

LAT, south latitude, ALT, altitude (m), MAP, mean annual precipitation (mm), MAT, mean annual temperature (C), MMT Amp, annual amplitude of mean monthly temperatures (C).

Rodent diets have been described broadly as opportunistic and omnivorous (Landry, 1970), but there are temporal and spatial differences in the proportion of major food tissue types and plant species in the diets of species of Sigmodontinae (Pizzimenti and De Salle, 1980; Meserve et al., 1988; Ellis et al., 1994; Ellis, 1996). Something of the complexities of sigmodontine diet have been revealed through the study of stomach contents and the contents have been described for 519 individuals of 16 species of Sigmodontinae from three contrasting study sites in South America (Table 3.1). The adjusted percentages of broad food classes for these species vary by the composition of leaf, seed, and insect components (Figure 3.2). However, the description of diet by stomach content analysis is subject to biasing by methodological differences, different digestive rates, and the identification and manner of quantification of fragments (Rosenberg and Cooper, 1990). For example, percentages of food types for Sigmodontinae are not directly comparable, as Meserve et al. (1988) calculate percentage volumes based on area or percentage cover of identified food fragments whereas Ellis (1996) based volumes on frequency of occurrence.

3.1.2.1 Chile Meserve et al. (1988) studied sigmodontine diets in the temperate Nothofagus (southern beech) Andean rainforest of Osorno Province, Chile. The study area is near Refugio La Picada (41 S, 72.5 W) in a west-facing valley that drains the north slope of the active Volcán Osorno in Parque Nacional Vicente Pérez Rosales. Historical eruptions of Volcán Osorno have been registered as early as 1575 and while its last recorded eruption occurred in 1869, nearby Volcán Calbuco last erupted in 1961. The vegetation at the study site was described by Meserve et al. (1982, 1988), and Patterson et al. (1990). Specimens were trapped at altitudes between 425 and 1135 m. For each trapping site, six habitat values were recorded (canopy height, number of large trees, number of logs, number of large logs, number of shrubs, number of large shrubs). Individuals of ten species of small mammals were snap-trapped (kill-trapped) at two- month intervals over two years (Meserve et al., 1988). Excised stomachs were ﬁxed in 10% formalin or 100% ethanol and then transferred to 50% ethanol–methanol solution. The stomach contents were removed, washed with water over silkscreen and physically homogenized. Three subsamples were spread on microscope slides, boiled a few 3.1 Mammalian hypsodonty in South America 65

0 1

0.2 0.8

Seeds (%) 0.4 0.6

Leaves (%)

0.6 0.4

0.8 0.2

1 0

1 0.8 0.6 0.4 0.2 0

Insects (%)

Figure 3.2 Ternary or de Finetti diagram of diet components in 16 species of Sigmodontinae from study sites in Peru (crosses), Chile (closed circles), and Argentina (open boxes). (See Table 3.1 for a brief summary of the general environment of these three sites.) seconds in Hertwig’s solution, cooled and then covered with a cover slip. On each slide, 10 randomly located fields were examined at 100 magnification in a conventional light microscope. The area percentage was determined for all fragments to the nearest 20% using a calibrated micrometer disc with 0.1 mm intervals. Open spaces not included in area estimates and optical fields with <50% of the area occupied by fragments were excluded from measurement. An identification key was made from reference material collected for most of the plants (include seeds, fruits, and flowers) in the forest and their fragments found in the animals’ stomachs. From these, thin sections were prepared and mounted on microscope slides. The results were tabulated and summarized for each individual, and from this data, bimonthly and overall average diets were calculated for each species. Sixty-nine categories of food items were distinguished during scoring and these categories were combined into 18 broad categories by food type. Dietary results 66 South America and global hypsodonty

were simplified further by combining categories into three broad classes in de Finetti diagrams: (1) animal (include arthropods, annelids, and all other foods of animal origin), (2) vegetation and fungi (include epidermal foliage tissue, vascular and structural tissue, all fungi), and (3) seed, fruit, flower, or pollen. Percentages of total identified material were interpreted as a measure of food volume in the diet and these percentages were adjusted to 100% by excluding unidentified material, bait, sand, and rock.

3.1.2.2 Peru John Pizzimenti and Robert De Salle (1980) described the diet in 13 species of Sigmodontinae based on the stomach contents of 144 specimens collected at nine localities in Arequipa, Puno, and Cuzco departments, in southern Peru, between Febru- ary 15 and May 9, 1976. Most were trapped on the Andean puna highlands near Juli in Puno Department. The general geography of this part of southern Peru has been described by Bowman (1916), and Pearson (1951) provides additional information about the trapping areas in Puno Department (Cailloma, Santa Rosa, Hacienda Pairumani). In Arequipa Department (including trapping sites at Cailloma, 10 km west of Chiguata and in the altiplano between 3700 and 4400 m altitude near Chivay) are rock-strewn habitats dominated by low Tola shrubs and sparse coarse grass. In Puno Department, trapping sites were between 4100 and 4500 m elevation near Santa Rosa and Hacienda Pairumani, in Stipa ichu bunch-grass and forb or puna habitats in the western Cordillera west of Lake Titicaca. In Moquegua Department, trapping sites were between 3000 and 4600 m elevation near Torata. In Tacna Department, trapping sites were between 3400 and 4200 m elevation at Tarata. In Cuzco Department, rodents were trapped at Machupicchu, in upper montane ceja. The trapping sites at Arequipa and near Juli are on volcanic ash soils receiving significant aerosol ash from eruptions of El Misti (5822 m), Ubinas (5672 m), and nearby volcanic centers in the western Cordillera where the last recorded eruption occurred in 1969 (Smithsonian Volcano Inventory). The digestive systems were dissected and preserved in ethanol and their contents were described following Hansson (1970). Large items >1 mm were macerated and recombined with pulp prior to analysis. The contents were placed on fine mesh cloth stretched over an embroidery hoop, thoroughly mixed, and briefly washed under tap water to remove digestive juice and dissolved starch. A pea-sized sample was placed on a3 1 inch glass slide and heated gently with Hertwig’s solution to facilitate identification of vegetative species by epidermal characteristics. This material was spread evenly over the slide, covered, and then examined at 100 and 400 magnification. Food items were drawn or photographed for comparison to reference slides made from vegetative samples taken at the same locality. The items were identified as insect, seed, or leafy vegetation, and leaf material was subdivided into grasses and non-grasses on the basis of cell shape. The small quantity of unidentifiable material was ignored. For each stomach, 15 random optical fields (100 magnification) were analyzed using the relative frequency method of Hansson (1970) (relative frequency of each item ¼ frequency sighted/frequency of all food items sighted) by estimating relative ocular area covered by each item as a percentage of each microscopic field. 3.1 Mammalian hypsodonty in South America 67

3.1.2.3 Argentina Ellis (1996) described, in detail, the food habits of Calomys musculinus and C. laucha (Phyllotini), Akodon azarae and Bolomys obscurus (Akodontini), and Oligoryzomys flavescens (Oryzomyini) at a site in the non-volcanic humid pampas of Pergamino in northern Buenos Aires Province, in a nearly level rolling plain (pampa humeda ondu- lada) less than 100 m above sea-level, with predominantly internal drainage and a high water table. The deep fertile pampas soil parent material is very fine windblown loess with high soil phytolith content. Pergamino has a characteristically long growing season, mild humid subtropical climate with a mild winter and hot summer, adequate rainfall, no dry season, and soil moisture that varies with precipitation and time of year. Originally the area was described as tall-plumed grassland prairie and marshland, but is presently under an intensive crop–livestock production system. Crop rotation involves alfalfa, sorghum, or natural and recycled grassland pasture. Agricultural mechanization is widespread and involves mechanical plowing and harvesting but no weeding (high weed populations are characteristic). Based on a thorough analysis of stomach contents in individuals collected over a 15-month period between August 1, 1989 and October 31, 1990, histological features of epidermal cells, and specialized epidermal cell types used to identify plant fragments, and general procedures followed Holechek (1982) and Sparks and Malechek (1968). Reference plants were collected at peak growing period, and grasses were collected at flowering. The stomach contents were first rinsed through a 1 mm screen, then a sample was placed on a slide, Hertwig’s solution added, heated to boiling over a flame, cooled, and allowed to evaporate. With several drops of Hoyer’s solution, the sample was placed on a slide, mixed, covered, and heated to boiling, cooled, and then oven-dried (60 C, 1 week). Five slides were prepared from each stomach, 20 non-overlapping, systematically spaced fields were read under a phase contrast microscope at 125 (100 microscope fields per sample, a field being the area of a slide visible under a microscope at 125 ). Twenty observations of five slides per sample provided 80%–90% confi- dence that estimates were within 10% of the mean for plant species that comprised 20% or more of the diet. The presence and frequency of occurrence of each food item was recorded (not the number or size of pieces) and a relative frequency for each dietary item was obtained for each stomach. Relative frequency was defined as the number of occurrences of an item/number of occurrences of all items. Frequency was defined as the number of fields in which the diet item occurred among the 100 fields examined. Ellis et al. (1994) reported that “the relative volumes of seeds, vegetative material (stem, foliage, or root), and insects (larval or adult) were determined for all stomachs” and the frequency of occurrence and percentage volume of major food species in the stomach were examined by species and season. General food categories included: (1–4) monocot and dicot seeds and leaf, (5) all other plant organs combined (flowers, stems, fruits, roots), (6) invertebrates (mostly insects), (7) other food types (vertebrate muscle, earthworm, feathers, filamentous fungi, moss, higher fungi), and unidentifiable items. Using these protocols, the diets were described for 16 sigmodontine species at the three study sites in South America (Table 3.2), and the following comparisons were made. 68 South America and global hypsodonty

Table 3.2 Principal constituents of the diet by volume (approximate percentages) in South American species of Sigmodontinae (Rodentia, Muridae)

Fruit Dicot Monocot and Summary Diet Species Tribe leaves leaves Seeds Insects fungi Description

Phyllotis Phyllotini 37 15 13 35 Dicot leaves and darwini insects Phyllotis osilae Phyllotini 22 31 26 20 – Grass leaves and seeds Chroeomys Akodontini 42 19 4 35 – Dicot leaves and jelskii insects Akodon Akodontini 6 8 8 78 – Insects boliviensis Akodon azarae Akodontini 8 10 32 53 Insects and seeds Calomys laucha Phyllotini 8 12 56 27 – Seeds and insects Calomys Phyllotini 10 10 53 26 Seeds and musculinus insects Bolomys Akodontini 7 24 40 33 Seeds and obscurus insects Oligoryzomys Oryzomyini 10 14 55 20 Seeds and ﬂavescens insects Akodon Akodontini 3 1 22 35 38 Fruit and insects olivaceus Akodon Akodontini 2 1 14 35 48 Fruit and insects longipilis Akodon Akodontini 2 2 7 46 43 Insects and fruit sanborni Oligoryzomys Oryzomyini 2 – 60 18 20 Seeds and fruit longicaudatus Irenomys Phyllotini 14 14 42 3 26 Seeds and fruit tarsalis Auliscomys Phyllotini 6 9 31 2 53 Fruit and seeds micropus Geoxus Akodontini 6 4 5 85 – Insects valdivianus

To convert geographically isolated descriptions of mammal diet to an adaptive landscape, we would need to relate change in the physical properties of plant tissues to environmental gradients. From the literature of physiological plant ecology (Larcher, 1995;Lüttge,1997), some plant tissue types can be expected to vary with moisture, temperature, atmospheric humidity, altitude, solar radiation, and productivity (or fertility), but for some classes of plant tissue, how physical or mechanical properties vary over geographic or environmental gradients is not well known (Table 3.3). Table 3.3 Plant tissues and their physical or mechanical properties along environmental gradients

Productivity (fertility) gradient (above Atmospheric Solar radiation ground net primary Plant tissue Moisture Temperature humidity Altitude (irradiance) productivity)

Stem cellulose Thicker bark in dry climates Thicker insulation Increased ratio of stem to leaf layer, fewer but allocation to stem biomass? thicker stems in in low light4 cold climates2 Cellulose Parenchyma to collenchyma to sclerenchyma (thickened

to ligniﬁed cell walls) in dry America South in hypsodonty Mammalian 3.1 climates Leaf epidermis Thicker with decreasing Thicker with Thicker with Thicker and more rainfall; C4 more dominant in decreasing increasing glaucous with drier climes humidity elevation increasing (humid irradiance mountains) Solid silica Increased soil moisture leads Low temperatures Phytolith size and Phytolith production in to greater Si uptake1 (4 C) suppress Si angularity varies crops increases with assimilation3 in sun and shade ANPP6 leaves5

1 Mayland et al., 1991 2 Kingdon, 1989 3 Liang et al., 2006 4 Poorter et al., 2012 5 Dunn, 2013 6 Song et al., 2013 69 70 South America and global hypsodonty

The prevalence of mammalian tooth shapes can be expressed geographically (as can tooth wear), and any ideas we may have about the relationship between tooth shape or wear and the mechanical properties of foods should be tested against predictions from how these properties change over environmental gradients. The structural allocation of photosynthates by plants and the spectral properties of foliar canopy chemicals can be mapped through remote sensing (Asner and Martin, 2011; Asner et al., 2011; Poorter et al., 2012; Roelofsen et al., 2013) and in the future it may become possible to relate these to geographic variation in tooth morphology and wear. However, in all these studies of mammal diet, what is traditionally important to the investigators is the nutritional component of the diet. For this purpose, the dietary material was first washed in water, often over a screen or sieve to remove obscuring or uninteresting material, and then the food items were identified. Unidentifiable material, like sand and bits of soil that were too large to pass through the initial washing, were ignored. Then, comparisons of diet between mammal species were made after classify- ing or categorizing the constituents of the diet. In all cases, the mineral particles that were either part of the plants or not, and that could have been or were ingested were not considered part of the animal diet and ignored. Such was the level of concern in zoology. The legacy of this bias has been significant.

3.1.3 Results

To explore the proposition that diet or some unique feature of South American tectonism (Andean mountain building or pyroclastic volcanism) offers plausible explanations for evolutionary trends toward higher tooth crowns, the percentage of high-crowned mammal species within each diet category is depicted in the form of box plots that compare the frequency distributions for each diet type (Figure 3.3). The box plot command in Statview(v5.0.1) from the SAS Institute Inc. compares frequency distributions by their 10th, 25th, 50th (median), 75th, and 90th percentiles. Values above the 90th and below the 10th are plotted as points. Frequency distributions of the proportion of high-crowned or hypsodont species in each fauna by diet category reveal an increasing central tendency across a dietary gradient from carnivory, through animalivory, frugivory, granivory, insectivory, folivory, and herbivory to grazing (Figure 3.3). In other words, the highest prevalence of high-crowned teeth is found among herbivorous diets. The differences in the median values between diet categories suggests these data capture the essential relationship between crown height and diet. All categories of diet involving plant foods include some mammal species that are classiﬁed as having high crowns (“hypsodont”), whereas all diet categories involving consumption at higher trophic levels, with rare exceptions, involve species with low- crowned molars. Carnivory and animalivory are dietary habits that do not introduce abrasives into the diet. The relatively higher proportions of hypsodont species among insectivores may reﬂect the often mixed nature of these diets (combining both insects and plant material) or something about the food acquisition behavior of terrestrial insectivores among the leaf litter on the soil surface. Assuming that abrasion is 3.1 Mammalian hypsodonty in South America 71

100

20 Hypsodont species (%)

N=78 N=65 N=75 N=77 N=71 N=78 N=52 N=73

CFrAGnI Fo HGz

Figure 3.3 Box plot of the percentage of high-crowned mammal species in each diet category at each site. C, carnivore; Fr, frugivore; A, animalivore; Gn, granivore; I, insectivore; Fo, folivore; H, herbivore; Gz, grazer; N, number of sites. Among grazers, all species are hypsodont at all but one site. Similarly, high levels of hypsodonty are found among mammal species classified as herbivores. The lowest levels of hypsodonty are found among carnivorans, frugivores, and animalivores. responsible for tooth wear and the evolutionary response to wear, plant reproductive structures (seeds, fruits) appear less abrasive than foliage, herbs, and grasses. The diet categories of grazing, animalivory, and carnivory show little or no dispersion and thus provide the clearest contrasts. Exploring the implications of mountain uplift, there is a noteworthy increase in the frequency of faunas with high proportions of hypsodont species among two diet classes in mountain environments (Figure 3.4). Herbivores and folivores are more often hypsodont in mountains than in lowlands. It is difficult to imagine what these contrasting central tendencies imply or how mountain environments exert their influence via foliage but not plant reproductive parts. On the other hand, more insectivorous and granivorous species are hypsodont in lowland environments than in mountains. Why this might be true is not immediately obvious. Possibly, seeds and insects become more contaminated by soil grit in lowland environments where they are often harvested directly off the soil surface or in leaf litter. Carnivores, frugivores, and animalivores show no mountain effect. Volcanic ash soils appear to exert similar influences, but a more conspicuous positive influence than mountain environments (Figure 3.5). That is, for all but two diet categories (granivory and insectivory), mammal habitats on andisols appear to exert an important positive influence on crown height proportions and serve to increase the proportion of hypsodont species. Folivorous, herbivorous, and grazing species are hypsodont almost without exception when they occur at sites on volcanic ash soils 72 South America and global hypsodonty

100

80 montane 60 lowland 40

Hypsodont species (%) 0 N=52N=47N=48 N=52 N=50 N=52 N=27 N=49

C Fr AGn I Fo H Gz

Figure 3.4 Box plot of the percentage of high-crowned mammal species in each diet category at sites partitioned by occurrence in mountain or lowland settings in tropical South America. C, carnivore; Fr, frugivore; A, animalivore; Gn, granivore; I, insectivore; Fo, folivore; H, herbivore; Gz, grazer; N, number of sites. In the tropics north of 24 degrees S latitude, mountain or Andean environments exert a positive inﬂuence on the prevalence of hypsodonty among herbivores and folivores, and a negative inﬂuence on insectivores and granivores.

100

60 andisol

40 other

20 Hypsodont species (%)

CFrAGn I Fo H Gz

Figure 3.5 Box plot of the percentage of high-crowned mammal species in each diet category at sites partitioned by occurrence on volcanic ash soils of recent origin. C¼carnivore, Fr¼frugivore, A¼animalivore, Gn-granivore, I¼insectivore, Fo¼folivore, H¼herbivore, Gz¼grazer, N¼number of sites as in Figure 3.3. Volcanic ash soils exert a strong positive effect on mammalian faunal hypsodonty across all diet classes except insectivory and granivory.

(or soils with tephra parent material), as do the proportion of animalivores and frugivores. Curiously, this is not the case for insectivorous species. There is a noteworthy increase in the proportion of high-crowned mammal species among folivores and herbivores in faunas from mountain environments and on volcanic ash soils. These relationships indicate that tectonism and volcanism may contribute to increase the proportion of high-crowned species in mammalian faunas, but the mechanism of this inﬂuence remains to be determined. 3.2 Sigmodontine hypsodonty and geography 73

3.2 Sigmodontine hypsodonty and geography

Living species of sigmodontine rodents in South America provide a unique experiment in the accommodation of mammals with low-crowned teeth to geographic variation in the environmental factors associated with high tooth crowns. While no sigmodontine is truly hypsodont (HI>1), the proportion of relatively high-crowned species in modern South American faunas has been regressed against four dimensions of continental climate, mean annual temperature (MAT), mean monthly temperature of the coldest month (CMMT, the severity of winter), the annual amplitude of mean monthly temperatures (TempAmp, the intensity of seasonal temperature variation), and mean annual precipitation (MAP) (Kay et al., 1999) (see Chapter 8, Figure 8.6). In general, the proportion of high-crowned sigmodontine species is: (1) negatively correlated with mean annual temperature (as MAT decreases, the proportion of species with high crowns increases), (2) negatively correlated with mean annual precipitation, (3) negatively correlated with the mean temperature of the coldest month, and (4) positively correlated with the amplitude of monthly mean temperatures (temperature seasonality). An analysis of variance (Table 3.4) shows that the variation in sigmodontine hypsodonty explained by the four-climate-variable model is significant, although the leverage of each variable within the model is not (p<0.05). This result is not surprising given that the four climate variables are strongly and significantly correlated with each other (Table 3.5). While general trends in sigmodontine hypsodonty are apparent in all four dimensions of climate, the relationships are weak. Nevertheless, there seem to be threshold values for faunas without any high-crowned species and other thresholds where 50% or more of species are high-crowned (Table 3.6). In semiarid climates (MAP<750 mm), some species of sigmodontine rodents are always high-crowned, whereas in wet climates (MAP>2000 mm) high-crowned sigmodontines are rare. There are only two sites that have recorded MAP as much as 3000 mm (but normally between 1400 and 2500 mm) where high-crowned sigmodontines occur in any proportion, the Nothofagus forests of Los Alerces and Ñahuel-Huapi in Argentine Andean Patagonia. Where MAT is <23 C and where MAT is <15 C, the proportion of high-crowned sigmodontines increases, and the proportion increases notably wherever MAT is <15 C. There is only one site with MAT>22 C where high-crowned species comprise 50% of the sigmodontines, the semiarid Prosopis “vinal” shrub parkland of Formosa Province, northern Argentina. Why such thresholds of temperature and precipitation exist is not easy to answer, although the general relationship between precipitation and tooth crown height is now well established (Eronen et al., 2010a, b). Canonical community ordination (CCA) can be used to explore more complex sets of environmental variables to the tooth crown shape composition of mammalian faunas. CCA permits percentage data (for example, the percentage of hypsodont species in each diet class), a mix of nominal and continuous environmental variables, and partial ordination removes the effects of covariables biasing the fidelity of the data (area, geographic difference between nearest meteorological station and inventory site, and 74 South America and global hypsodonty

Table 3.4 ANOVA table and Effects Test for the inﬂuence of four climate variables on sigmodontine hypsodonty

Source DF SS MS F ratio P-value

Model 4 1.4177104 0.354428 19.2764 <0.0001 Error 63 1.1583568 0.018387 C total 67 2.5760672 Source Nparm DF SS F ratio P-value

MAT 1 1 0.00586803 0.3191 0.5741 CMMT 1 1 0.00039441 0.0215 0.8840 TempAmp 1 1 0.00051425 0.0280 0.8677 MAP 1 1 0.06468684 3.5181 0.0653

Table 3.5 Correlation matrix with Fisher’s r to z for mean annual precipitation (MAP), mean annual temperature (MAT), the amplitude of mean monthly temperature (TempAmp), and coldest month mean monthly temperature (CMMT)

MAT CMMT TempAmp MAP

MAT <0.0001 <0.0001 <0.0001 CMMT 0.968 <0.0001 <0.0001 TempAmp 0.555 0.740 <0.0001 MAP 0.589 0.652 0.594

Table 3.6 Threshold values for sigmodontine faunal hypsodonty in relation to mean annual precipitation (MAP), mean annual temperature (MAT), the amplitude of mean monthly temperature (TempAmp), and coldest month mean monthly temperature (CMMT)

Climate Variable Threshold Sigmodontine Hypsodonty

MAP <750 mm >25% of species are high-crowned MAP >2000 mm All species low-crowned MAP <1500 mm >50% of species are high-crowned MAT <15 C Always some species are high-crowned MAT <17 C >50% of species are high-crowned TempAmp >13 C Always some species are high-crowned TempAmp >9 C >50% of species may be high-crowned CMMT <15 C >50% of species may be high-crowned CMMT <5 C Always some species are high-crowned

sampling intensity). Using partial direct gradient CCA, the structure of variation in faunal hypsodonty can be depicted by ordination diagrams (species/environment biplots) where the axes are correlated with environmental variables. The ﬁrst two axes summarize the original suite of environmental variables by revealing those with the greatest inﬂuence or explanatory power (Ter Braak, 1995, 1996; Ter Braak and Smi- lauer, 1998; Leps and Smilauer, 2003). 3.2 Sigmodontine hypsodonty and geography 75

0.6 Closed

Relief

Surplus

JanRRate

Altitude MAP 5 D Trees Andisols D 4 1D RadAmp Hot and humid Lat Cool and dry Axis 2 D D 3 AMPMMP 2 TempAmp Wind

MINMMT Mosaic Open DryDays Deficit MAT GrowDD AnnRAD

Disperse AnnPET

–0.6 –1.0 1.0 Axis 1

Figure 3.6 Multivariate partial direct-gradient canonical community ordination (CCA) biplot of South American mammal and sigmodontine rodent species tooth crown height classes and 23 environmental variables. Triangles represent centroids of the number and proportion of low- or high-crowned species in 80 mammal faunas; (1) number of low-crowned mammal species, (2) number of high-crowned mammal species, (3) proportion of high-crowned mammal species, (4) proportion of sigmodontine species that are high-crowned, (5) number of sigmodontine species that are high-crowned. The correlation of faunal crown height classes and the environmental variables is depicted by the general polarity of Axis #1, the ﬁrst or horizontal axis. Left side of Axis #1, low-crowned teeth correlated with moisture variables and temperature conditions favorable to year-round plant growth. Right side of Axis #1, high tooth crowns correlated with temperature seasonality, aridity variables, wind intensity, open habitats, and volcanic ash soils.

The results are best visualized in a CCA biplot (Figure 3.6). CCA selects the linear combination of environmental variables that maximizes the dispersion of species scores. Here, species scores are measures of faunal hypsodonty, both for all South American mammals, and separately for Sigmodontinae. In general, species that fall closer to the center of the diagram are less well represented by the ordination and inferences about their correlations are less warranted. The arrangement of “species” in the biplot indicates that tooth crown height in Sigmodontinae is more sensitive to environmental variables than crown height in all South American mammals. Sigmo- dontine hypsodonty has higher values along the ﬁrst axis than mammalian faunal hypsodonty, consistent with their more recent evolutionary accommodation to South American environments. In Figure 3.6, each arrow determines an axis for an environmental variable and species points can be projected onto that axis in an order corresponding to the rank of the weighted average of each species with respect to the environmental variable. The arrows point in the direction of maximum change and their length is proportional to the “rate of change” in that direction. Environmental variables with long arrows aligned 76 South America and global hypsodonty

Table 3.7 Matrix of weighted species–environment and intraset correlations of environmental variables on the prevalence of mammal and sigmodontine species with high-crowned teeth

Axes 1 2 3 4

Eigenvalues 0.110 0.008 0.003 0.001 Species–environment correlations 0.9101 0.6668 0.5779 0.4269 Cumulative % variance of 90.6 97.3 99.5 100.0 species–environment relation OPEN 0.6663 0.1306 0.0503 0.1211 CLOSED 0.4464 0.5199 0.3236 0.2045 DISPERSE 0.0157 0.4718 0.2531 0.1636 MOSAIC 0.0132 0.1313 0.2797 0.4326 ANDISOL 0.8336 0.1948 0.3441 0.1639 ALTITUD 0.3165 0.2471 0.0902 0.1991 MAT 0.8742 0.3742 0.0798 0.1573 TEMPAMP 0.3546 0.0653 0.3454 0.2187 MAP 0.7515 0.1586 0.2561 0.1567 AMPMMP 0.5471 0.1087 0.2182 0.2522 DRYDAYS 0.4582 0.1864 0.1070 0.1599 ANNPET 0.3784 0.5550 0.1300 0.1784 ANNRAD 0.2582 0.3522 0.2398 0.2106 WIND 0.5001 0.0372 0.0134 0.1916 DTEMPAMP 0.1328 0.2491 0.0781 0.2467 GROWDD 0.5861 0.3280 0.2228 0.0585 JANRRATE 0.5558 0.2520 0.1003 0.3568 SURPLUS 0.4046 0.3577 0.3084 0.2592 RELIEF 0.1383 0.5383 0.0992 0.0509 SDPHOTO 0.5358 0.0987 0.3498 0.1059

more closely to the ordination or canonical axes are more strongly correlated with that axis, and therefore more closely related to the pattern of variation in faunal and sigmodontine hypsodonty. Arrows pointing in roughly the same direction indicate a high positive correlation, whereas arrows pointing in opposite directions indicate high negative correlation; arrows crossing at right angles indicate near zero correlation. The position of the arrowheads depends on the eigenvalues and intraset correlations (Tables 3.7 and 3.8). Longer arrows are more strongly correlated with the ordination axes and are more strongly correlated with faunal and sigmodontine hypsodonty. A ranking of interset correlations of environmental variables with the ﬁrst two ordination axes (Table 3.8) reveals that the ﬁrst canonical axis is polarized by moisture. Environmental variables with positive correlations denoting drier, open, windy habitats or andisols cluster at the positive (right) extreme pole and environmental variables denoting warmer, wetter, and closed habitats with negative correlations cluster at the opposite or negative (left) pole. The second or vertical canonical axis is not characterized by any obvious or simple environmental polarity, but captures a complex environmental web around the remaining variation, with relief appearing at one extreme and the opposite extreme is annual potential evapotranspiration. 3.2 Sigmodontine hypsodonty and geography 77

Table 3.8 Ranked interset correlations ( 1000) of the environmental variables with the ﬁrst two ordination axes

Ranked axis 1 Ranked axis 2 Variable (fraction extracted Interset Variable (fraction extracted Interset (N) ¼ 0.202) correlation (N) ¼ 0.042) correlation

6 ANDISOL 759 24 RELIEF 359 1 OPEN 606 2 CLOSED 347 25 SDPHOTO 488 23 SURPLUS 239 19 WIND 455 22 JANRRATE 168 14 DRYDAYS 417 8 ALTITUD 165 26 DEFICIT 329 6 ANDISOL 130 11 TEMPAMP 323 12 MAP 106 8 ALTITUD 288 25 SDPHOTO 66 24 RELIEF 126 19 WIND 25 20 DTEMPAMP 121 11 TEMPAMP 44 3 DISPERSE 14 13 AMPMMP 72 4 MOSAIC 12 1 OPEN 87 17 ANNRAD 235 4 MOSAIC 88 15 ANNPET 344 14 DRYDAYS 124 23 SURPLUS 368 26 DEFICIT 155 2 CLOSED 406 20 DTEMPAMP 166 13 AMPMMP 498 21 GROWDD 219 22 JANRRATE 506 17 ANNRAD 235 21 GROWDD 533 9 MAT 250 12 MAP 684 3 DISPERSE 315 9 MAT 796 15 ANNPET 370

A forward selection among these variables (Figure 3.7) suggests a relationship between the prevalence of high tooth crowns in Sigmodontinae and decreasing MAT and MAP, and more seasonal and open environments, but especially andisols. These variables are inter-related, that is, as MAT decreases with latitude and altitude, South American environments come under the inﬂuence of the Andes. MAT decreases with altitude at all latitudes, and as MAT decreases with latitude, the continent narrows and the “imprint” or “shadow” of the Andes is felt with greater intensity as the erosion products of the Andes extend eastward away from the orogen axis, and come to cover (and inﬂuence) a greater part of the adjacent lowlands. Additionally, the Andes originate in subduction, and andesitic volcanism is a feature of much of its meridional extent. Altitude and latitude gradients in South America are intimately related to rainfall (and through rainfall and temperature together, to plant growth and vegetation structure) and the zonal patterns of circulation that distribute atmospheric moisture through prevailing wind regimes. Just exactly how does the relationship between faunal hypsodonty, MAT, MAP, and andisols work? Using the Fit Model command in JMP v3.1 and JMP v5.0.1.2, standard least squares multiple regression of the percentage of high-crowned Sigmodontine species using the four environmental variables (CMMT, MAT, Amplitude MMT, and MAP) as model effects, yields a whole model R2 value of 0.64 (p<0.0001). 78 South America and global hypsodonty

0.4

MAP

5D 4D Andisols 1D Axis 2 D Hot and humid 3 Open and volcanic 2D TempAmp MINMMT

MAT Open

–0.4 –1.0 1.0 Axis 1

Figure 3.7 Forward selection among the environmental variables by CANOCO reveals a more explicit relationship between hypsodonty in South American mammals and Sigmodontinae (1, 2, 3, 4, 5, as in Figure 3.6) and open habitat (OPEN), seasonality (TempAmp), and volcanic ash soils (Andisols). High mean annual rainfall (MAP), high mean annual temperature (MAT), and warm minimum monthly temperature (MINMMT) are negatively correlated with hypsodonty.

A contour map of residual hypsodonty was created using the contour plot command with x ¼ LongDD and LatDD and y ¼ residual (Figure 3.8). Latitude and longitude coordinates for the coastline of South America were assigned the highest negative residual (-0.22282 ¼ Perito Moreno). The contour plot command depicts residual hypsodonty (after removing the effects of the four climate variables MAT, MAP, CMMT, and TempAmp) and reveals geographic areas of high positive residual hypsodonty. The areas of high residual hypsodonty align along the western side of the continent. There are several distinct or disjunct areas of high residual hypsodonty, the largest of which centers at about 30 S latitude where the highest values are observed. The latitudinal distribution of the two most important sources or generators of environmental mineral particles in the Andes (glacial erosion and volcanic eruptions) and the dominant erosion process mobilizing these particles were examined for geographic coincidence. These variables include the latitudinal distribution of: (1) 7239 Andean glaciers (World Glacier Monitoring Service, Laboratory of Hydraulics, Hydrology and Glaciology, Section of Glaciology, ETH-Zurich), (2) 186 active volcanoes (Smithsonian Global Volcanism Program database [http://www.volcano.si.edu/ world/allnames.htm]), and (3) the annual frequency of dust storms reported from 127 meteorological stations in Argentina (courtesy of the Servicio Meterológico Nacio- nal, Buenos Aires). Glaciers have a discontinuous latitudinal distribution in the Andes, and are clustered where segments of the Andean batholith complex emerge like crystalline jewels at the crest of the orogen. Likewise, active volcanoes have a discontinuous latitudinal distribution described by three distinct zones, the Northern Volcanic Zone-NVZ in southern 3.2 Sigmodontine hypsodonty and geography 79

Dust sources and hypsodonty 10 in sigmodontinae

-10

-20

-30 Residual % sigmodontinae –0.20000 hypsodont –0.15000 –0.10000

-40 –0.05000 –0.00000 0.05000 0.10000 0.15000 -50 0.20000 0.25000

600 0 12 8 4 0 16 12 8 4 0 -80 -70 -60 -50 -40 Number of Number of Annual frequency glaciers volcanoes duststorms

Figure 3.8 Disjunct areas of high residual hypsodonty among Sigmodontinae, the latitudinal distribution of the principal sources of mineral particles in Andean environments (active volcanoes and glaciers) and the intensity of surface process that mobilize ﬁne-grained volcanic ash (and glacial loess) expressed as annual dust storm frequency. The latitudinal distribution of (1) 7239 glaciers from the World Glacier Monitoring Service, Laboratory of Hydraulics, Hydrology and Glaciology, Section of Glaciology, ETH-Zurich; (2) 186 active volcanoes: Smithsonian Global Volcanism Program [http://www.volcano.si.edu]; and (3) 127 stations reporting annual dust storm frequency, courtesy of the Servicio Meterológico Nacional Argentino, Buenos Aires.

Colombia and Ecuador (between 7 N and 0.5 S latitude); Central Volcanic Zone-CVZ in southern Peru, western Bolivia, northern Chile, and NW Argentina (between 14 and 29 S); and a Southern Volcanic Zone-SVZ (between 33 and 46 S) in southern Chile and Argentina with subsidiary northern NSVZ (33–35 S) and southern SSVZ (41–46 S) subzones. The discontinuities in the geographic distribution of high residual hypsodonty appear to correspond more with the earth surface process that transports and disperses these mineral abrasives (dust storm frequency) than with discontinuities in the latitudinal distribution of the two sources of mineral particle abrasives (active volcanoes and glaciers). Thus, there is circumstantial evidence from geographic coincidence that implicates at least one mechanism of soil mineral transport, the dust storms that mobilize the products of glacial erosion and ash-rich volcanism. The results show that hypsodonty is a complex phenomenon involving correlations with herbivorous diets, large-scale climate variation in temperature and rainfall, and both the sources of 80 South America and global hypsodonty

Volcanic rivers

Rivers in tectonically active regions

World rivers

0.001 0.01 0.1 1 10 100 1000 - Erosion rate (mm yr 1)

Figure 3.9 Central tendency and range of ﬂuvial erosion rates (surface denudation rates) in catchments in tectonically active areas and areas of active volcanism. Note erosion rates are plotted on a logarithmic scale. (From Koppes and Montgomery, 2009; with permission from Macmillan Publishers Ltd.)

sediment and the surface processes that mobilize environmental abrasives through the animal’s environment. Tectonically active mountain topography or high relief and active volcanism enhance erosion intensity and the amount or ﬂux of mineral particles (Montgomery et al., 2001; Montgomery and Brandon, 2002; Koppes and Montgomery, 2009)(Figure 3.9).

3.3 Hypsodonty in mammals around the world

Whether this pattern of distribution of areas of high residual hypsodonty in South America is unique requires an exploration of global patterns of molar crown height in herbivorous mammals. For this, a much larger dataset has been compiled from species inventories and environmental variables at 256 sites or localities around the world (Damuth, et al., 1998). In this data, living mammal species are classiﬁed by tooth morphology (hypsodont versus not hypsodont) and values of faunal hypsodonty (the percentage of herbivorous species that are hypsodont) for each of the 256 localities have been plotted on latitude (using JMP v5.0.1, SAS Institute). Smoothing spline functions (lambda¼10 and 100) were ﬁtted to the latitudinal distribution of faunal hypsodonty for each continent (Figure 3.10). In this analysis, the prevalence or proportion of species with high tooth crowns (“faunal hypsodonty”) means different things for each continent. For South American localities, it is the proportion of primary consumers that are high-crowned, and this includes rodents, xenarthrans, and ungulates. In South America, of 474 mammal species that are primary consumers, 191 have either high-crowned or ever-growing cheek teeth. For Australia, primary consumers included in this measure of faunal hypsodonty include domestic ungulates, Vombatidae, and Macropodidae. For all other continental faunas in the NCEAS dataset (including Africa, North America, and Eurasia), faunal 3.3 Hypsodonty in mammals around the world 81

70 60 50 40 30 20 10 0 -10 -20

Latitude (degrees) -30 -40 -50 -60 -150 -100 -50 0 50 100 150 Longitude (degrees)

0.8 Africa

Australia 0.6

0.4 Eurasia

South America 0.2

Percent faunal hypsodonty faunal Percent North America 0

-60° -40° -20° 0° 20° 40° 60° Latitude

Figure 3.10 Smoothing splines ﬁtted to latitudinal variation in the proportion of high-crowned species among herbivorous mammals in 256 modern mammal faunas. Peak faunal hypsodonty in northern continent mammals are coincident at around 30 degrees N latitude. An evident mirror of this coincidence is found in the southern hemisphere at 30 degrees S latitude. (Data courtesy of Damuth et al., 1998.)

hypsodonty is the proportion of ungulate species that are hypsodont. Only in this sense is this measure of faunal hypsodonty equivalent across all continents. [At this point, many readers will throw up their arms, throw the book across the room, and return to more useful work until we get comparable measures of the total volume of tooth mineral substance secreted and mineralized throughout the dentition, during the life of each and every mammal species on the planet, in a measurement unit of mineral density for the summed volume of dentin, orthodentin, enamel (of different microstructures), and cementum.] The smoothing splines reveal interesting things about the latitudinal distribution of hypsodonty. Most signiﬁcant are the coincident peaks of the prevalence of hypsodonty in northern hemisphere continents (North America, Eurasia, and Africa) at about 30 N. While there are small but coincident peaks in faunal hypsodonty at about 30 S latitude (Australia and South America and the southern part of Africa), the shape of the curves in the southern hemisphere is more complex. Coincident peaks of faunal hypsodonty at 82 South America and global hypsodonty

Latitude 60°

Eurasia

40°

20° North America 0.2 0.4 0.6 0 Africa 0.2 0.4 0.6 0.8 % Hypsodont 0 % Hypsodont Australia -20° 0.2 0.4 0.6 0.8 0 1 -40° Aridity Index % Hypsodont 0.2 0.4 0.6 0.8 0.0-19.9 South % Hypsodont 20.0-39.9 America 0.2 0.4 0.6 40.0-59.9 0 -60° 60.0-79.9 % Hypsodont 80.0-100 no data

Figure 3.11 Peak latitudes of faunal hypsodonty on a map of De Martonne aridity zones (De Martonne, 1941 and FAO, 2006a; with permission from the Food and Agriculture Organization of the United Nations). The aridity index of De Martonne is the ratio of annual precipitation (mm) and mean annual temperature (Cþ10). The higher the index, the higher the precipitation compared to evaporation. A high aridity index means a humid climate while a low aridity index means an arid climate. (http://www.fao.org/nr/climpag/globgrids/kc_commondata_en.asp)

around 30 degrees latitude in both hemispheres implicates general features of Hadley- cell circulation and zonal climates at this latitude. The polymodality of faunal hypsodonty in the southern hemisphere appears to relate in some way to the interaction between atmospheric conditions and land surface conﬁguration (for example, Australia has its largest land area situated at about 30 S latitude), the orientation and continuity of orographic belts and their inﬂuence on atmospheric transport (for example, the Great Dividing Range of Eastern Australia, the Andes, the East African rift system), and as already demonstrated, to latitudinal discontinuities in the dominant sources of mineral particles (glacial erosion and active volcanoes) and the surface processes that mobilize and transport mineral particles (e.g., dust storms). When the distribution of faunal hypsodonty on latitude is compared with the global distribution of aridlands (Figure 3.11) (World Resources Institute, 2002), grasslands (Figure 3.12) (Murai and Honda, 1990; Del Grosso et al., 2008), and dust storm frequency (Figure 3.13) (ISMCS, 2002; Tegen et al., 2004), latitudinal coincidence suggests a stronger association with measures of high aridity and high dust storm frequency, and these associations appear stronger than any relationship with the geographic distribution of grasslands. In particular, peaks in the latitudinal distribution of faunal hypsodonty for Eurasia, Africa, and North America agree closely with the distribution of high aridity (Figure 3.11), do not appear to coincide with the distribution of grasslands (Figure 3.12), and are coincident with areas of high dust-storm frequency (Figure 3.13). 3.3 Hypsodonty in mammals around the world 83

Latitude

60°

Eurasia

40°

20° North America 0.2 0.4 0.6 0 Africa

% Hypsodont 0.2 0.4 0.6 0.8 0

% Hypsodont Australia

-20° 0.2 0.4 0.6 0.8 0 1 -40°

% Hypsodont 0.2 0.4 0.6 0.8 South America % Hypsodont 0.2 0.4 0.6 -60° 0 % Hypsodont Grasslands & savannas Desert Wetlands & ice Boreal, temperate & tropical forest Tundra

Figure 3.12 Peak latitudes of faunal hypsodonty and the global distribution of grasslands. (From Del Grosso et al., 2008, ©Ecological Society of America, with permission.)

Figure 3.13 Peak latitudes of faunal hypsodonty on station-based global dust storm frequencies (Engelstaedter et al., 2003, ©2003 American Geophysical Union, with permission from John Wiley and Sons). Dust storm frequencies (days/year) were estimated using daily measurements from 2225 meteorological stations from the International Station Meteorological Climate Summary (ISMCS) dataset. By deﬁnition, a dust storm occurs when visibility is less than 1 km because of mineral particle dust (Kohfeld and Harrison, 2001; Tegen et al., 2004). 84 South America and global hypsodonty

Either mammalian herbivores are evolving high tooth crowns elsewhere (in grasslands, for example) and later distributing into aridlands characterized by high dust storm frequency under mid-latitudes or environmental conditions at middle latitudes are contributing to the evolution of tooth crown height. 4 Excess tooth wear in New Zealand

4.1 History of study

4.1.1 Early interest in excess tooth wear

The quality of mouths of sheep in New Zealand, particularly in certain parts of the North Island, has progressively deteriorated in the last 30 or 40 years. (Barnicoat, 1957, p. 583.) The main factor responsible for poor mouths is abrasion (excessive wear) due to external causes. (Barnicoat, 1947, p. 100.) Guthrie-Smith (1921) was the first to explore three issues of long-standing interest to pastoralists: “herbage of high-yielding type,” the process of forest conversion, and the erosion of pasture soils. Once natural forest was felled, sheep had to “create his own pasture” and “grow his own keep” (Guthrie-Smith, 1921). Paraphrasing his words to describe this process, he observed native grasses colonizing pig-rootings, deserted native clearings, and landslip scars. These patches of self-sewn native grass were isolated from each other, linked only by narrow tracks through tall bracken fern. For the task of increasing the acreage of grassland, “fern-crushing” was undertaken. The earliest colonists overstocked to defeat the bracken. Every animal was kept, however old, as “a pair of jaws, a beast that could bite bracken” leading to the practice of “murdering the sheep to make the country.” The sheep became “fern-scythes and mowing-machines.” Guthrie-Smith (1921) also observed the soil erosion that accompanied this process of forest conversion to pasture. But the significance of soil erosion was only recognized when Cumberland (1947) implicated “axe and fire” rather than “a pair of jaws” as the principal agent promoting deforestation and initiating soil erosion. Soil erosion went unheeded officially until 1938, the year of the Hawke’s Bay floods. Two significant rainstorm events followed in 1943 and 1944, the “Anzac” rains. Cumberland’s work drew attention to the extent of soil erosion as a consequence of European colonization and land-use practices. Cumberland also noted that New Zealand wool production, unlike everywhere else, did not increase during World War II to meet increasing needs associated with this emergency. Barnicoat’s inquiry was intended to answer this mystery.

85 86 Excess tooth wear in New Zealand

Barnicoat’s 1947 preliminary or interim report is the oldest scientific publication on the subject in New Zealand, and includes an interesting question-and-answer session that followed its presentation at the 10th Annual Meeting of Sheep Farmers at Massey Agricultural College. The problem was characterized as “sheep’s teeth do not last well and...this deterioration has become more pronounced during the last 20 or 30 years” during which time “radical changes in sheep farming practices have taken place” (p. 98). During the questions and answers, numerous seat-of-the-pants explanations were suggested by sheep farmers. Some data were presented on varying incisor crown length at four farms within an eight-mile radius of Massey College in Palmerston North, part of a more ambitious research program involving the annual recording of mouth condition in 700 tagged ewes on 13 different properties in the Taihape area (Rangitikei), and over 300 others in the Manawatu district. Barnicoat reviewed evidence for seven factors implicated in the problem of excess tooth wear: (1) abrasion or excessive wear due to external causes; (2) the lack of evidence for structural differences between good and bad teeth; (3) whether the toughness of pasture predominates over other factors such as soil type; (4) why high- fertility ryegrass and clover pastures seem to cause more wear than pastures of fine native and brown-top grasses; (5) why teeth on high-rainfall pastures are unworn, but under seasonal and interannual cycles of dry climate, teeth wear down even on native pastures, especially during long droughts, (6) overstocking causes excess wear, especially in winter, when soil is deposited as a film on grass by treading and rain-splashing; and (7) mineral deficiencies. During the questions and answers, Barnicoat acknowledged that “on land which floods in this district the teeth wear badly, and this is ascribed by the owners to the presence of a deposit of fine silt on the leaves of the herbage.” The term “flood” in New Zealand describes both conventional effects of high-rainfall and the widespread land-slipping that frequently accompanies it. During the course of his studies, Barnicoat surveyed many parts of the North Island and concluded that overgrazing was a factor promoting rapid wear. In his later publications, Barnicoat often repeated that the problem was most pronounced on low country improved pastures. When he studied the problem in more detail, he found less wear under rotational grazing than with set stocking (Barnicoat, 1957). Thus, a management solution was identified early in the course of study, and for practical purposes, the problem of excess tooth wear was solved. What remained, though, was an explanation for occurrences of accelerated tooth wear and areas of endemic excess wear. To find an explanation, an experimental farm at Te Awa was established through the Manawatu Catchment Board Soil Conservation and Rivers Control Council in 1945, nominally to study methods for improving productivity of hill-country stations and controlling severe erosion (Suckling, 1950, 1954, 1959). Suckling reported that thun- derstorms contributed to erosion in the district. Among the control methods tested was gully realignment using bulldozers to restore the broad grassy runways that existed before the gullies washed out. After the gully floor was flattened with a bulldozer, it was grassed over. In spite of heavy seeding, topdressing, and favorable weather conditions, 4.1 History of study 87

pasture establishment was poor and growth slow. However, over the years grassland improvement proved to be among the most successful aspects of the experimental work at Te Awa, motivated as a solution to a soil erosion problem and not to address the specific problem of excess tooth wear, although these were eventually found to be inseparable. Concern about the prevalence of excess tooth wear increased markedly when sheep farmers began to age mark their birth cohorts. Barnicoat (1957) stated that “since the introduction of age-marking, farmers have become aware of the variations and ranges in quality of sheep’s mouths, even within their own flocks.” Previously the age of ewes was judged only by dental eruption. Now, farmers became aware of the fact that ewes were being sent to slaughter at five years of age because their incisors were worn to the gumline and their condition was beginning to decline, and the implications of premature mortality (Figure 4.1) and the truncation of reproductive lifespan (Figure 4.2)on production became evident.

100

80 ) x 60

40 Mortality rate (q Premature culling

0 042610 812 Age (years)

Figure 4.1 Biological consequences of the premature culling of ewes due to premature dental senescence in endemic areas of excess tooth wear expressed in terms of mortality. Age speciﬁc female mortality rate (qx) is based on the age distribution of 83 113 ewes assessed between 1954 and 1959 (Hickey, 1960). 88 Excess tooth wear in New Zealand

0.7

0.6 Truncated reproductive lifespan

0.5 ) x

0.4

0.3

Fecundity rate (m 0.2

0.1

0 0 24681012 Age (years)

Figure 4.2 Biological consequences of the premature culling of ewes due to premature dental senescence in endemic areas of excess tooth wear expressed in terms of fecundity. The age speciﬁc fecundity rate (mx) is female offspring per female of age years for sheep from the North Island of New Zealand (Hickey, 1960).

Barnicoat’s(1957) long-term study, reported to the New Zealand Stock Station Agents Association in 1957, showed excess tooth wear to be a serious problem on many North and South Island farms. The report included a map showing the extent of the areas where excess tooth wear was a special problem. Barnicoat compared this distributiontoasmanymappedfeaturesofthe physical and botanical environments as he could find. Evidence is presented that shows the problem occurs on farms in certain areas of improved grassland, and is most serious on heavily stocked, lush, low-country farms carrying high-fertility European perennial pasture grasses, and least evident on lightly stocked hills with “finer” and more diverse native grasses. Barnicoat (1957) came to suspect that abrasion was aggravated by enamel corrosion caused by substances in the rapidly growing leaves of high-yielding grasses and clovers. The average length of the central incisors in five-year old ewes in four settings on the North Island demonstrated that tooth wear in improved low-country pastures was more accelerated than in high-country pastures. Part of the explanation was thought to relate to the fact that sheep on lush low-country pastures ingest two to three times as much dry matter (DM) daily as those on sparse hill country, and thus, they take in different amounts of calcium and phosphorus. However, the chemical composition of enamel and dentin from sheep in high-wear and low-wear situations did not differ 4.1 History of study 89

and differences in the chemical composition of soils are not correlated with the extent of tooth wear (Barnicoat, 1959). Only fluorinewasfoundtodiffer,and the variation in fluorine was attributed to fertilizer, that is, to the influence of topdressing. Substances in the herbage of improved pastures were thought to dissolve the teeth, a process aided by the abrasive action of plant fiber. However, electron micrographs of the biting edge of worn incisors showed that the dentin surface was subjected to both chemical and abrasive action. Freshly expressed juices of grasses and clovers contain enzymes, cell fluids (sugar, inorganic and organic phosphates, amino acids, polypep- tides), and organic acid from herbage. Of all these, freshly expressed juices etch dentin the most strongly, and this reaches a maximum during spring growth. Suspicion was that etching by proteinases in actively metabolizing leaves weakens the bonding material of the organic components of dentin, thereby facilitating wear by attrition (Barnicoat, 1963). Between 1947–48 and 1960–69 there was a huge increase in pasture production from 3261 kg/ha DM to 13 178 kg/ha DM. This increase was paralleled by the change in botanical composition involving an increase in ryegrass, the relative diminution of other grasses, an increase in stocking rates from 2.4 to 12 ewes/ha, and the widespread adoption of aerial top-dressing with superphosphate fertilizer (Suckling, 1975). Suckling (1964) reported measurements in the field of stocking rate and tooth wear and confirmed the early findings of Barnicoat that indicated high rates of tooth wear were associated with high stocking rates. Suckling reported that between 1948 and 1959, as stocking rate increased, there was an increase in tooth wear and in the culling rate of five-year-old ewes. Suckling (1975) reported the results of a long-term trial at Te Awa where tooth wear was monitored under four different stocking rates without supplementary feeding. Suckling (1975) examined two possible explanations for the observed variation in mean incisor crown height between paddocks: stocking rate (herbivore density) and differences in the number of herbivore species occupying the paddocks (sheep with or without cattle). Between 1963 and 1969, tooth length was measured in February of each year on live sheep, thereby permitting a calculation of the rate of central incisor linear tooth wear (disregarding the effects of changing crown shape with wear). Tooth wear rates were variable from year to year and were high in 1963, 1966, and 1968, and low in 1964 and 1967. In the first years between 1963 and 1965, measurements compared with initial or baseline incisor crown length agreed with both suppositions, that is, crown length decreased with increasing stocking rates and in the presence of cattle. Suckling (1975) noted that this association was partly a consequence of soil intake by sheep grazing very short pasture. In addition, high-stocked pastures were observed to be dustier and had a larger number of worm casts in winter. During a collaborative study of soil nematode parasitism in 1962–1964 (Tetley and Langford, 1965), large amounts of soil were found in sheep stomachs, as much as 1.6 kg in sheep from pastures with the highest stocking rates. 90 Excess tooth wear in New Zealand

4.1.2 Soil ingestion

A postal survey by Wellington (New Zealand Department of Agriculture, unpublished report) of 229 farms in the Wairarapa found that a substantial number of farms (15%) were concerned about tooth wear and were affected by wear (the number of five-year- olds sent to premature slaughter). Furthermore, considerable differences in wear were found to occur on farms separated by relatively short distances. The results of this survey inspired the work of Healy and Ludwig. Healy worked for the Soil Bureau of the Department of Scientific and Industrial Research office in Lower Hutt, and Ludwig worked for the Dental Research Unit of the Medical Research Council in the city of Wellington. Through their work, soil ingestion was discovered to be the culprit (Healy and Ludwig, 1965a, b, 1966;Ludwigetal.,1966; Healy, 1967). The relationship between tooth wear and soil ingestion was first established in the Te Awa hill country of the North Island. In the nearby Wairarapa, the amount of incisor wear at the occlusal surface was found to be directly related to the amount of soil ingested by the grazing animal (Healy and Ludwig, 1965; Ludwig et al., 1966). Fully 70% of annual incisor wear occurred between July and October (during the austral winter) when the soil content of feces exceeded 40% (Ludwig et al., 1966), and more rapid incisor wear was detected between the months of July and September in another later study (Thurley, 1984, 1985a, b). This “normal” seasonal variation in tooth wear suggests either biological or direct environmental influence, or some combination of the two.

4.1.3 A syndrome of dental pathologies

Up to this time, excess tooth wear was a simple pathology, not a syndrome of multiple pathologies. Only somewhat later was a complex of dental and oral pathologies (that included excess tooth wear) described and termed the Wairarapa Syndrome by Bruere et al. (1979; Orr et al., 1979). The complex clinical picture of this syndrome was not typical of wear caused by simple abrasion, and for Bruere and others, the abrasion theory failed to explain the variety of different features seen in flocks with severe tooth deterioration. Instead, Mitchum and Bruere (1984) proposed that there were different mechanisms producing the excess loss of tooth mineral substance, namely nutritional problems leading to enamel defects and solubilization. The intensification of sheep farming involved (1) replacement of native vegetation by highly productive European grasses and legumes, (2) application of fertilizer (lime, superphosphate), and (3) increasing stocking rates through rotational grazing in paddocks. The soil inputs (urine, feces, fertilizers) associated with intensification included increases in earthworm biomass and an absolute increase in soil microbe mass. Another consequence was an increased uptake of soluble soil minerals by plants. The organic acids produced by soil microorganisms not only dissolved the apatite in phosphate rock fertilizer, but also the biogenic apatite in tooth enamel, dentin, and bone. Thus, incisors were shedding enamel volume not only by abrasion but also by dissolution. Thus, while 4.1 History of study 91

grazing sheep ingest as much as 300–400 g of soil each day during winter and spring (amounting to as much as 25 kg seasonally), the teeth were also bathed in apatite- dissolving substances. Mitchum (1985) reviewed the voluminous literature on tooth wear and periodontal pathologies leading to progressive deterioration and loss of tooth volume. Barnicoat (1957) was the first to draw a distinction between abrasion due to mechanical causes and progressive deterioration of mouths on improved country. Bruere and his student Mitchum revived the distinction and the many associated pathologies that no one causal agent explained successfully. By reviving this distinction, they amplified the role of soil ingestion, and claimed that progressive deterioration, not simple excess tooth wear, was the major problem in the southern part of the North Island. Thurley (1983, 1984, 1985a, b) described the syndrome of dental abnormalities in sheep as involving six distinct pathologies: (1) excessive wear of deciduous incisors, (2) maleruption of permanent incisors associated with osteopathy of the mandible, (3) frequent dentigerous cysts, (4) periodontitis of the incisors, (5) excessive wear of the permanent incisors, and 6) premature tooth loss. Other observed pathologies included an increase in the length of the exposed incisor root, excessive deposition of cementum over unerupted labial enamel, and a regression of Hertwig’s sheath. The clinical picture of the Wairarapa syndrome is complex and includes enamel surface dissolution, inter- proximal wear, weak calcification of the anterior mandible, pitting of the labial enamel (hypoplasia), rapid tooth eruption, dentigerous cysts, and maleruption, in addition to apical abrasive wear (Bruere et al., 1979; Orr et al., 1979; Thurley, 1985a, b; West, 2002). The diverse pathologies associated with the Syndrome inspired the examination of many possible additional causes of tooth wear and enamel degradation, including heritable susceptibility to tooth wear (Meyer et al., 1983), dietary mineral imbalances (Bruere et al., 1979), soil acidity (Mitchum and Bruere, 1984), chemical composition of pasture juices (Cutress and Healy, 1965), and bacterial infection (Spence and Aitchison, 1985). Causal pathogenesis in complex syndromes is difficult to establish when the sequence of appearance of the pathologies is not clear. Among all the suspected causes, only one mechanism appears to be consistently present, soil ingestion. Soil ingestion is evident in all studies, and has yet to be abandoned in preference to any other single root cause. In fact, soil ingestion is the simplest explanation for excess wear and is implicated in many if not all of the related pathologies.

4.1.4 A role for earth surface processes?

The “Wairarapa syndrome” has been reported from a large district of the southeastern North Island, from Taihape at the edge of the Central Volcanic Plateau, to Raetihi, Stanway, Pohangina (the valley where the Te Awa experimental farm is located), Masterton, and Carterton (West, 2002). The last two areas are in the Wairarapa region at the southeast corner of the North Island (Bruere et al., 1979). The Wairarapa region is a sheep-farming district of pastureland in a wide valley east of the adjoining forested foothills of the Ruahine range. Average annual rainfall rises 92 Excess tooth wear in New Zealand

steeply from <1000 mm on the plain to over 5000 mm in the mountains, and reaches 1500 mm in the eastern hills and 2500 mm in the Aorangi Mountains. While rainfall is generally adequate throughout the year, summer droughts are frequent. Mean monthly temperatures range from about 5 C in winter to 16 C in summer. Pasture growth peaks are bimodal, peaking in October, falling to a minimum in late summer, resuming after autumn rains in March to May, and falling again in mid-winter. For the Te Awa research farm located just west of the Ruahine range, between Pohangina (to the south) and Apiti (to the north), in the valley of the Pohangina River, Suckling (1975) noted that summer droughts are coupled with strong winds that dry out the soil with consequent wilting of close-grazed pastures. Conditions were especially dry in 1954, 1960, and 1963. Additionally, heavy and consistent rainfalls in late autumn and winter led to saturated soils, and under these conditions, intense downpours in August 1961 caused extensive soil slipping and slumping of the regolith on hillsides throughout the district. The Wairarapa syndrome was exacerbated by especially inclement weather between the spring of 1977 and autumn of 1978. In this interval, heavy rains caused widespread erosion of the hill country. The rains were followed by a severe drought that led to a widespread shortage of feed (Bruere et al., 1979). During a seven-week period of unusual climate conditions in the winter of 1977, severe landslips in number and volume occurred in the Wairarapa and the Hawke’s Bay area to the north. Mass movement erosion included land slipping, debris slides, and mudﬂows that were especially prevalent on the steeper slopes (Lambert et al., 1984). The 1977 event was preceded by above-average rainfall. Cumulative rainfall was high, evapotranspiration rates were exceptionally low, and soil moisture was at capacity (Crozier et al., 1980). The total area affected extended from Wellington to Hawke’s Bay. During the study of this particular event, slip scars of four distinct ages were recognized (1977, 1961, 1941, and 1906) using aerial photographs (Trustrum and Stephens, 1981; Stephens et al, 1983; Trustrum et al., 1983).

4.2 The epidemiology and etiology of excess tooth wear

Soil ingestion causes tooth wear and temporal variation in soil ingestion drives temporal variation in tooth wear rates in domestic sheep in the North Island of New Zealand (Healy and Ludwig, 1965a, b). The mechanism linking earth surface processes to variation in tooth wear rates is soil erosion. Here I review available evidence for the relationship between soil erosion, soil ingestion, and tooth wear rates. From the evidence for temporal and geographic variation in soil ingestion, soil erosion contributes directly to the amount of ingested soil and thereby to rates of tooth wear. Furthermore, evidence shows that soil ingestion by herbivores varies geographically and temporally with the erosion processes that expose soil at the surface and mobilize soil minerals onto plant surfaces. Additionally, soil ingestion varies geographically with the attributes of soils that make them susceptible to erosion. 4.3 Geographic patterns 93

One of the greatest impediments to accepting a link between climate, the driver of erosion, and tooth shape evolution is the difﬁculty of “visualizing” how a relationship observed at ecological timescales (e.g., soil ingestion and tooth wear as seen by a veterinary pathologist) could operate at the timescale of evolutionary morphology as seen by a paleontologist. As will be shown, soil erosion is the key that bridges these timescales. Erosion is any disturbance of the soil surface that separates and transports soil mineral particles. Disturbances that increase the amount of exposed soil at the land surface include the pulling up of plant roots during feeding, trampling the soil surface by hooves at high population densities, rain-splash during torrential downpours, widespread storm-induced slumping of soil regolith that exposes large areas of soil parent material, and the deﬂation of denuded surfaces by wind and water. Soil erosion occurs at different geographic scales ranging from the displacement of mineral grains by a single raindrop, to the geographic area affected by a rainstorm-induced erosion event, and with zonal climate bands across continents at the same latitude. The hypothesis that tooth wear and soil ingestion should vary geographically with the susceptibility of soil to erosion leads to a prediction that there should be coincident geographic patterns of variation in rates of tooth wear, the rate of soil ingestion, and the intensity of soil erosion. The proposed mechanism also predicts geographic coincidence between the intensity of premature mortality (or the culling of domestic herds) for tooth senility and the intensity of soil erosion. Initial tests of coincident geography require comparisons of tooth wear and soil ingestion rates between study sites with different intensities of soil erosion.

4.3 Geographic patterns

Like the temporally coincident patterns of tooth wear, soil ingestion, and soil erosion, geographic variation in tooth wear and soil ingestion on the North Island of New Zealand can be related to geographic variation in the intensity of soil erosion.

4.3.1 Te Awa versus Feilding

Between 1954 and 1959, Hickey (1960, 1963) collected data on the mortality, fecundity, and longevity of domestic sheep in the southern North Island from abattoirs servicing sheep stations in the vicinity of Feilding (Table 4.1). Feilding, in the Whan- ganui, 19 km NNW of Palmerston North, is an area of flat, low, and gently rolling hills subject to little soil erosion (Grange and Gibbs, 1949). Hickey’s data show the onset of reproduction at 18 months of age and the fecundity curve describes a flat plateau through at least nine years of age (Figure 4.2). Hickey’s data provide an expectation for fecundity and reproductive longevity (Figure 4.1) in domestic ewes in areas unaffected by soil erosion. Tooth wear leading to premature dental senescence and culling was first studied in detail by Barnicoat (1947) at the Te Awa Experimental Station, an intensely managed experimental farm with improved pasture on moderately steep to steep hill country just 94 Excess tooth wear in New Zealand

Table 4.1 Contrasting geographies of Feilding and Te Awa

Location Coordinates Tooth wear Reference(s)

Feilding NNW of Palmerston 40.224 S Insigniﬁcant Hickey, North 175.568 E 1960, 1963 72 m.a.s.l. Te Awa Pohangina River, W of 40.179 S Noteworthy Suckling, Ruahine Range 175.859 E 1975 260 m.a.s.l.

west of the Ruahine Range and in the Pohangina River drainage about 30 km NE of Feilding. Subsequently, Barnicoat (1957), Ludwig et al. (1966), and Suckling (1975) all studied tooth wear in sheep at Te Awa. Te Awa is situated in a zone of high topographic relief and soft sedimentary soil parent material susceptible to rainstorm-induced landslide erosion. Te Awa thus provides a contrast to Feilding in terms of erosion susceptibility and ewe reproductive performance. Feilding is a flat area on late Pleistocene alluvium with a loess mantle unaffected by heavy soil erosion. Grange and Gibbs (1949) map the general area around Feilding as a zone of no soil erosion, and the steep land of Te Awa suffers significant rainstorm-induced soil erosion. For example, the area around Feilding was unaffected by landsliding in the February 2004 rainstorm event (Fuller, 2005) whereas Te Awa pastures, and the entire area NE of Kiwitea in the Pohangina River drainage between the valley bottom and high ridge of the Ruahine Range, was heavily impacted by landsliding during the February 2004 event. The geography of excess tooth wear can be compared to the susceptibility of soils to erosion using a map of the extent of rainstorm-induced landsliding in the February 2004 storm (Figure 4.3). Hickey (1960, 1963) collected fecundity and mortality data for domestic sheep on the North Island from stations in the vicinity of Feilding, an area unaffected by the February 2004 storm. The first studies of excess tooth wear by Barnicoat (1957), Ludwig et al. (1966), and Suckling (1975) were conducted at the Te Awa experimental farm where erosion was severe in the past, and still subject to episodic rainstorm-induced events of land-slipping (Suckling, 1954). The area affected by the 2004 storm (Fuller, 2005) is partly within the area of volcanic ash soils on the North Island (Gibbs, 1968), but extends beyond to encompass the soft-rock hill country of the southeastern North Island. The area affected by the 2004 storm is part of a larger area of the North Island with high erosion potential and susceptibility to rainstorm-induced erosion (Eyles, 1983). That erosion susceptibility is a property of the parent material and not the consequence of the most superficial recent ash fall is indicated by the displacement of the affected zone by the right-lateral strike- slip fault complex that includes the Wellington and Wairarapa faults. This fault-line displacement within the affected zone may be a result of the properties of soil parent material and topographic relief (Figure 4.4). Land-slipping occurs in all kinds of soils, and on all kinds of parent material and bedrock. While the soil parent material is varied, the yellow-gray loam soils on late 4.3 Geographic patterns 95

RAETIHI

TAIHAPE

Average % landsliding

SPOT imagery extent

0-1% STANWAY 1-5% 3 8 5-10% POHANGINA >10% 4 9

High tooth wear

Low tooth wear

Wairarapa syndrome polygon

ALFREDTON

1 MAURICEVILLE

MASTERTON 7 6 5

CARTERTON

Figure 4.3 Endemic area of excess tooth wear on the southeastern North Island and annual tooth wear rates plotted on a map of the intensity of surface erosion on the southeastern North Island of New Zealand. The intensity of surface erosion is represented by an event-proxy, the percentage of surface area affected by the cyclonic rainstorm event of February 2004, an ENSO-related cyclonic storm. (From Fuller, 2005 map prepared from SPOT data by Anne-Gettle Ausseil, courtesy of John Dymond, with permission from Landcare Research, Palmerston North.) Endemic area of excess tooth wear represented by enclosed polygon with tail, following Bruere et al. (1979). Study sites (numbered squares) and annual tooth wear rates as follows; 1 ¼ Wairarapa (1982¼3.97 mm/yr, 1983¼ 8.90 mm/yr), 2 ¼ Kaitoke (1982¼2.38 mm/yr, 1983¼1.55 mm/yr), 3 ¼ Pohangina (5.86 mm/yr), 4 ¼ Tangimoana (2.87 mm/yr), 5 ¼ Motukai (6.87 mm/yr), 6 ¼ Ranui (6.84 mm/yr), 7 ¼ Riverside (3.21 mm/yr), 8 ¼ Te Awa (high wear), 9 ¼ Feilding (low wear). Annual tooth wear rates for Kaitoke and Wairarapa from Thurley (1984, 1985a), for Pohangina, Tangimoana, Motukai, Ranui, and Riverside from Mitchum and Bruere (1984), and Mitchum (1985), for Te Awa from Ludwig et al. (1966). 96 Excess tooth wear in New Zealand

RAETIHI

TAIHAPE

STANWAY

3 8 POHANGINA 4 9

ALFREDTON

1 MAURICEVILLE

MASTERTON 6 Lake 7 Tutira 5

CARTERTON

Lake Wairarapa

Figure 4.4 The two endemic areas of excess tooth wear on the southeastern North Island plotted on a map of the percentage of surface area affected by the cyclonic rainstorm event of February 2004. (From Fuller, 2005; with permission from John Dymond, Landcare Research, Palmerston North.) The two areas are displaced by the Wairarapa–Wellington strike-slip fault complex, indicating that erosion susceptibility is a property of soil parent material. Symbols as in Figure 4.3.

Tertiary “New Group papa” is mostly mudstone and marls, and is often found to include volcanic minerals. The volcanic input usually is in the form of accumulations of windblown tephric loess, deposited during the Pleistocene and Holocene, with properties of high microporosity, low clay content, and poor cohesion, with interbedded marine limestones serving as slip surfaces. 4.3 Geographic patterns 97

4.3.2 Wallaceville versus the Wairarapa

A second geographic comparison was made by Thurley (1984, 1985a) who compared tooth wear rates between the Wallaceville experimental station where “normal” tooth wear was observed, and a sheep station in the Wairarapa reporting “excessive” tooth wear (Table 4.2). The “normal” property (eventually known as the Wallaceville Animal Research Center) is located at Kaitoke near Upper Hutt in the Wellington district. The Wairarapa property with excess tooth wear is located between Mauriceville and Alfredton, north of Masterton. As was the case for the comparison between Feilding and Te Awa, these two sites differ in the susceptibility of their pastureland to soil erosion (Grange and Gibbs, 1949; Eyles, 1983; Fuller, 2005). Soil ingestion and tooth wear at the two study sites can be compared with the susceptibility of soils to erosion as indicated by the average percentage of land surface affected by the February 2004 rainstorm (Fuller, 2005). Thurley conducted a two-year- long study comparing tooth wear at the Wallaceville Animal Research Center at Kaitoke and the Wairarapa sheep station. Annual rates of wear on central permanent incisors for 1982 and 1983 at both sites were indicated in mm/yr (see Figure 4.3). The Wallaceville Animal Research Center at Kaitoke, in the Upper Hutt valley, is an area of Quaternary fan and alluvial fill, surrounded by hill country. Kaitoke is situated on the flat bottom of the Hutt river valley east of Glade’s(1997) Wellington study area, on aggradational-degradational terrace and fan deposits eroding off deformed sandstones and mudstones (Berg and Johnston, 2003). While Kaitoke is situated geographically outside the zone affected by the February 2004 rainstorm, the surrounding area has a history of landslide erosion indicated by the distribution of abundant landslide scars on the steep slopes of the west side of the Hutt valley (Glade, 1997). However, even short distances (such as between the Wallaceville Research Center and the surrounding hills) may have great significance for soil ingestion and tooth wear when slope and relief increase dramatically across the axis of a major fault. The Wairarapa property, where high tooth wear was observed, is on massive to poorly-bedded calcareous mudstone parent material with minor rhyolitic tephra (Palmer, 1982; Berg and Johnston, 2003). This property is located just north of Glade’s Wairarapa study area, in an area the topography, soil parent material, and susceptibility to erosion of which is similar to the hill country around the Tauweru River southeast of

Table 4.2 The contrasting geographies of the Wallaceville Experimental Station and the Wairarapa property studied by Thurley (1984, 1985a, b)

Latitude/longitude/ Station Location altitude Tooth wear

Wallaceville Kaitoke, Upper Hutt (Wellington) 41.098 S; 175.103 E; 281 Normal m.a.s.l. 1982¼2.38 mm 1983¼1.55 mm Wairarapa Between Mauriceville and Approx. 40.727 S; High Alfredton, north of Masterton 175.796 E; 300 m.a.s.l. 1982¼3.97 mm 1983¼8.90 mm 98 Excess tooth wear in New Zealand

Masterton (see later). The Wairarapa property is within the area affected by the February 2004 rainstorm (see Figure 4.3). The vicinity of Mauriceville and Alfredton was heavily affected by landslide erosion during a 1981 storm (Crozier, 2005) and again during the February 2004 rains (Fuller, 2005). Thurley’s study was undertaken during the interval between September 1981 and December 1983, prior to and during the drought that began in Spring 1983 and lasted into 1984. A 1976 rainstorm-induced erosion event affected the Hutt Valley (Glade’s Wellington study area) ﬁve years prior to the beginning of Thurley’s study, and the 1977 and 1981 rainstorm-induced erosion events occurred in the Wairarapa closer to and at the start of Thurley’s study (Crozier, 2005). Thus, the higher wear rates observed in the Wairarapa may reﬂect this more proximate antecedent history. While both the Wellington and Wairarapa areas are susceptible to landslip erosion, Glade’s Wellington study area has a maximum threshold of 140 mm daily rainfall (Glade, 1998), whereas susceptibility is slightly higher in the Wairarapa (120 mm/d).

4.3.3 Six farms

Mitchum (1985) studied tooth wear and soil ingestion at six farms in southeastern New Zealand. These six farms extend in distribution from the West Coast of the southern North Island to the Wairarapa. One farm (Waipukurau) is situated farther north, in the southern Hawke’s Bay area. Mitchum (1985) provides further details about the geographic location, physical geography, and tooth wear conditions on these six sites. Tooth wear on the Waipukurau farm in southern Hawke’s Bay was studied between September 1983 and September 1984, and on the other ﬁve properties beginning in October 1983 and lasting until June 1984 (the study period did not include winter when soil ingestion and tooth wear is usually greatest). Fecal samples were dry-ashed and some were further processed for acid-insoluable residue. Incisor wear was measured at irregular intervals on about 20 individuals that had their central permanent incisors marked with a drill. Mitchum (1985) reported fecal ash as a percentage of fecal DM. There appears to be some seasonal variation in the amount of ingested plant ﬁber as measured by fecal ash. The study also reports acid-insoluable residue for some, but not all fecal ash samples. The proportion of acid-insoluable residue in fecal ash is not constant for all samples, that is, fecal ash is not a substitute for the measurement of acid-insoluable residue nor as a proxy for soil ingestion. This makes comparisons hazardous between Mitchum’s study and studies that measure soil ingestion using acid-insoluable residue. Moreover, detailed comparisons of seasonal variation in fecal ash and tooth wear among the six farms would require calibrating local lambing or birth dates, not only for reasons of tooth shape but more importantly for maternal effects on soil ingestion. Five of the six study sites of Mitchum (1985) and Mitchum and Bruere 1984) are mapped in approximate relation to the susceptibility of soils to rainstorm-induced landsliding as indicated by the February 2004 rainstorms (Fuller, 2005)(Figure 4.3). Annual tooth wear rates on the central permanent incisors (in mm/yr) are indicated in Table 4.3. Monthly tooth wear was measured only between January and May during the season 4.3 Geographic patterns 99

Table 4.3 Comparison of the geographies of the six farms studied by Mitchum (1985)

Latitude/ Farm or longitude/ station Location altitude Tooth wear rate

Waipukurau 6 km S of town of Waipukurua, Hawke’s 40.169 S “High wear” Bay, 50 km SW of Hastings, banks of 176.67 E (0.649 mm/yr) Tukituki River, Waipawa River Basin 189 m.a.s.l. Tangimoana W Coast, near Tangimoana, Manawatu- 40.299 S Normal (0.287 Wanganui, 30 km W of Palmerston North, 175.254 E mm/yr) south bank of mouth of Rangitikei River 14 m.a.s.l. Riverside 16 km N of Masterton, Wairarapa (valley of Not Normal (0.321 Ruamahanga River, Q alluvium valley available mm/yr) bottom) Pohangina 30 km N of Palmerston North, Pohangina 40.2 S Serious wear county, Manawatu-Wanganui 175.799 E problem (>0.586 224 m.a.s.l. mm/yr) Ranui E of Masterton, Wairarapa (in hill country Not Significant in either Whangaehu or Tauweru valleys) available incisor wear (>0.685 mm/yr) Motukai 15 km SE of Masterton, Motukai Road, near 41.075 S High wear Wainuioru, Wellington, Wairarapa 175.857 E (>0.688 mm/yr) 265 m.a.s.l. when wear is generally lowest (not between June and November when tooth wear and soil ingestion are generally highest). As might be expected, Mitchum (1985) found fecal ash concentrations (a less than ideal proxy for soil ingestion) were generally higher between June and November, when pasture production is generally lowest and soil ingestion generally highest. Considerable variation in annual tooth wear was observed between the six farms. High annual tooth wear rates were observed on four of the six properties (Pohangina, Motukai, Ranui, and Waipurkurau), all located on land susceptible to rainstorm-induced soil-slip erosion, as indicated by the February 2004 event. By contrast, the two properties with the lowest annual tooth wear (Tangimoana and Riverside) are situated in areas of low soil erosion (Grange and Gibbs, 1949). Tangimoana is near the coast of the Manawatu-Wanganui, 30 km West of Palmerston North, on the south bank of the Rangitikei River. Although there is some wind erosion from onshore flow here, the flat land along this coast experiences no landslip erosion. The other low wear property, Riverside, is situated 10 km North of Masterton in the Ruamahanga valley, on a flat alluvial floodplain unaffected by landslip erosion (Glade, 1997; Lee and Beeg, 2002). Three high tooth wear properties (Pohangina, Ranui, and Motukai) are in areas of high soil erosion, all within the area affected by the 2004 rainstorm event, and in areas with long histories of rainfall-induced erosion. For example, Mitchum’s study site at Pohangina is located in the same valley as Te Awa. Ranui is located east of Masterton just north of Glade’s Wairarapa landslide study area, and Motukai is located near Wainuioru, 15 km southeast of Masterton, just west of Glade’s study area. Both Ranui 100 Excess tooth wear in New Zealand

and Motukai are pastureland on hilly relief over massively bedded unconsolidated mudstone with minor rhyolitic tephras (Lee and Beeg, 2002) in areas with a history of susceptibility to rainstorm-induced erosion. A fourth high-wear site, Waipukurau, is a sheep station in southern Hawke’s Bay, on the banks of the Tukituki River, in the Waipawa Basin, an area subject to frequent rainstorm-induced landslide events, possibly the area most susceptible to this style of erosion on the North Island. The period of Mitchum’s ﬁeldwork (September 1983–September 1984) was one of signiﬁcant prolonged drought, one of the most intense El Niño’s in modern history. The climate couplet of heavy rains (above erosion thresholds) followed by prolonged drought may present a particularly active mechanism for the resuspension of soil minerals onto plants (see following discussion).

4.3.4 The geography of endemic excess tooth wear

The geographic distribution of the “Wairarapa syndrome” of dental and oral pathologies (some of which involve excess tooth wear) extends from Taihape at the southern edge of the Central Volcanic Plateau, and encompasses a polygonal area in the Manawatu- Wanganui demarcated by Raetihi (39.26S 175.17E), Stanway (near Feilding), and Pohangina (Table 4.4). The endemic area extends further to Masterton and Carterton east of the axis of the Ruahine range (Bruere et al., 1979). The authors also mentioned reports of the syndrome in the Napier region of Hawke’s Bay. The polygon described by the geographic areas mentioned by Bruere et al. (1979) corresponds to the area affected by the 2004 landslip event (Fuller, 2005) and the area notoriously susceptible to rainstorm-induced soil-slip erosion events (Figure 4.3).

4.3.5 Survey by the New Zealand Stock and Station Agents Association

Possible correlations between excess incisor wear and environmental factors were discussed by Barnicoat (1957), based on observational data obtained through a survey conducted by district ofﬁces of the New Zealand Stock and Station Agents Association.

Table 4.4 Geographic districts on the North Island where the “Wairarapa syndrome” has been observed (Bruere et al., 1979)

Geographic placename Location Latitude/longitude/altitude

Taihape Edge of Central Volcanic Plateau 38.686 S; 176.0697 E; 397 m.a.s.l. Raetihi 39.4276 S; 175.2818 E; 537 m.a.s.l. Stanway Near Feilding 40.0995 S; 175.5471 E; 176 m.a.s.l. Pohangina 40.1732 S; 175.7940 E; 219 m.a.s.l. Masterton 40.9490 S; 175.6608 E; 132 m.a.s.l. Carterton 41.0273 S; 175.5253 E; 82 m.a.s.l.

Note: Taihape was the ﬁrst area where sheep tooth wear was studied (Barnicoat, 1947) in the area of inﬂuence of Tongariro ash (Gibbs, 1968) from the Central Volcanic Plateau. 4.4 Temporal patterns 101

Barnicoat (1957) published a map of the average length of the exposed incisors in five-year-old Romney ewes throughout New Zealand. The teeth were not measured, but the survey provided ranchers with a photographic chart of a five-part classification for reporting average or general tooth condition of five-year-old ewes in their herds. Observations were restricted to ewes bred on farms “typical” of the district. From these survey reports the areas of relative wear were mapped. The map can be said to indicate geographic variation in the wear rate of central permanent incisors. Barnicoat (1957) compared the map of tooth wear (average length of exposed incisors in five-year-old ewes) with maps of the physical and botanical environments then available, including: (1) the 1947 Geological Map of New Zealand, (2) a map of soil types, (3) the 1955 map of New Zealand Landforms, (4) average annual rainfall (1930), and (5) a pasture survey map, but not the 1949 map of soil erosion of Grange and Gibbs (1949). Barnicoat concluded that while no correlation with geologic formation was evident, wear was related to climate and rainfall. Furthermore, teeth were not found to wear more on pumice land around Lake Taupo and near Waikato. Barnicoat also found that sheep on steeper high country under natural vegetation had better mouths, and the least wear was found in sheep from areas with an even distribution of precipitation throughout the year. These conclusions suggested that the simple presence of pumice is insufficient to cause high tooth wear and that natural vegetation stabilizes soil surfaces even in steep land. In addition, evenly distributed rainfall may cleanse plant surfaces and not induce significant erosion. “The least-worn teeth are found in mouths of sheep from the high-rainfall areas...[d]istribution of precipitation, especially in summer, rather than actual rainfall, is the crucial factor, and dews and mists undoubtedly contribute to maintaining succulence and softness of the grasses, which appears to be a major factor in preventing wear in sheep’s teeth...wind militates against this as it dries up and toughens the pasture and in some areas distributes abrasive matter as well.” (Barnicoat, 1957, p. 608).

4.4 Temporal patterns

In addition to the geographic predictions, three temporal predictions are suggested by the proposed link between climate and tooth wear. If climate is to be implicated as an agency underlying temporal variation in rates of soil ingestion and tooth wear, we should expect to ﬁnd temporal coincidence between these and climate-induced variation in rates of soil erosion. Temporal coincidence between tooth wear rates, soil ingestion, soil erosion intensity, and the climate drivers of soil erosion should occur over all timescales for which observations are available; including seasonal, interannual, and decadal, and when sustained and manifest by tooth shape evolution, at evolutionary timescales. Soil erosion occurs with each cropping bite, each diurnal activity cycle of feeding and ruminating, each seasonal cycle of herbivore reproduction and plant growth, at interannual cycles along with the ENSO, and with climate cycles at longer timescales such as the Inter-decadal Paciﬁc Oscillation that modulates the intensity of ENSO. 102 Excess tooth wear in New Zealand

4.4.1 Seasonal variation in soil ingestion and tooth wear

Seasonal variation in soil ingestion and tooth wear should be evident in all cases where wear and ingestion are monitored over an annual cycle or through multiple annual cycles. Indeed, all available studies document important seasonal variation in tooth wear and soil ingestion. The amount of incisor wear appears directly related to the amount of soil ingested by the grazing animal (Healy and Ludwig, 1965a, b; Ludwig et al., 1966). While pasture phytolith concentrations do not change through the annual cycle, tooth wear and soil ingestion have strong coincident seasonal peaks (Figure 4.5). On the North Island of New Zealand, fully 70% of annual incisor wear occurred between July and October, during the austral winter when fecal soil content exceeds 40% of DM (Ludwig et al., 1966). In another study, more rapid incisor wear was also detected between the months of July and September (Thurley, 1984, 1985a, b). Mitchum (1985) observed that the rate of wear of central permanent incisors was generally greater in winter and spring and less than in summer and autumn, and found this to correlate with higher fecal ash levels. Highest seasonal tooth wear and soil

70 2.5

60 Fecal AIR (ingested mineral particles) 2.0

50 (mm/sampling interval) Tooth wear rate 1.5 40

30 Tooth wear 1.0 (% dry matter) 20

Acid-insoluble residue (AIRf) 0.5 Ludwig et al., 1966 10 Healy and Ludwig 1965 Pasture AIR (phytoliths) 0 0.0 February June January June

Figure 4.5 Seasonal variation in tooth wear (closed diamonds) and soil ingestion (closed circles) at Te Awa (hill country research area of the Grasslands Division of the Department of Scientiﬁc and Industrial Research in the Pohangina River valley near the Ruahine Range), and seasonal variation in soil ingestion (open circles) and pasture phytolith concentrations (closed triangles) at a high-wear station in the Wairarapa district of the North Island of New Zealand. Whereas soil mineral abundance in fecal AIR varies seasonally and peaks during winter when animals feed aggressively and crop pasture plants close to the soil surface, the concentration of phytoliths in the AIR of pasture grass is essentially unvarying throughout the year and comprises only a modest proportion of fecal AIR. (Data from; Healy and Ludwig, 1965a, b; Ludwig et al., 1966; Healy, 1967, 1968.) 4.4 Temporal patterns 103

19 95 Temperature Soil Wear

90 Mean monthly precipitation (mm) 17

85 15 80

13 Precipitation 75

11 70 Mean monthly temperature (°C)

65 9

60 JFMAMJJASONDJ

Month

Figure 4.6 The austral winter peak in tooth wear and soil ingestion at Te Awa on the North Island coincides with the season of lowest mean monthly temperatures and highest mean monthly rainfall (long-term averages [1971–2000] from the nearest meteorological station at Palmerston North). Local monthly precipitation at Te Awa was more variable during the study period from February 1965 to January 1966 (Suckling, 1975).

ingestion occurs when mean monthly temperatures are at their lowest, and when rainfall is highest (Figure 4.6). Using long-term meteorological station data for Palmerston North, coincident peaks in the monthly variation in tooth wear and soil ingestion (Healy and Ludwig, 1965a) coincide with (1) the season of lowest mean monthly temperatures, shortest day-length, and slowest plant growth; (2) the rainy season of highest long-term average monthly rainfall (Figure 4.4); and (3) peak energy demand of pregnant and lactating ewes during the reproductive cycle of the SE North Island (Figure 4.7). Peak soil ingestion occurs in winter, coincident with high demands imposed by the reproductive cycle combined with the low temperature effect on plant vegetative growth. Both Ludwig et al. (1966) and Thurley (1984, 1985a) documented winter peaks in tooth wear. Mitchum (1985) failed to observe winter peaks in tooth wear because his monthly observational study only lasted the duration of the austral summer.

4.4.2 Interannual variation in soil ingestion and tooth wear

Few studies of soil ingestion and tooth wear in domestic sheep extend over more than a single annual cycle (Healy and Ludwig, 1965a, b; Arnold et al., 1966; Ludwig et al., 1966; Thurley, 1984, 1985a, b;), but all reveal year-to-year or interannual variation in 104 Excess tooth wear in New Zealand

Period of maximum reproductive and energetic stress 2.0 45

1.8 40 1.6 35

1.4 Wear (% fecal dry matter) Ingested soil (AIRf) 30 1.2

1.0 25

0.8 Soil 20 0.6 15 0.4 4 10 0.2 3 3

Tooth wear rate (mm/sampling interval) Tooth 2 22 Number of landslides 5 0 1 0 00 00 JFMASONDMJ JA

Reproductive cycle

Conception Lambing Weaning

Figure 4.7 The annual calendar of reproduction on the southeastern North Island. Peak tooth wear and soil ingestion coincide with the period of highest energy demand in the reproductive cycle of sheep (from Caughley, 1971). Peak tooth wear and soil ingestion are also coincident with the highest monthly frequency of rainstorm-induced landslides (landslips or slumps in the regolith) (from Glade, 1997).

the winter peak of ingested soil, tooth wear, and cumulative annual total tooth wear (Figure 4.8). All but one of these studies were conducted on the North Island of New Zealand, and for these studies, it is possible to assemble a partial extended multiyear chronology of tooth wear for the southern North Island using cumulative annual totals. The two most comparable published studies (Healy and Ludwig, 1965a, b; Ludwig, et al., 1966), between July 1964 and January 1966, extend over 19 months. The fairly comparable studies of Thurley (1984, 1985a, b) and Mitchum (1985) extend between September 1981 and September 1984, and comprise the longest continuous multiannual records of variation in tooth wear and soil ingestion (Table 4.5). Winter peaks in soil ingestion vary notably from year to year, as does annual tooth wear where it has been studied over a full year or longer (Figure 4.8). Why this should occur has never been explained satisfactorily. Interannual variation in soil ingestion and tooth wear was ﬁrst brought to the attention of veterinarians by the exceptionally exacerbated tooth wear immediately following the climate couplet of a rainfall-induced landslide event followed by prolonged drought that afﬂicted the Wairarapa district in 1977–1978 (Bruere et al., 1979). The “Wairarapa syndrome” of dental and oral pathologies was exacerbated between 4.4 Temporal patterns 105

70 A

60 Very high density High density 50 Medium density Low density 40

20 (% Faecal dry matter) Acid insoluble residue (AIRf) 10

0 Jul Jan Jul Jan Jul

B 60

40 High wear Medium wear 30 Low wear

20 (% Faecal dry matter) 10 Acid insoluble residue (AIRf)

0 Jul Jan Jul Jan Jul

60 C

50 Wa Po 40 Ta Ri 30 Mo

Faecal ash 20 Ra (% Dry matter)

0 Jul Jan Jul Jan Jul Month

Figure 4.8 Seasonal and interannual variation in fecal acid-insoluble residue. Top: monthly fecal AIR (AIRf) measured over two consecutive years (through three winters) in sheep from 106 Excess tooth wear in New Zealand

Table 4.5 Duration of short- and long-term studies of tooth wear and soil ingestion in domestic sheep in New Zealand (NZ) and Australia

Study (location, subject) Study start date Study stop date References

Taihape, Manawatu, NZ 1947 1952? Barnicoat, 1947, (1000 tagged ewes on 24 types 1957, 1959, 1963; of land, teeth) Barnicoat and Hall, 1960 Canberra, Australia July 1959 June 1961 Arnold et al., 1966 (longitudinal study of soil ingestion at monthly intervals, tooth wear semiannually) Te Awa, NZ 1963 1968 Suckling, 1975 (longitudinal study of wear at annual intervals) Wairarapa, NZ July 1964 July 1965 Healy and Ludwig, (3 properties, locations 1965a, b unknown, soil ingestion at 6-week intervals) Te Awa, NZ February 1965 January 1966 Ludwig, et al., 1966 (longitudinal study of soil ingestion and tooth wear at 6-week intervals) Wairarapa and Kaitoke, NZ September 1981 September 1983 Thurley, 1984, (longitudinal study of wear at 1985a, b 6-week intervals) Wairarapa and Manawatu, NZ September 1983 September 1984 Mitchum, 1985 (longitudinal study of wear and fecal residue at monthly intervals)

spring 1977 and autumn 1978 when heavy rain caused widespread erosion of hillslope pastures, followed by severe drought that in turn led to a widespread shortage of feed. This observation suggests that unusual (or perhaps cyclical) climate conditions may be associated with higher rates of tooth wear. If this association between tooth wear and climate is true, one might expect to register similar exacerbations of tooth wear after rainstorm-induced erosion and climate couplets of landslides followed by prolonged drought. That is to say, high values of cumulative annual tooth wear should coincide with interannual variation in climate factors controlling the intensity of soil erosion.

Figure 4.8 (cont.) New South Wales, Australia (Arnold et al., 1966) at four different stocking rates; solid circle (black), very high (9/acre); open circle (black), high (6/acre); closed circle (gray), medium (4/acre); open circle (gray), low (2/acre). Middle: seasonal variation in AIRf at three stations in the southeastern North Island of New Zealand reporting different rates of tooth wear; closed circle (black), high wear station; open circle (black), medium wear station; closed circle (gray), low wear station (from Healy and Ludwig, 1965a, b). Bottom: seasonal variation in AIRf at six different stations on the southeastern North Island, Waipukurau (Wa), Pohangina (Po), Tangimoana (Ta), Riverside (Ri), Motukai (Mo), Ranui (Ra) (from Mitchum, 1985). 4.4 Temporal patterns 107 Annual wear rates (mm) 4 10 9 3 8 2 7 1 6 5 0 4

(monthly) -1 3 2 -2 1

Multivariate ENSO index -3 0 1950 1960 1970 1980 1990 2000

Figure 4.9 Interannual variation in annual tooth wear rates in New Zealand plotted with the monthly Multivariate ENSO Index (MEI), an expression of climate variability in the tropical Paciﬁc. Monthly MEI (1950–2005) from NOAA Earth System Research Laboratory, Physical Sciences Division, Climate Indices: Monthly Atmospheric and Ocean Time Series (http://www. esrl.noaa.gov/psd/data/climateindices/). Monthly MEI uses six observed variables over the tropical Paciﬁc, sea-level pressure, zonal and meridional components of surface wind, sea surface temperature, surface air temperature, and the total cloudiness fraction of the sky, as standardized departures from a 1950–1993 reference period.

As already shown, when measured at monthly intervals, rates of tooth wear vary seasonally, and winter peaks of soil ingestion and tooth wear are coincident but winter peaks vary from year to year. When seasonal peaks of soil ingestion are plotted (Figure 4.8), there is considerable interannual variation between winter peaks. In addition, interannual variation in cumulative annual tooth wear is consistent with interannual variation in soil ingestion. Fluctuations in the highest recorded published values for annual tooth wear (mm/yr) are coincident with fluctuations in the Multivari- ate ENSO Index (MEI) (Figure 4.9). Positive MEI values correspond with La Niña events and negative values are El Niño events of the Southern Oscillation. In general, rainfall on the North Island is higher during La Niña years and lowest during El Niño years. These ENSO cycles are associated with increased storminess (Sinclair, 2002) and the periodicity of large-magnitude rainstorms that produce widespread landsliding on the North Island (Eden and Page, 1998). ENSO cycles have a variable period ranging from 2.5 to 7 years, but its usual frequency is between three and five years (Tudhope et al., 2001). Between 1803 and 1987, the mean time between moderate or stronger El Niños was about 3.8 years (Quinn et al., 1987). A vigorous maritime climate perturbed locally by the effects of cyclonic storms associated with the ENSO underlies the frequency and periodicity of rainstorm-induced erosion on the North Island. This storm-induced erosion contributes to the suspended sediment yields of New Zealand’s rivers, which are among the highest in the world (Hicks et al., 2000), and reflect widespread surface lithologies susceptible to erosion. Lacustrine and marine sediment basins along the East side of the North Island preserve a long temporal record of storm-generated landslide activity through the accumulation of storm runoff from surface areas of unconsolidated late Cenozoic and Quaternary marine sediments and eolian tephric loess. Soils developed on recent ash-fall deposits and on older Quaternary tephric loess are widespread in the hill country on the North Island. 108 Excess tooth wear in New Zealand

These soils and their parent material are weakly cohesive, and at these south temperate latitudes, have never been subject to strong chemical weathering. Today, on the east side of the North Island, rainfall-initiated shallow regolith landslides are the most significant erosional process and these episodic events expose great amounts of sediment on the land surface (Preston and Crozier, 1999). It has been established that significant landsliding occurs on hillslopes steeper than 18 degrees during rainstorms of more than 150–200 mm within a 72-hour period (Reid and Page, 2002). Slip scars of distinct ages (with mean dates of 1906, 1941, 1961, and 1977) are recognized using aerial photographs (Crozier et al., 1980; Trustrum and Stephens, 1981; Trustrum et al., 1983). Studies reveal six episodes of widespread storm-generated landsliding between 1965 and 1988 at a periodicity of just under four years, coincident with ENSO periodicity (Glade, 1997; Preston and Crozier, 1999). Sediment cores from Lake Tutira reveal an even longer history of these low-frequency high-magnitude storm-generated landslide events (Eden and Page, 1998). Over the longer term, the total amount of sediment produced during high-frequency but low-magnitude rainstorms is said to far exceed the contributions from low- frequency, high-magnitude landslide events (Hicks et al., 2000). Thus, normal high rainfall is itself a mechanism that serves to prolong soil mineral mobility long after significant storm-induced landslide events. While a correlation between interannual variation in soil ingestion (and tooth wear rate) and interannual climate variation has not been substantiated through the direct long-term study of tooth wear through one or more full ENSO cycles, there is suggestive coincident geography in the intensity of La Niña rains and El Niño droughts and anecdotal observations of dental pathologies in the veterinary literature in New Zealand (see later). The geography of La Niña rains in 1974, 1976, 1984, 1985, 1989, 1996, 1999, 2000, and 2001, and El Niño composite drought conditions for the years 1973, 1977, 1978, 1983, 1987, 1988, 1992, 1995, 1998, and 2003, mapped by Mullan et al. (2005), suggests coincidence between the type and intensity of soil erosion and the incidence of veterinary dental and oral pathologies. The chronology and coincidence of these merit long-term study, spanning full ENSO cycles (with transitions) on farms varying in the surface conditions leading to high susceptibility to erosion, including stations with a history of excess tooth wear.

4.4.3 Variation in tooth wear at decadal timescales?

In the absence of long-term studies, cyclical variation in tooth wear at longer timescales can only be established indirectly. For example, using a chronologic record of scientific publications about tooth wear and soil erosion as indirect “proxies” for incidents of intensified tooth wear and decadal-scale variation in the intensity of ENSO modulated by the Inter-decadal Pacific Oscillation (IPO) or Pacific Decadal Oscillation (PDO), temporal coincidence might be established. The period of most intense scientific publication about excess tooth wear (and associated pathologies) extended from 1947 to 1985. Within this period, there appears to have been five pulses of publication activity: (1) 1947, (2) 1957–1960, 4.4 Temporal patterns 109

Tooth wear and soil ingestion Soil erosion

5 4 3 2 1 Number of publications 0

1.5 1.0 0.5 0.0 E PDO -0.5 -1.0 -1.5 1900 1910 1920 1930 1940 1950 1960 1970 1980 1990 2000 Year

Figure 4.10 The role of longer-term (decadal) climate cycles on scientific publication relating to tooth wear and soil ingestion (black histogram) and soil erosion (gray histogram) in New Zealand. Positive anomalies of the Pacific Decadal Oscillation (PDO) are associated with more frequent and disastrous erosion events and higher scientific output as measured by the annual number of publications of studies of soil erosion and tooth wear. Annual PDO Index (1661–1991) from (http://www.ncdc.noaa.gov/paleo/pubs/biondi2001/biondi2001.html).

(3) 1965–1970, (4) 1973–1974, and (5) 1983–1985 (Figure 4.10). What might explain the period of interest (1947–1985) and the apparent pulses of scientific activity within that period? Do these simply reflect the episodic fits and starts of progress in understanding and solving a problem in veterinary pathology? Alternatively, does it reflect cycles in the soil erosion/climate system that drives variation in tooth wear rates and the government response (funding scientific activities) that naturally arises in reaction to climate-induced erosion events and significant outbreaks of excess tooth wear? A plot of the annual North PDO Index as reconstructed by tree ring chronologies (Biondi et al., 2001a, b) and a frequency histogram of the number of scientific publications about soil erosion and tooth wear in New Zealand by calendar year, suggests a temporal coincidence between erosion and tooth wear at decadal timescales. The North Pacific PDO Index of Mantua et al. (1997) is said to be essentially the same as the Inter- decadal Pacific Oscillation Index (IPO Index) of Salinger et al. (2001) that has been shown to modulate ENSO climate variability over New Zealand. Positive phases of PDO are associated with intensified scientific interest in soil erosion in New Zealand. Peak values of PDO Index during the 1946–1977 negative phase are associated with “outbreaks” of scientific interest in the pathology of excess tooth wear. There was also a coincident peak of scientific interest in tooth wear and soil erosion during the positive PDO phase between 1977 and 1988. Government funding to applied science, of course, responds to real events on the ground (at the soil surface, so to speak). What observation precipitated Barnicoat’s initial curiosity and the funding of his survey in 1947 and subsequent work between 110 Excess tooth wear in New Zealand

1957–1960? Barnicoat (1957) repeatedly emphasized that the problem of excess wear started in the 30–40 years prior to his study, that is, around 1927–1937. Unfortunately, premature dental senility cannot be related to the earliest significant erosion events recorded in the Lake Waikopiro and Tutira sediment cores (1917, 1924, 1938, and 1945) because station managers did not mark birth cohorts at that time. However, the 1945 landslide event preceded Barnicoat’s(1947) initial inquiry and subsequent ten- year study. In addition, the 1961 landslide event was followed up by Wellington’s postal survey in 1963 and the follow-on studies of Healy and Cutress between 1965 and 1968. An economically significant premature culling followed the 1961 erosion event (Suckling, 1975). The 1977–1978 rainstorm-induced landslide and drought couplet was followed in 1979 by the survey of Kane and Webster (Kane, 1984) and thereafter by the studies of Bruere and Mitchum (Bruere et al., 1979; Mitchum and Bruere, 1984; Mitchum, 1985). Did these apparent coincidences between erosion-induced increases in soil ingestion and accelerated tooth wear lead to an “epidemic” of obligatory premature culling that sheep farmers brought to the attention of the government? Was the flurry of scientific activity that yielded the important series of publications by Thurley, Mitchum, and Bruere between 1983–1985 initiated by the report in the journal “Surveillance” (Orr, 1983), suggesting farmers were reporting yet another incident of acute exacerbated tooth wear? Was this episode of increased scientific publication precipitated by yet another instance of a rainfall-induced erosion event followed by prolonged or intense drought conditions during a transition between La Niña and the particularly intense El Niño drought of 1983, as suggested by anecdotal observations in Mitchum (1985)? Three phases of the IPO have been identified during the 20th century: (1) a positive phase between 1922 and 1946 (a period with four significant rainfall-induced erosion events), (2) a negative phase between 1947–1976 (without any significant rainfall- induced erosion events), and (3) a more recent positive phase between 1977 and continuing today (with erosion events in 1985, 1988, and 2005). The IPO has been shown to modulate year-to-year ENSO precipitation and is a significant source of decadal climate variation throughout the South Pacific. The IPO also modulates variability in ENSO intensity over New Zealand. The negative phase of IPO between 1947 and 1976 corresponds to a period when La Niña rains were dominant over El Niño droughts. The positive phase of IPO beginning in 1977 and extending to 1998 corresponds to a period dominated by El Niño droughts. Thus, conceivably, the 1997–1978 La Niña–El Niño transition was unusual because it coincided with the shift out of the negative IPO phase in 1976 and into a positive phase in 1977. Temporal coincidences among lake sediment record, IPO index, and rainstorm frequency data suggest a relationship between soil erosion and decadal timescale variation in ENSO intensity (Figure 4.11). Storm sediment input events into North Island lakes (Page and Trustrum, 1997) are strongest during positive phases of the IPO index (Hobbs et al., 1998), as is rainstorm frequency (Glade, 1997). There was an increase of interest in soil erosion during the war years between 1938 and 1945, when the need for increased wool production led to the conversion of forest to pasture by fire and heavy grazing, which in turn increased the susceptibility of soils to widespread 4.5 ENSO, erosion, and tooth wear 111

Lake sediment cores IPO Index

2000 Lake Tutira Lake Waikopiro

0 1985 1985 1982-71 1977 1960 1963-60 1988 1988 1980

1985 500 1938 1938 1985 1977 1932 1973 1960 1924 1924 1960/1956/1954 1944 1960 1917 1917 1944 1943 1000 1910 1910 1895 1905 European arrival 1940 1897/1895 1938 1938 1500 LT15 European arrival LT16 1920 2000 1933 1933/1932/1929 1932 /1927 1924

Depth (mm) 1929 1918 1924 1917 2500 1900 1917 LW3 1916 1914 1910 3000 1906 1880 1905 1897 1895

3500 European arrival 1860 LW8

1840 321 0 -1 -2 -3 JFM

Figure 4.11 Lake Tutira and Lake Waikopiro cores reveal a chronology of storm-induced sediment input events, the frequency and intensity of which are coincident with positive IPO Index anomalies, and in turn with ENSO intensity and the frequency of above-threshold rainstorms (Page and Trustrum, 1997; with permission from www.schweizerbart.de). IPO Index (from Hobbs et al., 1998); rainstorm frequencies (from Glade, 1997).

slope failures (McSaveney and Whitehouse, 1989). Judging by the thickness of the 1938 and 1944 sediment input events in the Lake Tutira core, soil ingestion and tooth wear must have been correspondingly high, although there is no data that directly support this. While data bearing on the rate and extent of deforestation is not available for the war years, temporal variation in the percentage of bare ground between 1960 and 1985 also peaks in the intervals 1965–1968 and 1981–1985 (Whitehouse, 1984, Figure 2), corresponding to periods of high IPO index.

4.5 ENSO, erosion, and tooth wear

4.5.1 Erosion and the climate sea-saw

The main islands of New Zealand are located along convergent plate boundaries, are covered by widespread surface lithologies susceptible to erosion, have land surface that has experienced deforestation and conversion to pasture, and they enjoy a vigorous maritime climate perturbed locally by the effects of cyclonic storms and the ENSO. 112 Excess tooth wear in New Zealand

Lacustrine and marine sediment basins along the East side of the North Island preserve a record of this storm-generated landslide activity through the accumulation of runoff from surface areas formed on a variety of late Cenozoic marine sediments and eolian tephric loess. Suspended sediment yields of New Zealand’s rivers are among the highest in the world (Hicks et al., 2000). Rainfall-initiated shallow regolith landslides and gulley erosion are the most signiﬁ- cant erosion processes on the southeastern and eastern sides of the North Island (Preston and Crozier, 1999). Most landsliding occurs on hill-slopes during intense rainstorms (Reid and Page, 2002). Six episodes of widespread storm-generated landsliding occurred between 1965 and 1988 at intervals of just under four years (Glade, 1997; Preston and Crozier, 1999). Lake sediment cores on the North Island reveal this history (Eden and Page, 1998). Rainfall is higher during La Niña years and the ENSO has been associated with increased storminess (Sinclair, 2002) and frequent large- and smaller magnitude rainstorms (Eden and Page, 1998). Landslips or regolith slumps may be products of both, especially heavy normal seasonal rains, and extra-tropical cyclonic disturbances. Tropical cyclones are strong depressions and New Zealand gets the strongest storms in transitions between El Niño and La Niña phases of the ENSO. These storms are accompanied by strong winds and heavy rains. While the observed periodicities in widespread erosion events are coincident with ENSO periodicities, their association with positive or negative Southern Oscillation Index (SOI) extremes is not clear. What do El Niño and La Niña events mean for local weather anomalies in the area of the North Island where soil ingestion and the tooth wear of sheep was studied? During La Niña years, tropical storms move southward slowly and retain their intensity for longer. However, the strongest storms affect New Zealand during transitions from El Niño to La Niña (Sinclair, 2002). Cyclone Bola in 1988 occurred when the El Niño was fairly weak. A clearer signal is found in the pattern of storms accompanying enhanced easterly winds, reﬂecting the origin of storms as subtropical cyclones that are more in phase with La Niña conditions.

4.5.2 Wet climate erosion

Shallow landslides linked to high magnitude rainstorms are a conspicuous feature of deforested hill-country pastureland in the North Island. These landslides are slope failures occurring within the regolith above bedrock and are triggered by rainfall totals that exceed certain thresholds (Glade, 1997). They were observed by the early colonists and their signiﬁcance was noted very early in the process of deforestation and the transformation of the land to intensive pastoralism. They were ﬁrst described as “a mighty melting process” (Guthrie-Smith, 1921, p. 39). “Eastern Tutira, indeed, after a violent ‘buster’, appears to have been weeping mud. From the edges of all ancient slips the water-sodden fringes drip with clay; new red-raw wounds smear the green slopes, scalp-shaped patches detach themselves, slipping downward in slush and turf. Some- times a whole hillside will wrinkle and slide like snow melting off a roof, its huge corrugations smothering and smashing the wretched sheep, half or wholly burying them 4.5 ENSO, erosion, and tooth wear 113

in every pasture...After a ‘southerly buster’ or a ‘black nor’-easter’ of three or four days’ uninterrupted torrential rain, I have counted on a two-mile stretch of hillside over two hundred slips great and small, new or newly scoured out. Seven or eight times since [18]’82 the grasses and sedges of the valleys around the lake have been overlaid by mud verying [sic] in depth from six inches to a couple or three feet. Huge masses of solid hill have slid on to the larger flats” (Guthrie-Smith, 1921;p.39–40). Cumberland’s(1944) survey of soil erosion in New Zealand is an exceptional description of the mechanisms whereby soil minerals become mobilized at the soil surface by this process. With reference to the slips, slumps, and slow flowage erosion in the Wellington–Hawke’s Bay “hill country,” Cumberland has this to say: “[t]hese forms of erosion...are, perhaps, the most impressive and serious and the most disastrous in their ultimate effects of all the forms of erosion occurring in New Zealand in which man has had some hand” (p. 52). They effect the “late Tertiary and early Pleistocene mudstones, claystones, clay shales (‘rubbly papa’) and weak sandstones resting on equally weak and unstable Cretaceous sediments” (p. 52). “The presence of bentonite in varying amounts in some of these mudstones and claystones would appear to play a leading part in the ease with which slipping occurs” (p. 52, footnote 59). Eyles (1983) was the first to describe and map the scale, distribution, and severity of soil-slip erosion using a systematic national database of soil erosion observations. While many different kinds of erosion have been observed in the Wairarapa, soil slip erosion and earthflow are the two most intense and conspicuous. On the North Island, Eyles (1983) found that these occur most frequently on mudstone and fine siltstone, not claystone. Glade (1996) used historical records to draw a national map of the spatial distribution and temporal occurrence of landslide-triggering rainstorms for different regions. Generally, most precipitation falls in winter and historical data show that most of the landslides occur in the same period (Glade, 1998). In Hawke’s Bay, most landslide-triggering, high-intensity rainstorms occur between March and May. Since 1894, some 105 storms with more than 150 mm of rainfall occurred on a nearly annual basis. Of these, 20 were large rainstorms of 250 mm or more of precipitation within a two- to three-day interval, and resulted in the major erosion events. Some of the most notorious events were the 1938 Hawke’s Bay Flood (Grant, 1938– 39; Thornton, 1938–39; Lamont, 1939), the 1944 Anzac Rains, the 1977 land-slip event (Bell, 1976; Bruere et al., 1979; Crozier et al., 1980; Lambert et al., 1984), Cyclone Bola in 1988 (Marsden and Rowan, 1993; Page et al., 1994a, b), and the February 2004 rainstorm (Fuller, 2005; Hancox and Wright, 2005). Glade (1997) analyzed the historical record and found that larger landslide erosion events have a recurrence interval of 3.7 years in the Wairarapa and occur about once every 3.37 years in the Hawke’s Bay region. Both landslip scars and lake sediment cores reveal coincident histories of these storm- generated landslide events (Eden and Page, 1998). Around Lake Tutira, soils intergrade between pumice and loams formed in volcanic ash (Pohlen, 1971; Jensen, 1998), and the regolith is a combination of weathering products from marine sediments with eolian inputs of tephra and tephric loess (Page and Trustrum, 1997). With this composition, the regolith is highly permeable and rapidly becomes saturated. 114 Excess tooth wear in New Zealand

4.5.3 Volcanic ash and erosion on the North Island

The North Island of New Zealand contains the world’s highest concentration of youthful rhyolitic volcanoes, extensive pyroclastic flow deposits and abundant calderas, all primary features of topography. The active volcanoes include Egmont (Taranaki), Ngauruhoe, Pukekaikoire, Ruapehu, Tarawera, Tongariro, and White Island, all on the North Island and in adjacent waters. Most are aligned along a SW to NE axis extending from the Taupo volcanic center to the Coromandel volcanic center, and extending offshore to islands in the Bay of Plenty (e.g., White Island, Rumble islands, Whale Island) and beyond to the Kermadecs. Ruapehu, Ngauruhoe, and Tongariro are clustered at the southern extreme of the Taupo volcanic center, and no volcanic centers occur south of the latitude of Egmont and Ruapehu. Not surprisingly, volcanic ash deposits are the principal or a significant part of soil parent material of the North Island (Gibbs, 1968), and most volcanic ash soils on the North Island have formed from historical ash falls from nearby volcanic centers. The highest rates of erosion in the North Island are associated with unconsolidated marine and tephric sediments and their alluvial and eolian products. Tephra-covered pastoral hillslopes in the East Coast region of the North Island are especially prone to shallow landslides under near-saturation conditions and are caused by soil-strength reduction as the wetting front reaches the critical shear plane (Ekanayake and Phillips, 1999). Thresholds for triggering shallow landslides are combinations of rainfall, slope, and the hydraulic properties of soil. There is a 100 000-year history of pyroclastic sediment accumulation on the North Island. The prevailing westerly winds promote dispersal of ash mainly into East Coast basins and beyond into the Pacific. The tephra record is dominated by fluvially transported deposits and windblown loess. Fluvial systems have deposited tephra in units exceeding 20 m in thickness at distances of up to 250 km from the source. Even older Miocene and Pliocene marine basin sequences on the East Coast include tephra, and sedimentary basins on the North Island preserve numerous volcanic events and represent from 0.5 to 2.0 myr of deposition. The intensity and frequency of volcanic activity is reflected by the thirty named rhyolitic tephra dating from the last 64 kyr. In addition, the pre-64 kyr Quaternary record in the eastern sedimentary basins preserves 54 more events as fallout, fluvially transported volcaniclastic debris and distal pyroclastic flows in unconsolidated deposits. Few tephra are preserved from around the Last Glacial Maximum (LGM), when deposits are dominated by tephric loess and contain erosion surfaces. These late Quaternary loess deposits are widespread over lowland areas. Pillans (1991) describes the stratigraphy of Quaternary loess of the North Island, including most of Hawke’s Bay. In the Wairarapa and Wanganui Basins, the uplifted marine sediments include interbedded tephra, and Wanganui Basin marine units are overlaid by loess (Milne and Smalley, 1979; Palmer, 1982; Pillans, 1988, 1991; Vella et al., 1988).

4.5.4 Annual tooth wear and suspended sediment yield

Cyclonic rainstorm-induced erosion events result in a “halo” of plants contaminated by soil around the perimeter and down the slope from landslip scars. As sheep graze in this “halo” of contaminated pasture, they contribute to the enlargement and longevity of 4.5 ENSO, erosion, and tooth wear 115

these erosion scars. When the pasture cover is regenerating, the animals prefer this fresh growth, and through their preference for fresh green grass, the life of landslip scars is “sustained” even longer. The relationship between soil ingestion by sheep and soil erosion in their pastures is direct. Soil ingestion by sheep is simply a form of detachment and transport, and the grazing activity of the animals generates part of the mineral particle flux across the land surface and through their environment. Suspended sediment yield is an imperfect but reasonably good measure of erosion rates on the North Island, where much of the soil and regolith are reworked fine-grained tephra and most erosion is routed to river systems under variable and seasonally alternating wet–dry climates and rainstorm-induced events. From a geographic information systems (GIS) exercise using suspended sediment yield measured at about 200 sites and the key drivers of erosion, rainfall, rock type, topography, type and severity of past erosion, an empirical model was developed to predict suspended sediment yields from hydrographic basins without gauge stations. The model relates specific suspended sediment yield to mean annual rainfall and a terrain classification based on slope, rock type, soils, and dominant erosion processes. The model was calibrated from river suspended sediment gauge readings and sedimentation rates. Is suspended sediment yield a good measure of soil mineral particle flux and the active fraction of soil loss that has meaning for tooth wear? The relationship between suspended sediment yield and tooth wear (the consequence of soil ingestion) on the North Island can be established using the published annual tooth wear data for study sites on the North Island and the annual suspended sediment yields for catchments draining those sites. To answer this question, suspended sediment yield values were compiled for roughly similar 5–15 km2 surface areas around each study site (Table 4.6) to capture the essential characteristics of the site within the area selected. The correlation between tooth wear rates and suspended sediment yield (Figure 4.12) is indirect but meaningful, because soil erosion mobilizes mineral abrasives onto plant foods and sheep ingest soil directly (itself a form of erosion) as well as off the plants they consume. Although not immediately obvious, a polynomial function explains most of the variation (Figure 4.12). Tooth wear is directly related to soil ingestion, and the more soil ingested, the higher the tooth wear. Soil intake is ultimately limited by the dietary intake of digestible plant tissue, and eventually the ceiling (inflection in the curve) relates to the total plant matter consumed. Herbivores do not seem to eat more than they require. Additionally, soil intake should be limited by the plants’ capacity to sustain soil load that varies with adherence and other extrinsic conditions relating to mineral particle dynamics. The plot does not imply that soil has to be mobilized by erosion before it gets ingested by animals. The animals are grazing on the grass, not the soil. But if soil is mobilized by erosion, the animals will ingest more of it. For herbivores that feed farther from the soil surface, their ingestion of soil requires mobilization by erosion. Rain- splash is very effective at lofting soil mineral particles onto plant leaf surfaces, and wind is even better at lofting soil mineral particles onto plant surfaces and into the mouths of herbivores. 116 Excess tooth wear in New Zealand

Table 4.6 Long-term average suspended sediment yield in river catchments on the North Island of New Zealand of study sites where tooth wear rates and soil ingestion have been measured and range of speciﬁc suspended sediment yield (annual sediment yield divided by catchment area) for land surfaces drained by each catchment (http://www.niwa.co.nz./freshwater/management-tools/sediment-tools/ suspended-sediment-yield-estimator)

Suspended sediment yield (Kt/y) Stream (and range of speciﬁc sediment Tooth wear Catchment catchment yields for land surfaces drained study site (NZREACH number) area (km2) (t/km2/yr))

Between 7048374 12.3 11.1 Alfredton and Catchment extends 5 km SW (<200 to <5000) Mauriceville of town of Alfredton Between 9000901 11.6 3.2 Alfredton and Catchment extending NE of (<50 to <500) Mauriceville Mauriceville Ranui Undefined 12.1 6.2 Catchment 6 km NE of (<200 to <2000) Tauweru and 10 km E of Whangaehu Motukai 9009660 9 6.2 Catchment along Motukai (<200 to <5000) Road, 5 km SE of Wainuioru Kaitoke Undefined 6 0.6 Catchment along Hwy (<50 to <200) 2 draining Kaitoke Pohangina 7035541 14.2 18.8 Catchment NE of town of (<200 to <5000) Pohangina Te Awa 7033348 9.4 13.5 Catchment NE of Komako (<2000 to <5000) and NE of Kiwitea Riverside Undefined 4.4 0.2 Catchment flowing through (<50) Ruamahanga River valley 10 km N of Masterton Tangimoana Undefined 11.1 0.1 Catchment just S of estuary (<10) and S of town Waipukurau 8032143 6.9 4.3 Catchment 6 km SSE of town (<50 to <2000)

Hicks, D.M., U. Shankar, A. McKerchar, et al., 2011. Suspended sediment yields from New Zealand Rivers. Journal of Hydrology (New Zealand), 50(1):81–142.

4.6 Conclusions about the etiology of excess tooth wear

Ingested mineral particles are known to cause tooth wear and microwear studies show that linear striations on tooth surfaces result from the abrasion of mineral particles during mastication (Baker et al., 1959; Ciochon et al., 1990; Gali-Muhtasib et al., 1992; 4.6 Conclusions about the etiology of excess tooth wear 117

Annual wear rate (mm/y) 2

0 0246810121416 18 20 Suspended sediment yield (Kt/y)

Figure 4.12 Regression of annual tooth wear rates on suspended sediment yield for the southeastern North Island of New Zealand. Average annual tooth wear rates for each study site are plotted against NIWA-based suspended sediment yield for catchment areas of 4.4 to 14.2 km2 around each study site (see Table 4.6). Lalueza et al., 1996). Studies of the mineral particles that cause abrasive tooth wear distinguish between intrinsic (or endogenous) abrasives that form within plant tissues and extrinsic (or exogenous or adventitious) abrasives that occur as contaminants on the outside surfaces of plant foods or ingested directly off the soil surface. While both are known to contribute to tooth wear (Healy and Ludwig, 1965; Ludwig et al., 1966), extrinsic abrasives have been shown to be more abundant on herbivore foodstuffs at some times of the year and in some environments (Mayland et al., 1975, 1977;Arthurand Allredge, 1979) and signiﬁcant increases and decreases in the rate of tooth wear have been correlated with the amount of ingested soil as revealed in fecal material (Arnold et al., 1966; Ludwig et al., 1966). Geographic variation in the rate of tooth wear, as revealed by certain districts of the eastern and southeastern North Island that are notorious for premature culling for excess tooth wear, implies that other drivers operate there. These drivers may relate to the higher total amounts of ingested soil, and they may relate to prolonged soil ingestion during longer winters, or processes that sustain the delivery of high quantities of soil minerals into sheep diets, or the intrinsic properties of the ingested soil in these areas (e.g., enhanced abrasiveness). It has been shown that herbivore soil ingestion rates vary with stocking rates and season, with winter soil intake much higher than summer (Arnold et al., 1966; Healy, 118 Excess tooth wear in New Zealand

1967, 1968). At peak periods, sheep take in as much as 300 g to 400 g of soil per day, or about 25 kg over winter months (Healy, 1968). Ludwig et al. (1966) in their study of incisor tooth wear in sheep in the Te Awa hill country calculate that 1.5% of the acid- insoluble residue (AIR) from pasture was plant silica. They calculate that this amounts to approximately 9% of the AIR in feces. By comparison, soil mineral concentrations range from between 0% to over 40% of DM, and are at levels above 10% for nine months of the year. Thus, for most of the year, soil is the largest source of ingested mineral particles, and judging from the relative quantities, a much more important source of ingested mineral particles than plant silica. Levels of ingested soil are especially high during winter when pastures are characteristically short, pasture soils have abundant earthworm casts, and soil pasture grass is contaminated by soil minerals mobilized by the treading action of animals. Under these conditions, incisor tooth wear amounts to about 6.35 mm per year, with 70% of the total annual tooth wear occurring during the four months of winter when soil ingestion is highest. Signiﬁcant soil ingestion by grazing herbivores has been observed in Australia, New Zealand, and also in the United Kingdom where soil adhesion to vegetation is highest in autumn and winter, in the Lake District of Cumbria where vegetation samples were found to consist of up to 46% soil by dry weight (Beresford and Howard, 1991). Tooth wear may be produced by phytoliths in plant tissues, and where these are an unavoidable component of plant tissues, their contribution to rates of tooth wear will depend on their concentration in plant tissues, and the number that actually cross over and produce wear on occluding tooth surfaces. The concentration of silica phytoliths in plants, and especially in grasses, is low (Hodson et al., 2005). Phytoliths are embedded within leaf tissues, protected between or within thick epidermal cell walls, and covered by a lubricating wax and lipid cuticle. Most of the phytolith concentration in leaves passes through the mouth without ever leaving a trace on tooth surfaces, and much of the concentration passes through the digestive tract intact and in situ within incompletely digested plant tissue. Soil mineral particles, however, are either contaminants on the external surface of leaves or ingested directly off the soil surface, thus soil mineral particles always pass between tooth surfaces. Tooth wear produced by soil mineral contaminants on plant food varies with the environmental conditions that increase their concentration on plant foods. Extreme or excessive tooth wear can lead to premature tooth loss (Spence and Aitchinson, 1985) and may be accompanied by related periodontal pathologies (Wil- liams and Rudge, 1969; Porter et al., 1970; Rudge, 1970; Leader-Williams, 1980, 1982; Thurley, 1984, 1985a; Van Vuren and Coblentz, 1988). A general loss of condition accompanies advanced tooth wear when teeth loose the efﬁciency with which they subdivide plant food (Skogland, 1988; Kojola et al., 1998). In this way, excessive tooth wear leads to premature mortality (Anderson and Bulgin, 1984) and to an abbreviation of reproductive lifespan (shortening lifespan by as much as half, from 7 years to 3.5 years in domestic or hill sheep, according to Duckworth et al., 1962; Gunn, 1967, 1970a, b). Excessive tooth wear is known to result where herbivores occur in high density, leading to overgrazing, especially in winter, and when herbivores inhabit environments with high mineral particle mobility such as in hill country or on mountainous terrain (Thurley, 1983; Podwojewski et al., 2002). 4.6 Conclusions about the etiology of excess tooth wear 119

At temperate latitudes in New Zealand, soil ingestion has been found to vary seasonally with the growth rate of vegetation as influenced by temperature and rainfall and the seasonal reproductive demand on pregnant and lactating ewes. Seasonal peaks in tooth wear and soil erosion vary with seasonal peaks in rainstorms and rainstorms that result in extensive soil erosion. Seasonal peaks of soil ingestion and tooth wear also vary from year to year, as do cumulative annual totals, suggesting that erosion processes or events at interannual timescales contribute to longer-term temporal variation in tooth wear rates. Even longer cycles of climate variation at decadal timescales would be consistent with the intensity and scale of these same erosion processes, although in the absence of comparable long-term studies of tooth wear, their significance to rates of soil ingestion and tooth wear remains unknown. The available evidence suggests that rates of tooth wear may be explained by seasonal variation in soil ingestion during average climate, whereas acute conditions of exacerbated tooth wear are induced by extremes of ENSO variation. Abrasive soil minerals are mobilized by landslide erosion during cyclonic storms, the intensity of which varies through time in accordance with ENSO. Not only does New Zealand climate fluctuate between wet La Niña and dry El Niño conditions, the intensity of these conditions also fluctuates at longer decadal timescales. New Zealand climate has crossed thresholds in the intensity of soil erosion repeatedly since the late 1940s when veterinary pathologists first began to examine and remedy the consequences of excess tooth wear. These conclusions about climate-induced erosion as the ultimate cause of variation in tooth wear do not ignore the influence of proximate agencies such as density-dependent factors (stocking rate), mineral nutrition, the chemistry of the oral cavity, major changes in pastoral production systems, or hereditary differences, nor differences in cropping behavior or mechanical properties of teeth conferring resistance to abrasion, nor any of the other proximate causes that have interested and vexed veterinary pathologists. It simply proposes a causal mechanism (soil erosion, soil ingestion, tooth wear) that operates on several different timescales. The prevalence of this mechanism makes it seem plausible that it might operate at evolutionary timescales. However, before beginning to contemplate the implications of earth surface processes for dental evolution, we must ask whether what has been observed and established for the North Island of New Zealand can be observed or established elsewhere. 5 Soil erosion, soil ingestion, and tooth wear in Australia

5.1 Introduction

After Antarctica, Australia is the driest continent on Earth. It is also the lowest and flattest. Australia sits astride the southern horse latitudes, the climate zone of high atmospheric pressure, high evaporation, low rainfall and where we find the highest levels of faunal hypsodonty globally (see Chapter 3). Much of Australia is semiarid, arid, or hyper-arid desert, surrounded by a wide concentric ring of dry country grasslands. Australia is renowned for climate variability and extreme events. Dust storms, wildfires, floods, and cyclones (typhoons) punctuate the most highly variable agricultural productivity of all major grain exporters. Australia is home to a unique mammalian (or metatherian) fauna that evolved in geographic isolation from the rest of the world. However, with only a few exceptions, there are very few high-crowned marsupial herbivores. Christine Janis (1989) has argued that the bilophodont teeth of kangaroos could not have evolved hypsodonty because of a functional constraint, the requirement to maintain the functional utility of the lophs. Sanson (1980) has argued that grazing kangaroos resort to a different contrivance (or set of contrivances) to prolong the functional longevity of their teeth, including the progressive replacement of worn-out crowns of smaller earlier-erupting teeth that are shed by being pushed out or displaced by larger later- erupting teeth as these migrate forward to replace them. It is difficult to find a scientific basis for comparing these two alternative structural expressions of an adaptation to high abrasion, but it is conceivable that both alternatives (hypsodonty and serial tooth replacement) may generate an equivalent volume of tooth mineral substance over the total reproductive lifespan of the individual. Nevertheless, for a land like Australia that is dominated by grasslands and variable climate punctuated by extreme events, it is remarkable that so few elements of its native terrestrial fauna evolved high-crowned teeth, especially because a few did (the wombat), and in large numbers (more on this later). Given the prevalence of grasslands on the continent and the notorious dust storm record across southeastern Australia, this southern continent ought to provide the perfect test of whether grass consumption or earth surface processes play a dominant role in tooth wear and the evolution of tooth shape.

120 5.1 Introduction 121

The only long-term study of tooth wear in a living herbivore in Australia, the study that gave rise to the general belief implicating phytoliths as the cause of most tooth wear in sheep (and other herbivores), will be examined in some detail and an effort made to characterize what in fact was actually established about the causes of tooth wear in sheep. These classic studies will then be placed into the context of work on erosion and surface processes in New South Wales (Figure 5.1), where the original study was conducted, with special attention on surface conditions during the time of the study, the adventitious mineral content of sheep feed, the intensity of grazing at the soil surface, and mineral particle accession to pasture soils, all of which may have contributed to ingested silica and tooth wear. To provide yet another case testing the role of surface processes in the same part of the continent but at a different timescale, I then review what has been established about aboriginal tooth size and tooth wear. Through these examples, we will examine the essential features of surface processes on the continent before returning to address the original question. Related discussions about ﬂuvial-eolian interaction in the southeast

Figure 5.1 Mechanical dust flocker. Sheep grazing and wool production in the southern tablelands of New South Wales have a remarkable history (McManus, 1966). Part of that history is how ranching practice adjusted to the high concentration of dirt, sand, and soil in sheared wool. Sheep flocking machines were introduced for removing dust and grit from sheared wool. Today, aqueous wool scouring effluent is an important byproduct of the natural fiber washing industry in the aridlands of Australia, and the recovery of waste water is important to its efficiency. (With permission from the Office of Environment and Heritage, National Parks, New South Wales at http://www.environment.nsw.gov.au/resources/parks/cmpFinalKinchegaVol1Sec3Part2.pdf) 122 Soil erosion, soil ingestion, and tooth wear in Australia

dust path and the signiﬁcance of the introduction of rabbits to erosion of Australian rangeland are deferred to later chapters. There is a curious historical coincidence behind the interest of science in sheep soil ingestion and tooth wear in the late 1950s and early 1960s that may explain, at least in part, why the role of intrinsic abrasives in plants came to dominate the discussion of herbivore tooth wear and tooth shape evolution for so long.

5.2 The original study of sheep tooth wear

5.2.1 Introduction and scientiﬁc impact

One particular experimental study and another long-term study of wool production in Australian sheep seem to have pointed a finger at grass phytolith consumption as the cause of tooth wear. The experimental study was undertaken by Baker et al. (1959, 1961), and will be reviewed here. The long-term study of wool production was conducted in southeastern Australia from May 1958 through June 1961 (Arnold et al., 1964a, b, 1965, 1966; McManus et al., 1964, 1965, 1966). This study placed emphasis on the role of stocking rate (population density or grazing pressure) on the wool production system of southern New South Wales, but included observations on tooth wear and both seasonal and interannual variation in silica ingestion during the period from June 1959 to July 1961 (Arnold et al., 1966). As part of the long-term study, researchers undertook to determine the concentration of plant phytoliths and adventitious silicate minerals and to relate this in a general way to the total acid-insoluble residue in fecal material (AIRf), tooth wear, and grazing pressure. The concentration of opal phytoliths in the silica excreted with fecal material was found to be very low (<1% of DM), and the association between tooth wear and excreted silica suggested that incisor tooth wear was due primarily to contact with the soil surface, rather than plant opaline abrasives (Arnold et al., 1966). This result was surprising, given that just prior to these studies, high concentrations of plant silica had been observed in an experimental setting by other researchers in Australia (Baker et al., 1959, 1961). Most recently, the significance of the mineral hardness values for silica phytoliths reported by Baker et al. (1959), and by implication, the dominant role of silica phytoliths in tooth wear in general, has been brought into question (Sanson et al., 2007). The experimental studies by Baker et al (1959, 1961) have long influenced the prevailing view in science that gives plant silica special status in the evolution of mammalian tooth shape. That such great significance was given to an idea originating in a highly unusual experimental setting of sheep provisioned by commercial feed and published in a single conjecture in Nature is remarkable and troubling. In this particular case, publication in Nature had an exaggerated impact on the citation histories of two contrasting ideas, that is, whether phytoliths or soil mineral particles cause significant and excess tooth wear in sheep. 5.2 The original study of sheep tooth wear 123

Table 5.1 Citation counts for the original experimental study (Baker et al., 1959) and contemporary long-term studies of sheep tooth wear and soil ingestion in Australia and New Zealand published in technical journals

Serial Publication (subject) Citation count as of 2010

Nature Baker et al., 1959 (phytoliths) 99 Healy and Ludwig, 1965a (soil) 66 Technical serials Baker et al, 1961 (phytoliths) 20 Ludwig et al., 1966 (soil) 13 Arnold et al., 1966 4 (phytoliths and soil)

Google Scholar citation counts for Baker et al. (1959) and Healy and Ludwig (1965), both published in Nature,revealasignificant readership, but the Baker article on phytolith mineral hardness has been cited far more often than the long-term study by Arnold and others and the work of Healy, Ludwig, and associates on soil ingestion. The significance of these citation counts for high-profile Nature articles is best understood when compared to the citation history of subsequent more substantive research results as reported by Google Scholar in 2010 (Table 5.1). The next year, Arnold et al. (1966) described, in much more detail, the relative significance of phytolith and soil ingestion in a long-term study, published in a technical agriculture research serial in Australia. The contrasting low impact of this more substantive empirical study is dramatic. While there were well over a hundred subsequent citations for the brief Nature article (Baker et al., 1959), there were only 7 and 35 citations (Google Scholar, Web of Science, respectively) for the more substantive technical publication. The contrasting citation histories suggest that science sometimes operates more on high impact than careful scholarship. Baker et al. (1959) implicate phytoliths based only on their abundance in samples of commercial feed and their relative mineral hardness in brief descriptive studies of a special case (see later). There are only 16 and 27 citations for a somewhat later paper (Baker et al., 1961) describing the plant samples (oat chaff feed supplement) and how the phytoliths were processed prior to measuring their hardness, despite the fact that the consequences of laboratory preparation to the chemistry and physical properties of phytoliths was known at the time (Jones and Milne, 1963). Citation counts are still lower for Arnold et al. (1966), who presented a convincing demonstration of the lack of significance of phytolith abundance on total ingested silica in pasture-grazed sheep in outdoor enclosures, and conclude that tooth wear is the consequence of soil contact and soil ingestion.

5.2.1.1 The study site The original long-term study was conducted at the Commonwealth Scientiﬁc and Industrial Research Organization’s (CSIRO) Dickson Experiment Station, a 270-hectare research site of the Division of Plant Industry that operated between 1940 and 1965 in what is now the Downer suburb of northern Canberra. Originally an area of native grasslands, the CSIRO station was a big open paddock with Monterrey pine windbreaks 124 Soil erosion, soil ingestion, and tooth wear in Australia

until suburban development commenced in the 1960s. Mounts Majura and Ainslie are to the east and the Namidgi National Park to the west. Sullivan’s Creek runs through the area before emptying into Lake Burley Grifﬁn and from there into the Murrumbidgee River, part of the Murray–Darling hydrographic basin (ACT Heritage Council, 1960). Near the southeast part of the southern tablelands of New South Wales (McManus, 1966) and in the meteorological district of the Southern Tablelands, the study site is located east of the wheat–sheep zone (Michalk, 1980) where climate and topography permit aridland grain-cropping and sheep grazing in a crop–pasture rotation. The Dickson Experimental Station in Canberra sits squarely on the southeast dust path (McTainsh et al., 1998)(Figure 5.2). During the study, sheep were grazed outdoors on Phalaris aquatica–Trifolium subterraneum clover pastures at stocking rates ranging from 22/ha to 5/ha. Phalaris aquatica (canary grass, syn P. tuberosa), a perennial bunchgrass introduced from Europe, became an important winter-active pasture grass in this part of Australia. Subterranean clover (Trifolium subterraneum) is an introduced rangeland legume.

5.2.1.2 The research method The long-term study collected data on silica ingestion for the period June 1959 to July 1961 (Arnold et al., 1966). Arnold et al (1966) described the method to determine both total silica and phytolith concentrations in sheep fecal material and reported both the acid-insoluble residue as a percentage of dry fecal material (AIRf) and phytolith counts (PC). Fecal samples were ﬁrst dry ashed and non-siliceous material removed by digestion with hydrochloric acid. In essence, AIRf provides a measure of total ingested silica (Arnold et al., 1966). From the AIRf, microscope slides were made using a subsample of the silica residue. An unknown but “constant” amount was placed on each slide and opaline silica particles were counted under polarized light “at extinction” in ten ﬁelds of vision for each slide. While the authors do not describe how plant opaline silica was distinguished from soil silicates, in a diet of Phalaris clover pasture, plant silica morphologies would have been uniform. As the authors state, “the method is not quantitative but allows a rapid assessment of a large number of samples.” Counts of opaline silica particles (PC) are reported as well as AIRf, but not phytoliths as a percentage of AIRf. Neither the composition nor relative proportions of adventitious silicate minerals in the AIRf were described. Nor did the researchers distinguish between loose phytoliths (the fraction that may have contributed to tooth wear) and phytoliths wholly embedded within intact plant tissue (the fraction that could not have contributed to tooth wear). Any soil carbonate in the fecal material would have been dissolved by acid preparation.

5.2.2 Observed results 5.2.2.1 Tooth wear The central incisors were marked at the gum line on July 1, 1959 and the mean length of the clinical crown (mm) was recorded about every six months over the two-year duration of the study. Cumulative wear on the permanent central incisor ranged from 5.2 The original study of sheep tooth wear 125

Figure 5.2 Australia and the principal geographic features of the southeast dust path (large gray arrow). A line of demarcation extending from Fowler’s Gap to Cowra north of Canberra (McTainsh et al., 1998) separates the northern from southern dust paths across New South Wales and distinguishes their main dust source areas, the northwestern source region and the southwestern source region around Lake Eyre (Cattle et al., 2009). New South Wales has two different dust storm seasons, in the northern region encompassing most of NSW (and Queensland), the dust storm season runs from September to January, and in southern NSW (and Victoria), the dust storm season extends from December to March.

2 mm to 12 mm. At the highest stocking rate, an average cumulative total of 12 mm of crown height was lost to abrasion over two years. Tooth wear was greatest at the highest stocking rate, and diminished with decreasing stocking rates. After two years at the highest stocking rate, the central incisor was worn to the gum line in some individuals. Even at medium and high stocking rates, the occlusal table of the incisor arcade was depressed at the mid-line by high wear on the central incisors. This distinctive pattern of wear, and its association with high stocking rates suggested to the researchers that most incisor wear was probably caused by direct abrasion at the soil surface (Arnold et al., 1966). 126 Soil erosion, soil ingestion, and tooth wear in Australia

5.2.2.2 Fecal silica Over the course of the study, seasonal and interannual variation in silica ingestion were observed. Fecal silica content (AIRf) showed signiﬁcant seasonal and treatment (stocking-rate) effects, with a single peak in mid-winter. At the highest stocking rate and during the winter peak, silica amounted to 66% of fecal DM. As on the North Island of New Zealand, peak silica ingestion occurs every year during the austral winter between June and September, the season of lowest mean monthly temperature, and slowest plant vegetative growth. Phalaris is a winter-active grass, and peak silica ingestion occurs during the reproductive season when pasture is green and monthly rainfall highest. The amount of ingested silica (AIRf) during the peak winter season varies from year to year (see Figure 5.3, top). Over the three winter seasons of the interval of study, the July–September 1959 and June–July 1961 winter peaks were less than peak soil ingestion observed during the winter of 1960.

5.2.2.3 Plant phytolith counts Fecal sample preparation also included washing then ashing the remaining plant fragments. The ash was prepared in acid subsequently and the phytoliths counted as a subsample of the residue. In effect, this measures the abundance of phytoliths in intact plant tissue, and provides a relative measure of pasture phytolith concentrations or concentration in undigested forage.

5.2.2.4 Results Do PCs vary in any systematic way with what is known about (1) peak phytolith concentration at either the beginning (McNaughton et al., 1985) or toward the end of the growing season (Sangster et al., 2001), or (2) the positive correlation between grazing pressure and phytolith concentrations in plants and consumed plant parts (Barthram and Grant, 1984; McNaughton et al., 1985), or (3) the decline in herbage intake at higher stocking rates (Wade and Carvalho, 2000), or (4) seasonal variation in the amount of ingested pasture grass (Crawley, 1983, 1997)? As measured (see Figure 5.3, middle), there is a slight peak in fecal opaline silica counts in late summer–autumn (March–May), possibly related to seasonal pasture break, and these peaks were highest at medium to very high stocking rates. By contrast, the peak in AIRf occurs in winter and early spring when pastures are green and ewes are pregnant or lactating, and peak AIRf is highest at high to very high stocking rates (Figure 5.4). Thus, the highest observed or peak PC and AIRf are not coincident. Are there significant grazing intensity (density treatment) effects to either AIRf or PC? A one-way ANOVA testing group means against the grand mean, shows significant treatment effects to both AIRf (P<0.0001) and PCs (P¼0.0021) (Figure 5.5). Means comparisons (Tukey–Kramer HSD at P<0.05) show AIRf as significantly higher at very high grazing intensity, and PCs lowest at low grazing density. There is a trend toward higher AIRf with increasing grazing intensity from medium to high and from high to very high stocking rates, but no similar trend for PCs. 5.2 The original study of sheep tooth wear 127

Figure 5.3 Acid-insoluble residue as a percentage of fecal DM (AIRf), top; phytolith slide counts, middle; and incisor tooth wear rates, bottom; during the 740-day period between June 1959 and July 1961 in relation to grazing intensity or stocking rate (individuals/acre). Gaps in the temporal continuity or regularity of data are real. (Original data from Arnold et al., 1966.)

Seasonal effects on AIRf (P¼0.0014) and PCs were tested by one-way ANOVA (P<0.0001), but means comparisons show AIRf is highest in winter, whereas PCs are highest in autumn. PCs are lowest in December through February and highest in March through May, with peak counts occurring in April. AIRf appears to increase in autumn but only reaches a signiﬁcantly high peak in winter, whereas PCs are dramatically higher in autumn and appear to diminish through winter and spring. Quantile plots for each season reveal unequal and larger variances for these peak seasons, reﬂecting important interannual variation in peak season concentrations (Figure 5.6). 128 Soil erosion, soil ingestion, and tooth wear in Australia

Figure 5.4 Fecal acid-insoluble silica residue (AIRf), top, and phytolith slide counts, bottom, with season, pasture cycle, and reproductive cycle.

500 60

50 400

40 300

AIRf 30 200

20 Phytolith count

100 10

0 0 LOW MED HIGH VHIGH LOW MED HIGH VHIGH Stocking rate Stocking rate

Figure 5.5 The effect of grazing intensity on fecal acid-insoluble residue (AIRf), left, and phytolith slide counts (PC), right. One-way ANOVA for treatment effects is statistically signiﬁcant for each measure of mineral particle ingestion (using JMP v3.1, SAS Institute); for AIRf F3,144 ¼ 12.2959, P<0.0001, and for PC F3,144 ¼ 5.1438, P¼0.0021. 5.2 The original study of sheep tooth wear 129

70 500 60

50 400

40 300 AIRf 30 200 Phytolith count 20

100 10

0 0 Autumn Spring Summer Winter Autumn Spring Summer Winter

Season Season

Figure 5.6 Seasonal effects on AIRf, left, and phytolith slide counts, right. Results of one-way ANOVA for signiﬁcant seasonal effects on AIRf and PC (using JMP v3.1, SAS Institute); for AIRf F3,144 ¼ 5.4821, P¼0.0014, and for PC F3,144 ¼ 23.5304, P<0.0001.

At all stocking rates, PCs are lowest in summer, during the season of highest dust storm frequency, and there were significantly higher peak counts in the first six months of 1961 compared to 1960 (P<0.0071) (see later). In contrast to PCs, AIRf gradually increases from a low in December through June, and this appears true at all stocking rates. At high stocking rates, AIRf continues to increase from July through September in 1959 and 1960, but to very different peak values from year to year. What explains the observed results? There does not appear to be much of any relationship between AIRf and PCs at most stocking rates except the lowest (P>F¼0.0047, R2 adjusted¼0.224). If plant silica is the only component of AIRf, you might expect that AIRf would track PCs fairly closely at all stocking rates. As most of the variation in AIRf silica is unrelated to PCs at all but the lowest grazing intensity, AIRf may be capturing the ingestion of adventitious abrasives directly from the soil surface or indirectly through leaf soil load. The authors of the original study did not report PC as a fraction of AIRf. Bivariate regression of log transformed PC on AIRf for low and very high grazing intensities have low RSquare Adj values (0.1916 and 0.1023, respectively) although ANOVA values are significant (P>F¼0.0056 and 0.0343, respectively) and parameter estimates for log (AIRf) are also significant (P>|t|¼0.0056 and 0.0343). The low slope and R2 value suggest PCs are not accounting for the silica content of AIRf. The fit and dispersion of points suggests closer correspondence between PC and AIRf at low grazing intensity. However, at very high grazing intensity, while a similar relationship is found at AIRf values less than 30% fecal DM, when AIRf is from 30% to 70% of DM, PCs remain low and constant. Thus, high AIRf is not explained by high PCs. At high grazing intensity, more soil was being ingested. As PC was not reported as a fraction of AIRf, and AIRf was reported as a percentage of fecal DM, it is not possible to make a direct comparison between phytoliths and adventitious mineral particle abundances. However, PC and AIRf as a percentage 130 Soil erosion, soil ingestion, and tooth wear in Australia

of DM were both reported as monthly time series over the two-year duration of the study. In this way, it is possible to examine patterns of temporal congruence. Should PC account for all AIRf, there should be precise temporal congruence. To the extent there are differences in the temporal patterns of abundance, the composition of AIRf must be distinct. AIRf is a percentage ranging between 3.5% and 66.4%, and PC is a count between 29 and 505. How should these very different variables be handled? Log transformation helps reduce skewness, but the ranges are still very different, therefore they were also standardized to zero mean and unit standard deviation. Smoothing splines were fitted to the standardized and log transformed PC and AIRf at two lambda levels (lambda¼0.01 and 1 000 000). At lambda¼0.01, the smoothing spline fits to actual values; at lambda¼1 000 000, the spline functions as a “running average.” Not surprisingly, there is no coincidence between the observed peaks in phytolith abundance and the peak season of silica ingestion (AIRf), and variation in the concentration of phytoliths in undigested plant material does not explain peak AIRf (Figure 5.4). One might expect that peaks in relative opaline silica counts should be consistent with highest intake. Curiously, in the study, sheep had higher digestible organic matter intake at high stocking rates (1100 gm/d) than at low stocking rates (350 gm/d) in spring, and also in summer (680 vs. 200 gm/d) (McManus, 1966). Judging from intake, one would expect that opaline silica counts would be highest at high stocking rates, and higher in spring than in summer. Neither is the case. The late summer–autumn peaks in relative opaline silica counts were brief and did not coincide with the winter seasonal peaks in AIRf or spring peak in organic matter intake. To the extent that opaline silica counts are a measure of the phytolith content of intake, the lack of agreement suggests that AIRf is measuring ingested silica off the land surface and not simply phytoliths. Thus, the slide counts of opaline silica are unrelated to either stocking rates or organic matter intake. The observed unsystematic variation in PCs may be masking a more significant underlying fact, that slide counts of plant-sourced opaline silica were, in essence, fairly uniform throughout the year, and insignificant to the observed variation in AIRf and tooth wear.

5.2.2.5 Questions left unanswered From the pattern of wear on the incisors (Arnold et al., 1966, Figure 2), incisor tooth wear is a consequence of feeding at ground level. Given that AIRf increases with stocking rate, these observations seem to imply soil ingestion. While Arnold et al. (1966) implicate feeding at ground level, they do not describe the mineral composition of AIRf. If most or a substantial fraction of the soil composition is carbonate, weathered limestone, or carbonaceous parna, we would see tooth wear, but no AIRf. Instead, we see high levels of AIRf. What is the siliceous fraction of local soils and are the surface soils alluvium or eolian, or the result of accessions from a combination of earth surface processes? As on the North Island of New Zealand, there is interannual variation in the amount of AIRf (Figure 5.6). Between winter 1959 and winter 1961, there appears 5.2 The original study of sheep tooth wear 131

to be coincident peaks in AIRf at all stocking rates during winter of 1960. What might explain the high AIRf in winter of 1960, and the absence of similar peaks in 1959 and 1961? In retrospect, the greatest deficiency of the Arnold et al. (1966) study was the lack of concern for the mineral constituents in sheep diet and fecal material. If most of AIRf were not phytoliths, what was it? Why did they not inspect and describe the composition of the AIRf? As will be shown here, studies of the incidental minerals in sheep feed supplements and in aerosol dust reveal much about the source, movement, distribution, and concentration of mineral particles and mineral species. Despite all this, no comparison was made between the mineral composition of AIRf and local soils or aerosol dust. Soils around Canberra are heavy with clay, hard to work, wet in winter, and dry in summer when vulnerable to wind erosion, and the accession of mineral particles to soils is dominated by eolian processes (McTainsh et al., 1990). Approximately 21% of the land surface of Australia is covered by pedogenic carbonates formed in soils and then either incorporated into regolith or resuspended as windborne sediments. Pedogenic carbonates are particularly abundant in semiarid and arid regions. The carbonate material in eolian parna soils that blanket much of southern New South Wales originates from source areas in southern Australia (Dart et al., 2005),transportedbywindovertheMurray–Darling and Murrumbidgee Basins and deposited as a red-clay mantle (Crocker, 1946;Butler,1956; Butler and Hutton, 1956; Chen, 2001). The calcareous parna soils in southern NSW develop from this dust mantle. On occasion, windstorms fill the sky with red “sand” and after “red rains,” dust flocking equipment (Figure 5.1) is required to remove the dust from harvested wool. Noel Beadle (1948) observed that dust storms increased in frequency and intensity through grazing pressure, when the red earth soil exposed to disturbance by hooves becomes vulnerable to deflation. Costin (Australian Academy of Science, 2006) remarked that in the grazing environment of the southern tablelands of NSW, 70% ground cover is required for effective soil protection, and that once cover is reduced to below 70%, surface processes begin to expand bare areas. In the first years of the 1960s, dust storm activity was high (see later) and airborne dust accession to the soils of the southern tablelands included clay-sized particles of illite and kaolin, but most of the mass of the dust was in the silt-sized fraction (Walker and Costin, 1971). Did any of these minerals or these surface processes contribute to the observed variation in AIRf? It is particularly surprising that the researchers did not examine the AIRf more closely. It would have been very easy to send samples to George Baker, who at the time was describing the mineral particle content in sheep feed supplements and the rumen of sheep kept indoors for experimental purposes. A comparison of ingested mineral particles between these indoor sheep and sheep grazing in outdoor pastures would have been informative and of potential significance to wool producers, as it could have contributed to a better understanding of the role of soil ingestion in tooth wear. Why this was not done is still a great mystery. 132 Soil erosion, soil ingestion, and tooth wear in Australia

5.3 Dust ﬂux and soil ingestion in southeastern Australia

5.3.1 Background

Mineral particles observed in prepared feed (presumably incorported by harvesting local or regional feed crops) carry mineral species that are informative about geographic source and suggest the operation of surface processes that deliver (and delivered) mineral particles into local soils. What do we know about this? Some glimpse of the potential range of interesting soil minerals that can occur in processed sheep feed and the fecal material of caged animals is provided by the Baker et al. (1961) report that examined samples from both untreated fecal material and untreated feed. The study was conducted at the laboratories of CSIRO and School of Agriculture of the University of Melbourne. Baker et al. (1959, 1961) examined phytoliths in processed feed; oaten chaff (Avena sativa L.), Wimmera rye-grass (Lolium rigidum Gaud.), and Lucerne chaff (Medicago sativa L.), and also in rumen contents from caged animals fed the opaline sheaths of oat or lucerne chaff. The mineral particles in untreated samples of these feeds were examined and contrasted with treated samples processed with nitric, perchloric, and hydrochloric acids. The acid-insoluble residue (AIR) was obtained after being washed in water, dried, and ignited over a Meker burner. Not surprisingly, the AIR consisted mostly of dehydrated opal phytoliths. On these treated and dried phytoliths, Moh and Knoop hardness were measured (Baker et al., 1959). Given that the animals were housed indoors, the samples were found to contain relatively few adventitious mineral particles. Quartz, mica, augite, feldspar, and tour- maline mineral particles comprised a minor fraction (2.3%–12.6%) compared to abundant opal phytoliths (87.4%–97.7%). High specific-gravity particulate residue from the ventrum or floor of the rumen of animals fed untreated chaff included particles of these same mineral species plus olivine, zircon, hornblende, volcanic glass, glass microspherules, and opaque black and steel gray magnetic “artificial substances” from the chaff cutter blades, but relatively few opal phytoliths (apparently these were passed intact within plant tissue residues). This, then, is a somewhat more complete inventory of the mineral species in the washed and processed feed. No salts, carbonates, or “parna” clay particles could have been observed by these methods. The presence of ilmenite (crystalline iron titanium oxide) was mentioned, but not counted or measured. In passing, it was observed that calcite phytoliths in lucerne were destroyed by acid preparation (as were steel fragments from the chaff cutter), but not by gut passage. Where do these mineral contaminants in processed feed come from? Microspherules are microscopic beads of glass that form as the heat and energy of impact melts rocks and ejects them out of a crater as a fine spray. This spray may be transported by the atmosphere to eventually fallout as sedimentary deposits. There is literature about microspherules associated with fallout melt ejecta and shocked minerals or impactites. Microspherules can also be associated with basaltic glass, volcanic ash, and gasses inside eruptive volcanic craters, and nuclear weapons testing on the land surface. 5.3 Dust flux and soil ingestion in southeastern Australia 133

In the southern hemisphere, at 30–40 S, the date of the horizon of the first detection of 137Cs in sediment cores is 1955 (Leslie and Hancock, 2008). Radiocaesium is one of the most important artificial radionuclides produced by nuclear fission, and since it was first introduced into the terrestrial environment by nuclear weapons testing, it has been an important tool in the study of erosion rates in Australia (Longmore, 1982; Loughran et al., 1990). Coincidentally, while the dust storm record for Australia begins in the late 1950s for some meteorological stations, most published information about the history of dust storm frequency began later in the 1960s. Additionally, the classic study of sheep tooth wear sometimes cited to support a dominant role for phytolith ingestion (Arnold et al., 1966) was conducted between June 1959 and July 1961 at the Dickson Experimental Station in Canberra on the SE dust path downwind of the nuclear test site at Maralinga. It is a curious coincidence that the most comprehensive long-term study of wool production in Australia did not describe the mineral particle contribution to AIRf (surface soil). It is also an interesting historical coincidence that the much higher- profile experimental study attributing tooth wear in sheep to phytoliths, also reported that phytolith concentrations were very much higher than adventitious minerals in processed sheep feed. These reports were published in Nature at about the same time that radiocesium was entering surface soils for the first time, when microspherules were being detected in washed sheep feed, and the discovery that significant quantities of surface soil were being ingested by sheep. No wonder phytoliths (rather than ingested soil) are more often implicated as the cause of tooth wear. Nobody wanted to think about the implications of other sources of mineral particles in sheep ingesta.

5.3.2 The Dust Storm Index

After Antarctica, Australia is the most arid continent on Earth. Fully 70% of Australia is either arid (MAP<250 mm) or semi-arid (MAP¼250–350 mm). Thus, the study of herbivore tooth wear in arid and semiarid Australia would seem especially pertinent given the geographic association of high faunal hypsodonty with dust storm frequency at the latitude of Australia (and in South America and globally), and the inﬂuence of interannual ENSO and decadal Paciﬁc Ocean climate cycles on the surface conditions that govern erosion. Much of the aerosol dust in the southern hemisphere originates from Australia (120 Tg/yr). The source areas for the aerosol mineral particles in the SE dust path of Australia are the low and arid basins in the center of the continent. In the Australian earth sciences literature, windborne mineral particle behavior is often described in relation to the Dust Storm Index (DSI), a characterization of daily observations made about the visibility of the atmosphere. The expression provides a measure of the frequency and intensity of major dust storms and is used to track historical trends and the geographic pattern of wind erosion across Australia. DSI encompasses observations about three different types of dust events, and by weighting, places emphasis on infrequent severe dust storms while de-emphasizing local events. DSI is presented usually as monthly or annual average DSI for individual stations. While it is possible to talk about the DSI for a particular meteorological station, 134 Soil erosion, soil ingestion, and tooth wear in Australia

isolines contouring DSI values describe the regional or national geography of dust storm frequency and intensity. For students of soil ingestion and tooth wear, a contour map of DSI is, in essence, a “surface” of potential selection pressure. As DSI is not an instrument-based measurement, and does not incorporate dust trap data, we must ask how it relates to mineral particle flux. In a general way, DSI is flux, but because of its weighted emphasis on extreme events, it might not be the best expression for more constant but low-level flux that may prove more meaningful for soil accession, soil load on leaf surfaces, and tooth wear. Because soil ingestion is both direct (off the soil surface) and incidental (via deposition on leaf surfaces), a reconstruction of the dust budget for SE New South Wales during the 1950–1960 period of study might offer an explanation for the observed seasonal pattern of silica or soil ingestion. Published Annual Total Dust Storm Index values for New South Wales are available for 1960 and 1961, but not for 1959 (Cattle et al., 2009). In lieu of month-specific DSI for Canberra (the study site) and Wagga Wagga (the immediately upwind meteorological station) for the study period, I resorted to mean monthly dust storm frequency for the southern region of Eastern Australia over the period 1960–1987 and predicted frequency based on a model of seasonal controls on wind and effective soil moisture (McTainsh et al., 1998). Daily and annual eolian dust deposition rates are highly variable. Deposition rates between 5 and 68 tons/km2/yr were observed between 1987–1999 (years of low total annual DSI) and daily rates between 0.05 and 0.28 t/km2/d in 2001 (a year of very low DSI<20) were measured along the southeast dust path (Cattle et al., 2009). This dust path is the principal transport pathway blowing from the arid exposures of southern South Australia and the Lake Eyre Basin, through western NSW and NW Victoria, and eventually to the E and SE over the Tasman Sea and Southern Ocean (McTainsh et al., 2008; Cattle et al., 2009). Dust deposition rates are probably very much higher during drought years, when DSI is higher (between 50 and 180) such as occurred during the sheep wool production and tooth wear studies of 1959–1961, throughout the prolonged drought that extended from 1959 to 1968, but how much higher is not known.

5.3.3 Aerosol dust composition in southeast Australia

There have been many recent studies of aerosol dust composition in SE Australia, but for the period of the long-term study of sheep soil ingestion and tooth wear and high DSI, we only have the Walker and Costin (1971) description of atmospheric dust accession at Mount Kosciuszko in the Australian alps (1800 m) and at Canberra. Atmospheric moisture arrives over SE Australia from the Paciﬁc, from the NE, sometimes in cyclones. This moisture or water vapor becomes raindrops when it encounters westerly winds blowing ﬁne-grained dust off the Lake Eyre Basin. From there, the winds blow eastward, water vapor droplets form around the dust particles, the mass of air ascends the mountains, cooling, and there the aerosol dust rains out. Their data at Mt Kosciuszko were sampled on November 18, 1968 just after a severe drought and plentiful dust storms, and at Canberra in October 1967 after rainout following a severe dust storm. The clay fraction was removed by centrifuge, the silt fraction (2–31.3 μm) by 5.4 Methods 135

pipette, and the coarse fraction by sieving. The dust at Mt Kosciuszko was a silty clay with 75% of particles ﬁner than 31 μm, with median diameter close to 4 μm. The clay fraction comprised 37% of the mineral content and of this, roughly 80% was illite and kaolin. Curiously, nothing is said about the silt fraction that comprised 41%–43% of the mass. The coarsest particles, sand-sized, were biotite from local granite. Interestingly, the Canberra samples (of most relevance to the sheep tooth wear and soil ingestion study) were collected from rain gauges. These were samples of mineral particle rainout in association with windstorms, just after the strongest dust storms of the 1967–1970 period. Median particle size was 4 μm, and there was no coarser fraction (that is, no local mixing). Particle size analysis of the dust samples showed how important the silt fraction is. They note the similarities in grain size attributes between the dust sample and parna, and mention in passing that any carbonate in their dust samples might have been dissolved away by the processing. As the Canberra dust samples were collected from rainfall caught by rain gauges, they contained no rain-splash off the soil or leaf surface.

5.3.4 ENSO in New South Wales

ENSO contributes substantial variation to rainfall with consequences for rain-fed wheat production in New South Wales where there is a high correlation between annual rainfall and the SOI (Podbury et al., 1998). More specifically, wheat yield is negatively correlated with the SOI of the year previous to planting and positively correlated with the SOI during the crop season (Rimmington and Nicholls, 1993). The planting season for wheat in NSW begins around the first of May, heading begins at the end of August, and harvest begins around the first of October and runs through the end of December. It includes hard wheat, standard white wheat, general purpose wheat, and feed wheat. Assuming the climate conditions influencing wheat production will also influence pasture and forage plant growth, ENSO drought conditions might be assumed to contribute to ingested silica, as grasses have been observed to have higher solid silica concentrations late in the growing season and during dry years. However, although wheat production was reduced 40% during the 1963–1968 drought and the percentage of silicon in wheat husk is closely related to transpired water (Hutton and Norrish, 1974), silicon content shows a poor correlation with grain yield (Schultz and French, 1976).

5.4 Methods

The original PCs and AIRf silica as a percentage of fecal DM were presented in graphical form (Arnold et al., 1966) and were captured using GraphClick v3.0 (Arizona Software, 2008). The original published data were plotted as pseudo-time series at either roughly monthly or two-week sampling intervals. The actual date of each sample is not provided, but a day count can be reconstructed from the published ﬁgures and dates assigned to these. As the data comprise spot samples of fecal material, assuming gut passage time is constant, the irregular interval between sampling episodes does not affect the quantities reported. 136 Soil erosion, soil ingestion, and tooth wear in Australia

To explore the relationship between the observed variables to surface processes and their controls, environmental variables relating broadly to both fluvial and airborne mineral particle flux were used. The triggers and conditions conducive to dust storms include zero leaf area index, zero vegetation height, active surface disturbance, soil particle-size distribution (clay content), effective soil moisture, and deflation thresholds of wind speed and fetch in the dust source area (McTainsh et al., 1998; Leys et al., 2001). The frequency of dust storms is related to these same variables plus antecedent moisture (Yu et al., 1993; McTainsh et al., 1998). All other things being equal, the intensity of dust storms is related to the duration and velocity of peak wind speed. Average monthly and annual dust storm frequency is usually predicted from wind erosivity (a function of wind velocity and wind run or fetch) and effective soil moisture (rainfall minus evaporation). The best predictor of summer dust storm occurrence at Mildura (on the SE dust path) uses monthly rainfall during the preceding autumn in the upwind dust source areas (Yu and Neil, 1994). NSW has two different dust storm seasons: in the northern region encompassing most of NSW (and Queensland), the dust storm season runs from September to January, and in southern NSW (and Victoria), the dust storm season extends from December to March. The northern and southern regions of NSW are separated by a line extending from Broken Hill to Cowra (McTainsh et al., 1998). This line of demarcation also distinguishes the two main dust source areas, the northwestern source region and the southwestern source region (Cattle et al., 2009). To try to address how atmospheric particle flux relates to DSI, average daily dust deposition (t/km2/d) at three sites along the SE dust path (Cattle et al., 2009) was also used in the analysis. The three sites, Hillston, Lake Cargelligo, and Condobolin, are in central NSW from West to East along the Lachlan River. These are sites along the SE dust path where average daily dust deposition was sampled at 10 to 42 day intervals from December 2000 to December 2001, a year of DSI<20 (less than half of the long- term 1960–2006 average of 49). By comparison, during the study of sheep tooth wear, DSI was 103 in 1960 and 56 in 1961. The year 1958 was an exceptionally wet year in SE Australia, as recorded at Merbein, Victoria, with 440 mm MAP, only four

dust-event days, and 24.5 kg/ha of CaCO3 wet-dust deposition. By contrast, the next year, 1959, at the start of the study, was an exceptionally dry year, with 190 mm MAP,

13 dust-event days and 26.8 kg/ha of CaCO3 deposition. While 1960 was wetter (310 mm MAP), there were still many more dust-event days (29), and 41.0 kg/ha of

CaCO3 was deposited by wet processes (Goudie and Middleton, 1992). For local conditions, mean monthly temperature and precipitation for the meteorological station at Canberra during the period of the study (1959–1961) were assigned to each PC and AIRf sample. Total annual DSI for New South Wales for 1960 and 1961 (Cattle et al., 2009), observed and predicted mean monthly dust storm frequencies for the period 1960–1987 (McTainsh et al., 1998), and northern (or NW source region) and southern (or SW source region) NSW average monthly dust storm frequencies (McTainsh et al., 1998) were considered. The data also include mean monthly rainfall for upwind stations at Wagga Wagga and Mildura during the interval of study, along 5.5 Results and discussion of time series analysis 137

Table 5.2 Monthly values of silica ingestion by sheep and earth surface processes along the Southeast Dust Path in New South Wales, Australia

Mean Std Dev Max Min N

PC low density 115.15854 57.972423 278.405 29.785 35 PC medium density 186.85906 110.16978 505.054 56.382 36 PC high density 157.11469 98.197116 469.206 56.382 36 PC very high density 184.55149 82.185274 355.882 37.88 37 AIRf low density 12.240278 3.2507856 19.698 6.786 36 AIRf medium density 10.846556 4.8028701 26.236 3.565 36 AIRf high density 16.162222 13.47236 55.162 3.973 36 AIRf very high density 25.114861 16.62901 66.373 4.759 36 MMT-Canberra 12.651282 5.1944237 21.8 4.9 39 MMP-Canberra 68.564103 49.659257 160 2 39 MMP-Wagga Wagga 39.65641 30.525458 106.7 6.4 39 MMP-Mildura 22.412821 17.276714 59.4 2.3 39 Measured MMDS freq 0.0450154 0.0336615 0.1167 0.0067 39 Predicted MMDS freq 0.047259 0.0287329 0.1042 0.0183 39 SOI monthly 1.9492308 6.6266773 11.055 20.15 39 PDO Index monthly 0.0630769 0.5188406 1.18 0.94 39 MEI monthly 0.233974 0.1486765 0.065 0.511 39 Avg DS freq NNSW 0.0789231 0.0540207 0.171 0.023 39 MMESoilMoist NNSW 1.9905897 0.561414 3.368 1.249 39 MMWindRun NNSW 179.23379 20.04897 203.579 150.237 39 Avg DS freq SNSW 0.0441795 0.0344329 0.117 0.005 39 MMESoilMoist SNSW 2.2256154 0.7130704 3.51 1.17 39 MMWindRun SNSW 161.38836 20.985833 185.573 129.407 39 DailyDustDep WNSW 0.2732353 0.2072288 0.73 0.03 34 DailyDustDep ENSW 0.045641 0.0415993 0.16 0.01 39 AOD LowDSI 2001 0.0526667 0.025975 0.115 0.022 39 AOD HighDSI 2002 0.0874359 0.0667796 0.235 0.022 39

PC, phytolith count; AIRf, acid-insoluble residue from fecal material (% DM); MMT, mean monthly temperature (C); MMP, mean monthly precipitation (mm); Measured MMDS, measured (or observed) monthly dust storm frequency; Predicted MMDS, predicted mean monthly dust storm frequency; SOI, Southern Oscillation Index (monthly); PDO, Paciﬁc Decadal Oscillation Index (monthly); MEI, multivariate ENSO Index (monthly); DS, dust storm; MMESoilMoist, mean monthly effective soil moisture; NNSW, Northern New South Wales; SNSW, Southern New South Wales; MMWindRun, mean monthly wind run (at 2 m); DailyDustDep WNSW, daily dust deposition Western New South Wales; AOD, aerosol optical density; LowDSI, low Dust Storm Index year; HighDSI, high Dust Storm Index year.

with mean monthly effective soil moisture (precipitation minus evaporation) and mean monthly wind run for both southern and northern NSW (Table 5.2).

5.5 Results and discussion of time series analysis

Soil erosion in southeast New South Wales occurs by both wind and rain. Dry surface processes are dominated by wind erosion, and atmospheric dust transport and 138 Soil erosion, soil ingestion, and tooth wear in Australia

deposition. Waterborne surface processes in SE Australia are of two sorts, mineral particle accession to soils through the rainout of atmospheric dust, and mineral particle erosion and transport by rain and running water.

5.5.1 Dry climate processes

Within New South Wales, a gradient of decreasing wind erosion extends from the west to the east up the floodplains of the Darling and Murrumbidgee rivers, and this parallels increasing rainfall. Canberra is partially protected from aerosol dust originating from the west by the Snowy Mountains. Atmospheric dust accession at Canberra estimated by two samples collected in 1967 by rainout into rain gauges ranges from 0.3 kg/ha to 6 kg/ha (Walker and Costin, 1971). Dust storm activity has a long history in this part of Australia. Parna is a term used for the widespread eolian deposits covering the riverine plains of SE Australia, such as in the Mallee and the area around Wagga Wagga. Parna (aboriginal word for dust or dusty surface), the eolian dust deposits covering the Wagga Wagga region are the most common soil parent material. The variable thickness of the parna deposits is consistent with its eolian origin (Summerell et al., 2000; Chen, 2001). The parna- covered surfaces east of Wagga Wagga are the source area of dust transported toward Canberra, a short transport distance (Butler, 1956; Butler and Hutton, 1956). Source areas of the fine-grained material that composes parna were the coastal lowlands and shelf of the Bight of Australia that was extensively exposed during low sea-level stands, and fine-grained alluvial fans in lakes and shallow basins of the Lake Eyre area that are seasonally remobilized by wind erosion (Dare-Edwards, 1984). The isopach distribution pattern of parna indicates it formed sheet deposits by rainout over tall vegetation, the rainfall influenced both the extent of vegetation as well as increasing the rate of atmospheric dust deposition (Summerell et al., 2000). The northern part of New South Wales is directly east of Lake Eyre, the largest source of airborne dust in the southern hemisphere (NASA Earth Observatory, 2005). During the period 1960 to 1965, mean DSI for the New South Wales rangelands was 13.0, and mean rainfall-adjusted DSI was 0.76; both measures quite high for Australia (McTainsch et al., 2008). In general, the period between 1960 and 1963 was one of high DSI nationally (McTainsh et al., 2006) and at Wagga Wagga (McTainsh et al., 1990). Annual DSI values nationally were over 165 in 1960, up to 230 in 1961, and then back down to 180 in 1962. In addition, 1961 was a year of low rainfall, nationally. In New South Wales, DSI values were also high in 1960 and 1961, but unlike the national trend, the DSI index was higher in 1960 (>100) than 1961 (<60) (Cattle et al., 2009). This local trend is consistent with the observed interannual variation in AIRf. However, seasonal dust storm activity is not (Figure 5.7). The long-term average dust storm frequencies for SE Australia reveal a peak season of dust storm activity in summer, between January and March. This contrasts with the peak winter season of ingested soil (AIRf). Peak AIRf occurred between May and October in 1960 (with the highest values between July–September). Dust storms result from the interaction 5.5 Results and discussion of time series analysis 139

Figure 5.7 Dry climate processes and the time series of soil ingestion (AIRf) in sheep in Canberra between June 1959 and July 1961 (from Arnold et al., 1966). (A) AIRf; (B) effective soil moisture; (C) mean monthly wind run; and (D) monthly average dust storm frequency for Southern and Northern New South Wales. 140 Soil erosion, soil ingestion, and tooth wear in Australia

of soil moisture and wind, and dust storm activity does not begin until wind run increases toward the end of the season of lowest effective soil moisture in northern NSW. Peak dust storm activity begins later in southern New South Wales. Here, peak dust storm activity occurs when soil moisture deficit is lowest and winds are still high. The lack of congruence between the summer peak season of dust storms and the winter peak season of soil ingestion suggests that DSI, while indicating something useful and important about local climate, may not be capturing the elements of wind erosion and dust transport that are important to soil load on plants. However, there may be interannual variation in the peak season of dust storms hidden within the annual DSI and perhaps this variation may explain the lack of congruence. If daily or monthly dust storm records for Canberra and Wagga Wagga for 1959, 1960, and 1961 were available, it might be possible to examine for congruence with soil ingestion more appropriately. The question of whether infrequent but intense dust storms or more constant moderate wind erosion contribute most to soil particle flux near the land surface and thereby to ingested soil cannot be answered directly for the period between 1959 and 1961. How- ever, annual time series data for monthly mean Australian arid-zone aerosol optical depth (AOD) between 1997 and 2003 shows that there is interannual variation and higher and more variable AOD between September and January (Campbell and Mitchell, 2005). In addition, there is a lot of variation in the time series data for scattering coefficient (Mm-1) in the period between September 2002 and January 2003, with typical storms (>100 Mm-1) occurring about twice a week (Campbell and Mitchell, 2005). This more comprehensive description of aerosol mineral particle flux indicates that the season of wind erosion is longer. However, the fact remains that the season of highest dust storm activity, AOD, and scattering coefficient does NOT coincide with the season of high AIRf. The meteorological station at Wagga Wagga records more dust storms annually than Canberra. This must reflect the wind barrier represented by the Snowy Mountains, a mountain range west of Canberra that is sufficiently high to intercept most dust clouds as they move to the east. Thus, the long-distance fine-grained contribution to local soils may be less than expected. Alternatively, modern levels of Australian dust flux are not significant for soil load on plants, nor soil ingestion or tooth wear, but rather, sheep themselves are the active agents of erosion in the southern tablelands of NSW. When the levels of AIRf are highest in winter following the seasonal break, effective soil moisture levels are also high in southern NSW (Figure 5.7). This is the green winter season of maximum reproductive effort. AIRf peaks at all levels of grazing intensity and pasture PCs are low or at about their annual mean. This is also the season of lowest monthly average dust storm frequency (Figure 5.7). Long-term mean monthly wind run increases gradually through winter and into spring as soil moisture decreases, and average monthly dust storm frequency gradually increases. The season of highest dust storm frequency is out of phase with the winter peak in AIRf (Figure 5.7). Thus, it is unlikely that, in southern NSW, dust storm frequency contributed to the observed seasonal peak in AIRf. The total thickness of the clay-rich, calcareous, loessic parna deposits of SE Australia is low and deposition rates were very low during the Quaternary, ranging from as low 5.5 Results and discussion of time series analysis 141

as 0.5–0.7 cm/ka in the Holocene to only as high as 1.6–5.0 cm/kyr in the late Pleistocene in the Wagga Wagga region (Chen et al., 2002). These rates are lower than almost all major continental dust accumulation areas in the world (4.2–6.9 cm/kyr), assuming an average particle density of 2.6 (Pye, 1987). Mean annual dust deposition rates in central and western New South Wales range from 31.4 t/km2 to 43.8 t/km2 (McTainsh and Lynch, 1996).

5.5.2 Wet climate processes

At Canberra, during the interval of the study (1959–1961), mean annual temperature varied from 12.41 C to 12.93 C and mean annual precipitation from 774 mm to 892 mm. Monthly precipitation was bimodal, with a winter peak (MMP>100 mm) that varies in onset (November in 1962–1963, October in 1959–1960, and February in 1958–1959) and duration. There is a second brief mode of higher rainfall (MMP>100 mm) around June–July. During the study, monthly precipitation was highest during the winter season of peak AIRf all along the SE dust path between Mildura and Canberra. Interestingly, in 2001 when daily dust deposition was measured along the SE dust path, average daily dust deposition also peaked in winter (Figure 5.8). Wet deposition processes dominate the eolian contribution to soils in Canberra. Atmospheric moisture transported inland over southern NSW from off the Pacific meets the winds of the SE dust path, and windblown dust is rained out. Average daily wet process dust deposition reaches levels up to 0.7 t/km2/d (Figure 5.8), but whether this dust deposition by rains contributes to peak AIRf is not known. The upper Murrumbidgee River drains a basin that includes the tablelands around Canberra (500 m elv.) that are predominantly used for grazing. After headwater streams coalesce into a main channel, the river flows across the tablelands, and thenturnswestwardtoWaggaWagga(180m.a.s.l.).Withregardtosuspended sediment yield for the Murrumbidgee River, Olive et al. (1994) present data for the period 1989 to 1992 along with annual sediment budgets. Annual sediment loads are dominated by flood sediment transport, most generated in areas drained by tributaries above Wagga Wagga. All sediment sampled in the river system had measurable 137Cs, suggesting topsoil sources. For sampled areas of around 10 km2, mean annual sediment yield for the southern uplands around Canberra varies between 10 t/yr and 100 t/yr (Wasson, 1994). These sediment yields for the Murrumbidgee River draining the Snowy Mountains and southern tablelands are very low, consistent with the general pattern for Australian rivers. They are also low by comparison with tectonically active mountainous areas of the world with similar precipitation (500–1500 mm MAP).

5.5.3 Fluvial-eolian interactions

Despite the fact that Australia is the driest and ﬂattest continent, and has no signiﬁcant internal tectonism or volcanism, it manages to suffer through dust storms as a result 142 Soil erosion, soil ingestion, and tooth wear in Australia

Figure 5.8 Wet climate processes and the time series of soil ingestion (AIRf) in sheep in Canberra between June 1959 and July 1961. (A) AIRf; (B) mean monthly precipitation at three meteorological stations along the southeast Dust Path from west to east (Mildura, Wagga Wagga, and Canberra); (C) average daily dust deposition at two sites west and east along the Lachlan River (Hillston and Condobolin), parallel to the southeast dust path.

of fluvial-eolian interaction. This is the interaction that concentrates what little sediment is available and blows it all around the wheat–sheep biozone of the Murray–Darling Basin in New South Wales, where there were once aboriginals and are now sheep to record its effects in their tooth wear. Seasonal and interannual ENSO cycles bring the rains and the winds in combinations that give central Australia its reputation for dustiness. Since the time of the first introduction of sheep ranching in Australia, stock grazing is estimated to have increased the sediment flux in the upper Murrumbidgee River Basin of New South Wales by a factor of more than 150, principally through accelerated gully 5.5 Results and discussion of time series analysis 143

Table 5.3 137Cs soil loss rates for Southeast Australia and the North Island of New Zealand

137Cs soil loss rate (t/ha/yr)

Wagga Wagga, NSW (35.117 S; 147.35 E) cultivated bare soil 2.0 to 59.4 cropped 0.2 to 2.9 grazing lands 0.1 to 0.3 lightly grazed pasture 0.01 to 0.02 Cowra, NSW (33.833 S; 148.683 E) cultivated bare soil 31.3 cropped 0.1 to 11.9 grazing lands 0.03 to 1.3 lightly grazed pasture 0.0 to 0.1 Ginninderra, ACT (35.183 S; 149.116 E) cultivated bare soil 44.0 Gunnedah, NSW (31 S; 150.266 E) cultivated bare soil 7.0 to 87.0 cropped 0.6 to 9.6 grazing lands 1.1 to 4.0 lightly grazed pasture 0.0 to 1.1 Wellington, NSW (32.566 S; 148.95 E) cropped 0.0 to 1.7 grazing lands 0.84 NSW, Australia1, 2 cultivated bare soil 2 to 87 grazing lands 0.03 to 4 North Island, New Zealand3 Manawatu plain 11 to 14 Ohakune 80 to 142

1 Loughran et al.,1990. 2 Loughran et al., 1993. 3 Basher, 2000. erosion. The effects of cultivation and grazing can be seen in a comparison of soil loss rates for different parts of southeast Australia (Table 5.3). Neil and Yu (1991) provide a rainfall erosion index for the southern tablelands for each year during the period 1890–1990 and show a high erosion index during the interval of the study 1958–1961, especially for 1958 and 1960. Following the introduction of sheep and the transformation of the landscape to grazing agroecosystems, sediment flux in the southern tablelands became dominated by channel erosion (Wasson et al., 1998). Prior to European settlement, sediment flux out of the Murrumbidgee–Darling River Basin is estimated to have been much lower (about 2400 t/yr). With widespread sheep ranching, sediment flux attained levels of about 480 000 t/yr. Since the time gully networks matured to maximum extension in the headwaters, sediment yield has subsequently declined to about 250 000 t/yr. Gully erosion contributes directly to fluvial-eolian interaction. 144 Soil erosion, soil ingestion, and tooth wear in Australia

The importance of fluvial-eolian interaction in the dust storm source areas of central Australia is best illustrated in the Lake Eyre Basin, the principal source region for dust blowing along the SE dust path over the Murray–Darling Basin. The dust eventually is blown across the Great Dividing Range, passes over Sydney, and finally out over the Tasman Sea and beyond to the snowfields of the alps of the South Island of New Zealand. The Lake Eyre Basin receives internal drainage from rains that seasonally leave a fresh surface of suspended sediment on the alluvial flats along the lower courses of the streams that feed the lakes. With the dry season, accumulated lake water evaporates and the streams dry up, and with increasing wind run, the fresh alluvium, salt, and other evaporites are deflated and entrained into the SE dust path. It is a beautiful mechanism, but has made no known contribution to tooth wear in modern sheep, although perhaps in periods in the past of less benign climate, some role in aboriginal tooth wear (see later).

5.6 A more complex etiology?

Associated with the intensiﬁcation of production systems, interest in the nutrition of grazing livestock extended to trace elements (Masters et al., 1999). Geophagia from cobalt deﬁciency is one concern (Bourke, 1998; McGreevy et al., 2001). The prevalence of the “staggers” form of Phalaris aquatica poisoning in livestock depends on the total amount and availability of soil cobalt, which depends on the cobalt status of the soil parent material (Bourke, 1998). Phalaris-pasture plant cobalt levels are low year- round, so livestock supplement their cobalt intake by ingesting soil. Pasture plant cobalt levels are very low from June to September, the period of occurrence of Phalaris staggers on farms. This is the season of highest soil ingestion.

5.7 Human tooth size and molar wear

Tooth size variation in modern humans has been explained in relation to dietary practice (Brace 1980, 1995) and attrition or tooth wear (Kieser, 1990). The largest teeth seem to be associated with heterogeneous diets involving little food preparation, and in primitive cultures, tooth surfaces are often ﬂattened by wear (for example, Kieser et al., 2001a, b; Eshed et al., 2006). Although diverse methods of estimating, measuring, and comparing tooth wear rates have been proposed (Molnar et al., 1983; Smith, 1984; Johansson et al., 1993; Miles, 2001; Mays, 2002; Bermúdez de Castro et al., 2003), systematic comparisons of tooth wear rates in modern humans from different geographies have not been attempted, even to test potentially more widely applicable explanations. In Australia, as well as North America and Sub-Saharan Africa, the largest teeth among modern humans are found in populations inhabiting the most arid parts of those continents. People from the Great Basin have the largest teeth among native Americans. The Great Basin sample, measured by Hanihara and Ishida (2005), came from the arid 5.7 Human tooth size and molar wear 145

and windy rain-shadow of the volcanic Cascade Range in Washington and Oregon and the arid states of Utah, Colorado, Wyoming, and Nevada in the Western Interior. In Sub-Saharan Africa, populations from Tanzania and Kenya in the volcanic East African Rift System have the largest teeth. The Tanzanian sample comes from the Loe, Haya Tribe and the Kenyan sample from the Ngorongoro, the Turkana, Kikuyu, and Kaurite to Fort Hall. Why the largest teeth in these continents are found in arid areas, downwind from dust source areas, or downwind from active volcanoes (Tegen et al., 2002) may be mere coincidence, or may reflect the role of erodible sediment supply and earth surface processes in the directional evolution (or maintenance in the case of stabilizing selection) of the volume of tooth mineral substance, expressed as tooth size in humans. In high-wear environments, the largest tooth crowns in the dentition predictably have the greatest functional longevity (see Figure 6.7, for an example among island goats). In a sample of the living howling monkey Alouatta palliata from Omotepe Island in Lake Nicaragua, the largest crowns in the dentition, M1 and m3, are the last crowns to wear away. While M1 is among the first permanent teeth to erupt in the upper dentition, it is the largest tooth in the tooth row, and is the last tooth position to wear out with advancing dental senescence. The unusually high tooth wear among howlers on Omotepe has been attributed to the eruption of Volcán Concepción and deposition of volcanic ash over leaf surfaces in the forest canopy (Smith et al., 1977). The sample of Alouatta was obtained between 1962 and 1968, and in the ten-year period immediately preceding the collecting, periods of eruption activity were recorded from July 1951 to May 1955, from March 27, 1957 to July 1957, from November 28, 1961 to December 1961, during an eruption in June 1962, and an interval beginning on May 9, 1963. The June 1962 eruption VEI (Volcanic Explosivity Index)¼?2, and the July 1951 to May 1955 and March to July 1957 eruption periods included large explosive eruptions of VEI¼2 that damaged the surrounding land. On Omotepe, the prevailing winds are northeasterly, and ash is deposited on the southwest side of Volcán Concepción, where their accumulation over time has created the plain of Moyogalpa. As is typical of environmental causation, some Ateles in the same sample also showed excessive tooth wear. With regard to evolutionary trends in human tooth size, Kieser (1990) reviews selective models for both negative and positive trends, including reduced or relaxed selective pressure through food processing as an explanation for evolutionary tooth size reduction in Homo sapiens and the acceleration of tooth size reduction in the post- Pleistocene (Brace et al., 1987). With regard to positive odontometric trends in some modern human populations, there is little consensus. If there is a relationship between human tooth size, aridity, proximity to sources of pyroclastic sediment accumulations, and active surface processes delivering soil into the diet, one prediction might be that the largest teeth among modern humans inhabiting Oceania should be found closest to the Andesite Line. Brace and Hinton (1981) found the smallest tooth sizes in inhabitants at the eastern and western extremes of Oceania, and the largest teeth in Australian aboriginals and highlanders of eastern New Guinea. Across Oceania, most of the Pacific Island populations with total tooth size greater than 146 Soil erosion, soil ingestion, and tooth wear in Australia

Table 5.4 Tooth size in modern human populations (Homo sapiens) of Oceania with total tooth size (TS) >1300 mm2 (from Brace and Hinton, 1981) in relation to the Andesite Line of Marshall (1912)

Group TS >1300 mm2 Andesite Line

Borneo Neolithic 1312 No (far to the West) Bougainville Nasioi 1359 Yes (on it) Fiji 1338 Yes (on it) Guam1 1309 No Flores Mesolithic2 1358 Sunda arc Malay Peninsula Mesolithic 1370 No New Britain (Rabaul) 1334 Yes (on it) New Guinea, Eastern Highlands (Lufa, Goroka) 1395 Yes (just Southwest of it) New Guinea, Sepik River 1321 Yes (just South of it) New Hebrides 1328 Yes (on it) Samoa3 1311 Hot-spot (East) Tonga 1371 Yes (on it)

1 Guam is on the Pacific Plate, in the Marianas, an intra-ocean volcanic island arc oriented parallel to the Marianas Trench at the convergence of the Pacific Plate and Philippine Sea Plate. 2 Flores is in the lesser Sundas, an archipelago of the volcanic Sunda Arc where the Indo- Australian plate subducts northward beneath the Eurasian plate. 3 Samoa is on the Pacific Plate, just north of the Tonga Arc and trench, on a plume generating a chain of shield volcanoes and seamounts aligned along a hot-spot lineament (Hart et al., 2004).

1300 mm2 inhabit islands along the Andesite Line (Table 5.4), the line of suture separating regions wherein peri-continental andesitic volcanism occurs from oceanic regions where basaltic volcanism occurs. Most of the sea-floor of the Pacific is part of the Pacific Plate. The continent of - Australia and a large part of the South Pacific and Indian Ocean are part of the Indo- Australian Plate. The crust of the Pacific Plate and its low oceanic islands is basaltic, the product of the sea-floor spreading. The volcanics on the continental islands of Indo- Australia are andesitic, the product of subduction where the two plates meet along the northern boundary between the Indo-Australian and Pacific Plates. The line of volcanic island arcs occurring where the marine Pacific Plate subducts beneath the continental Indo-Australian Plate has been termed the “Andesite Line” (Marshall, 1911, 1912). In Oceania, the area around the Andesite Line is also called the Melanesian Borderlands, an area of active tectonism and explosive ash-rich volcanism. The original populations of large-tooth humans in Australia, New Guinea, and adjacent islands in Melanesia such as Bougainville, New Britain, Rabaul, and New Hebrides, are thought to have inhabited the area since around the late Pleistocene (Stone and Cupper, 2003). The North Island of New Zealand is on the Andesite Line. Prior to AD 1500, early Maori settlers showed little tooth wear. After about AD 1500, tooth wear became pronounced. The acceleration of tooth wear has been associated with a diet shift away from large birds (the now-extinct Moas) and sea mammals toward more abrasive sweet potato (kumara) and fern root, along with marine shellfish (Houghton, 1996). Initial Polynesian settlement (560 BP), AD 1250–1300, or AD 1280 (Wilmshurst et al., 2008), 5.7 Human tooth size and molar wear 147

was accompanied by little tooth wear. However, two different sorts of vegetation change followed Polynesian settlement, a rise in bracken and charcoal by AD 1350 and a decline in tall trees around AD 1500. In addition, eruptions of Taranaki and the Tongariro center were frequent throughout the period of Polynesian settlement. In particular, the Kaharoa Tephra (600 BP) is a datum used for human-induced burning and deforestation throughout the northern and eastern North Island. Thus, human plant cultivation, root crop harvesting, and soil disturbance (like grazing behavior) are all surface processes, and part of the complex relationship between soil ingestion and tooth wear. Aboriginal diets in Australia are heterogeneous, and the digging stick is a central piece of the aboriginal tool kit, as are big teeth. Hanihara and Ishida (2005) compiled mesiodistal and buccolingual crown diam- eters for 72 major human populations and seven geographic groups. Confirming the results of Harris and Lease (2005), they found that aboriginals from the Murray River Basin in SE Australia have the largest teeth. The Last Glacial Age inhabitants of the Murray River Basin had teeth as large as those of Homo erectus and the early Neanderthals (Brace, 1980). The Murray River Basin samples come from all along the river valley from above the vicinity of Mildura to its mouth near Adelaide. Aboriginal tooth size varies within Australia. There is a geographic gradient or cline in tooth size along the east coast, with the smallest occurring in northern Queensland, and the largest in southeast Australia. The largest tooth size is found in populations from the Murray River Basin, and among the populations along the Murray River (Figure 5.9); the largest teeth are found along the central Murray, and the smallest at the mouth (Brace, 1980). The population from Coorong has the smallest total tooth size, followed in order by the sample from Swanport, the middle Murray samples of Ren- mark and Mildura, and the largest total tooth size is found in the Cohuna sample (Table 5.5). What explains the cline of increasing aboriginal tooth size south along the east coast and the cline of increasing tooth size from west to east along the Murray River? For a relationship between large tooth size (large enamel volume) and the intensity of surface processes and soil ingestion to make sense evolutionarily, we ought to find a relationship between the frequency of atmospheric dust events and both tooth size and tooth wear among aboriginals. Dust storm activity declines progressively northward from peak activity in south and southeastern Australia, to the lowest activity in northern Queensland. This south to north trend of decreasing dust storm activity with lower latitude parallels the latitudinal decrease in total tooth volume among aboriginals. A similar trend of increasing tooth size and dust storm activity is found along the Murray River between its mouth and upper course (Table 5.5; Figure 5.10). The middle and upper course of the Murray River runs parallel to the southeast dust path and the river system interacts with the eolian Mallee (Pendergast et al., 2009). The westernmost dust source areas are the seasonally dry lakes of the Lake Eyre Basin and fluvial-eolian interaction in the Menindee Lakes (Hesse and McTainsh, 2003; Pardoe, 148 Soil erosion, soil ingestion, and tooth wear in Australia

Figure 5.9 Geography of samples used in the comparison of aboriginal total tooth size and molar wear along the Murray River in southeast Australia.

2003). Along this dust path, entrainment of surface mineral particles by wind begins in the west and increases eastward, and sediment grain sizes decrease eastward (Cattle et al., 2009). Tooth wear gradients (the difference between the wear stages of the ﬁrst and third molars) vary in aboriginal populations from SE Australia (Molnar et al., 1989). The lowest tooth wear rates are found near the mouth of the Murray River, and the highest are found along the central Murray. Tooth wear gradients (and relative wear rates) in both the mandibular and maxillary molar rows increase from west to east along the Murray River between Swanport and Euston (Figure 5.11). This geographic gradient of increasing tooth wear from west to east coincides with the gradient of increasing atmospheric dust storm intensities (Table 5.5). Both Mildura and Euston are situated along the southeast dust path, and both have the highest tooth wear and modern dust storm activity. When these aboriginal populations lived, was dust storm activity greater than today? The robust human remains from Kow Swamp (i.e., Cohuna) may be Last Glacial 5.7 Human tooth size and molar wear 149

Table 5.5 Tooth size in Australian aboriginal samples (from Brace, 1980) in relation to modern dust records (from McTainsh and Pitblado, 1987; McTainsh et al., 1990)

Total Meteorological Dust Dust Dust Sample/location tooth size station events1 storms2 haze3 DSI4

Darwin 1396 Darwin Airport 0000 014015 Cape York [N Queensland] 1296 Cape York Post 0000 Office 027004 Cairns [NE Queensland] 1272 Cairns Aero 031011 0.5–1.0 0 0.5 0 Brisbane [SE Queensland] 1332 Brisbane Airport 2–50 3 2 040842 Broadbeach [SE Queensland] 1530 0.5–1.0 0 0.5 1 Sydney 1351 Sydney Airport 1–20 1 0 066037 Adelaide 1442 Adelaide Airport 0001 023034 Swanport (Lower Murray) 1464 Murray Bridge 00[<10] 0 na [South Australia] 024521 Kow Swamp/Cohuna 1581–1588 Euston Post Office 0.5–1.0 0.5 2–55 (Upper Murray) [NSW] 049013 [30–50] Murray Basin (Middle 1486 Renmark AERO 0.5–1.0 0.5 1–23 Murray A–Renmark) 024048 [>50] Murray Basin (Middle 1486 Mildura Airport or >5 2 [74] 5 5 Murray B–Mildura) [Victoria] Post Office 076077 Coorong [South Australia] 1422 Meningie 024518 0 0 0 na

1 Mean annual frequency of dust events (any event involving dust entrainment, transport, and deposition by eolian processes). 2 Mean annual frequency of dust storms (turbulent winds raise large quantities of dust and visibility reduced to less than 1000 m) and total dust storms 1960–1984 (from McTainsh et al., 1990). 3 Mean annual frequency of dust haze (dust particles in suspended transport raised from the surface by a prior dust storm). 4 Mean Dust Storm Index 1992–2005 (from McTainsh et al., 1990).

Maximum age or somewhat younger, a time when lake levels fell with growing aridity and dry lake shoreline deposits were deflated by wind (Stone and Cupper, 2003). During this period, rates of dust entrainment, transport, and deposition were significantly higher than at present (McTainsh, 1989; Hesse and McTainsh, 2003), especially in the Lake Eyre Basin where internal drainage brings renewed supplies of fine sediment into the dust source area. At the same time, ocean sediments of the Tasman Sea, and the Pacific and Indian Oceans received massive amounts of eolian sediment (Hesse, 1994, 1997), and dust accessions to some Australian soils were also significant (Hesse and McTainsh, 2003). Using the signature of eolian deposits from airborne gamma ray survey data, dust mantles of various lithologies can be mapped (Figure 5.12). A map of modern salt deposits is superimposed on a DEM (Digital Elevation Model) in relation to their source paleolake Bungunnia (Bierwirth and Brodie, 2008). The salt appears to deposit in 150 Soil erosion, soil ingestion, and tooth wear in Australia

2 Dust Storm Index

0 1200 1300 1400 1500 1600 Total tooth size (mm2)

Figure 5.10 Bivariate plot of total tooth size (mm2) in aboriginal samples from eastern Australia (from Brace, 1980) in relation to mean Dust Storm Index for the period 1992–2005 (McTainsh et al., 1990).

relation to topography like other eolian material, such as parna. Where high elevations are the dominant sites of these deposits, thicker deposits are found on windward slopes and thinner deposits on leeward slopes of ridges (Summerell et al., 2000).

5.8 Conclusions

Studies of sheep tooth wear at the Dickson Experimental Station in the Australian Capital Territory , southeastern NSW provide a gateway to understanding the role of dry climate surface processes in soil ingestion and tooth wear. The most signiﬁcant result of these studies are that winter peak silica ingestion (as measured by the AIRf) is not coincident with the autumn season of highest plant silica (phytolith) concentration. The number of animals grazing in pasture explains most of the seasonal variation in silica ingestion, as at higher population densities, plant consumption decreases but soil ingestion increases. Coincident with the annual reproductive and pasture cycles, peak soil ingestion occurs in winter when ewes are pregnant and lactating following the seasonal break. Available measures of tooth wear are consistent with seasonal patterns of silica ingestion and not with plant silica abundance. Earth surface processes were examined for temporal and geographic coincidence with silica ingestion in sheep. Dust storm frequency and intensity reﬂect effective soil moisture and wind run (fetch). Dust storm frequency varies seasonally, but the season of highest dust storm activity is not coincident with high silica ingestion. 5.8 Conclusions 151

0.8 0.8

Males - Mandible Males - Maxilla 0.6 0.6

0.4 0.4

Wear score M1 0.2 M2 0.2 M3

0 0 Swanport Renmark - Rufus River- Euston Swanport Renmark - Rufus River- Euston Lindsay Creek Mildura Lindsay Creek Mildura

Darling River

Murray River Renmark - Rufus River- Lindsay Creek Mildura

Euston Adelaide

Swanport Tooth wear

West East

Figure 5.11 Molar tooth wear in male aboriginals from the Murray River in southeast Australia (from Molnar et al., 1989). (©1989 Wiley-Liss, Inc., A Wiley Company, with permission from John Wiley and Sons.) Top, mandibular and maxillary molar tooth wear in aboriginal samples arranged from left (west) to right (east); middle (arrows), the difference between wear scores for maxillary M1 and M3; and bottom, for mandibular m1 and m3 in aboriginal samples from west to east along the Murray River (see Figure 5.10).

Dry atmospheric winds blow from west to east along the southeast dust pathway and across the Murray–Darling Basin. Dust is entrained off dry lakes and mostly fresh alluvium in the streams feeding the Lake Eyre Basin. Dry deposition decreases from west to east along the Murrumbidgee River across southern NSW. Dust accession to soils occurs by rainout in the uplands approaching Canberra and the Snowy Moun- tains. Rainout results from the interaction of dust particles in dry atmosphere rising over the mountains meeting moisture-laden air moving inland from the northeast off the Paciﬁc. Surface soils in Canberra show a distinctive eolian signature but are not formed on a parna mantle. Salt attached to clay aggregates and carbonate are additional eolian inputs to surface soils that do not show up in AIRf. Mean monthly rainfall is highest during winter all along the dust pathway across southern NSW, and winter is the season of highest dust accession to soil through wet deposition. Thus, if surface processes contribute to sheep soil ingestion, it is through the mechanism of wet deposition in winter, not dry deposition. Among modern humans, Australian aboriginals have the largest teeth. Within Australia, with the exception of Broadbeach, the largest teeth among aboriginals are 152 Soil erosion, soil ingestion, and tooth wear in Australia

Figure 5.12 Airborne gamma ray survey map of the distribution of the eolian dust mantle of evaporitic salt deposits in the Murray River hydrographic basin superimposed on a DEM in relation to their source, the paleolake (Bierwirth and Brodie, 2008, with permission from Elsevier). The salt deposits appear in relation to topography like other eolian material, such as the similarly widespread parna. Where high elevations, such as the Snowy Mountains, are the dominant sites of deposition, thicker deposits are found on windward slopes (Summerell et al., 2000).

found in populations in the Murray–Darling Basin. Molar tooth wear among aboriginals along the Murray River between Swanport and Euston (Kow Swamp, Cohuna) increases upstream and from west to east. The contribution of aerosol dust to aboriginal tooth wear, whether through dry or wet deposition, is not known. The importance of fluvial-eolian interaction in the dust storm source areas of central Australia is best illustrated in the Lake Eyre Basin, the principal source region for dust blowing along the SE dust path over the Murray–Darling Basin. The Lake Eyre Basin receives internal drainage from rains that seasonally leave a fresh surface of suspended sediment on the alluvial flats along the lower courses of the streams that feed the lakes. With the dry season, accumulated lake water evaporates and the streams dry up, and with increasing wind run, the fresh alluvium, salt, and other evaporites are deflated and entrained into the SE dust path. It is a beautiful mechanism that may account for some variation in sheep and aboriginal tooth wear. However, as I have shown, any resulting tooth wear is hardly detectable in sheep in Canberra, but appears to have had 5.8 Conclusions 153

perhaps a detectable evolutionary significance among aboriginals. Beautiful mechanism, slight evolutionary impact, what does this mean? Sediment isopachs are very thin over much of Australia, but especially in the southeast. Thus, the system is sediment starved. There just does not seem to be thick accumulations of readily eroded sediment exposed at the surface. Possibly, during deglaciation, erosion in the mountains brought more mineral particles into the dust source areas, this fresh input became available to the SE dust path, and it contributed to aboriginal tooth wear. Thereafter, into the Holocene, the amount of surface sediment available to this routing system diminished, and today, direct disturbance of the soil surface is more significant to sheep tooth wear than eolian processes. While suggestive, evidence for the role of dry climate surface processes in soil ingestion and tooth wear in Australian sheep and aboriginals is only circumstantial. More plausible contributors are behaviors such as grazing at high densities (for sheep) and food procurement (for aboriginals). In deeper time, the low prevalence of hypsodonty among Australian native marsupial herbivores is another apparent peculiarity for such an arid continent at southern horse latitudes with high climate variability. Australia has well-known sediment routing systems but is a stable landmass with little tectonism or volcanism, and as such, is sediment starved. For example, andisols (volcanic ash soils) cover only 85 km2 of the land surface and comprise 0.001% of Australian soils, whereas they cover 32 100 km2 or 12.5% of New Zealand soils (Lowe and Palmer, 2005). This is reflected in the uniformly low erosion rates in Australia (<4.1 t/ha/yr), which are much lower than the volcanic North Island of New Zealand (11 to >89 t/ha/yr) or volcanic highland Ethiopia (16–300 t/ha/yr). Models for the evolution of hypsodonty that evoke aridity and climate variability alone are deficient, and must combine sediment availability with active surface processes and routing systems that deliver erodible sediment into and through the environment. 6 Crown height and tooth wear on islands

6.1 Why islands?

As is well known, evolutionary rates in mammals are higher on islands than continents (Millien, 2006). This is the consequence of the founder effect following the introduction of a small number of colonists and genetic drift subsequent to release from predator pressure. As the focus of evolutionary study, islands present relatively stable environments buffered by the surrounding sea, and more simpliﬁed ecosystems that are easily characterized. Given their small size and the small size of their mammal populations, mortality is unusually signiﬁcant demographically and genetically. Finally, because of their small size, the geographic scale of agency and target population match, which is another way of saying that island mammals have no escape. As we shall see, islands in the Mediterranean have remarkable fossil records that document many examples of the independent evolution of tooth crown shape in parallel ways. Given what we know about the geographic distribution of hypsodont mammals globally, Mediterranean islands with relevant fossil records occur at interesting latitudes: Mallorca, 39 N; Crete, 35–35.5 N; Cape Gargano, 41.82 N; Sardinia, 39–41 N; Ibiza, 38.91 N; and Maremma, 43.05 N. That is, they occur within the latitudinal band of the North latitude peak in the prevalence of hypsodonty (see Chapter 3).

6.2 Crown height evolution on Mediterranean islands

Myotragus (Caprinae or Rupricaprinae, Bovidae) and Vicugna (Camelidae) have long been considered the only examples of Artiodactyla to have evolved ever-growing teeth (Miller, 1924). Myotragus from the Balearic archipelago in the western Mediterranean (Alcover et al., 1999) and Vicugna in the altiplano of the Central Andes (Koford, 1957) are very different animals from very different parts of the world. Myotragus evolved large ever-growing central incisors by a process involving progressive loss of lateral incisors and an increase in the size and height of the central incisor crown (Alcover et al., 1999). Eventually this process resulted in the evolutionary loss of the tooth root of the central incisor and the acquisition of an ever-growing mechanism sustaining tooth formation throughout the animal’s life. Vicugna presumably evolved ever-growing incisors through a process of ontogenetic delay in the onset of root formation that

154 6.2 Crown height evolution on Mediterranean islands 155

resulted in a progressive increase in crown height and the eventual acquisition of an ever-growing mechanism without concomitant loss of the lateral incisors. Were Vicugna and Myotragus the only examples of the evolution of ever- growing teeth in Artiodactyla, they would be mere coincidence. But another artiodactyl Maremmia (?Alcelaphinae, Bovidae) also evolved ever-growing incisors more in the pattern of Vicugna. Maremmia is a second example of the evolution of ever-growing teeth in an artiodactyl from a Mediterranean island (Hürzeler, 1983). The ever-growing incisors of Mediterranean Maremmia and Myotragus suggest a context of adaptation to island life. That both the incisors and cheek teeth in Myotragus and Marremia are exceptionally high-crowned implies that tooth abrasion may not have been a simple correlate of specialized food acquisition behavior (as has been argued for Myotragus), but was likely accompanied by mineral particle ingestion. Further, the parallel evolution of high-crowned teeth and thick enamel among other mammals from the same and other Mediterranean islands, suggest the phenomenon may be less a peculiarity of artiodactyl adaptation, and rather the consequence of a more general problem in the adaptation to life on Mediterranean islands. Increased molar hypsodonty and thick molar enamel are common features of Mediterraneanislandherbivores(VanderMade,2008). Through the late Neogene and Quaternary, at least six insular faunas in the Mediterranean document conspicuous evolution of tooth structures useful for resisting abrasive wear (Mallorca, Maremma or Tuscany, Sardinia, Crete, Ibiza, and Gargano). Each island (or paleoisland) has a distinct faunal and environmental history (Moyà-Solà et al., 1999; Marra, 2005;Boveretal.,2008;Masinietal.,2008), and their herbivore taxa are phylogenetically distinct, vary widely in body size, and in geographic isolation appear to have evolved peculiar but parallel specializations for island life (Van der Geer et al., 2010). As is true for faunas from small islands everywhere, the faunal history of Mediterranean islands is not simple, nor is it complete (Sondaar and Van der Geer, 2005). The available evidence indicates these islands and their faunas were environ- mentally fragile and labile because of sea-level ﬂuctuations, alternating humid and dry climate cycles, and ultimately human activity (Sondaar and Van der Geer, 2005). In addition, like the altiplano habitat of the Vicugna in orographically insular altiplano of southern Peru, Bolivia, and NW Argentina, the Mediterranean is a volcanic province and was so in the late Neogene and into the Pleistocene (Savelli, 2002), at the time most of the islands were colonized and their insular faunas evolved their morphological peculiarities. Unfortunately, much of the sediment record and geologic history of these Mediterranean islands has been removed by subsequent erosion. The taxonomic heterogeneity and unique evolutionary and environmental histories of Mediterranean islands and their faunas have conspired to generate surprisingly little interest or search for a unifying explanation for the parallel evolution of morphological contrivances to resist abrasive tooth wear. In light of the vagaries of the fossil record, this is entirely understandable. However, as independent tests of the generality of the 156 Crown height and tooth wear on islands

proposition that earth surface processes underlay many if not most examples of increasing crown height in South American mammals, Mediterranean islands provide diverse examples of how such interaction might and might not be preserved by the rock and fossil record. It may be that a suitable environmental context for the evolutionary history for Mediterranean island life may have to be sought in the study of recovered cores of sea-ﬂoor sediments.

6.2.1 Mallorca

Myotragus provides one of the best-known examples of an insular lineage characterized by the progressive evolution of increasingly high-crowned incisors (Bover and Alcover, 1999). Myotragus balearicus Bate, 1909 is a fossil dwarf bovid endemic to the Gymnesic Islands (Mallorca, Menorca, and surrounding islets in the Western Mediterra- nean Sea). While the phylogenetic affinities of Myotragus are somewhat uncertain, recent analysis of mitochondrial cytochrome b points to phylogenetic affinity with Ovis (Lalueza-Fox et al., 2002, 2005). The caprine genus Myotragus includes five chronospecies from the Pliocene, Pleistocene, and Holocene on the island of Mallorca (Bover et al., 2008). Myotragus lived in Mallorca from about five million years ago (Köhler and Moyà-Solà, 2004)to>9 Kyr as subfossils (Lalueza-Fox et al., 2002), and became extinct more than 4000 years ago following the first human occupation of the island (Burleigh and Clutton-Brock, 1980; Bover and Alcover, 1999, 2003; Ramis and Bover, 2001). Myotragus balearicus is the smallest member of the Caprinae by shoulder height (25–45 cm) with body mass estimates of up to 60 kg and with late glacial and Holocene individuals between 33 and 46 kg body mass (Köhler, 2010). The robust postcranium of Myotragus balearicus had widely separated limbs (wide stance!) with shortened and solidly fused metacarpus and metatarsus, toes tightly bound together by ligaments, and broadened hooves adapted to climbing steep slopes of talus and loose scree (Andrews, 1915; Köhler and Moyà-Solà, 2001; Fornós et al., 2002). Myotragus evolved large ever-growing central incisors by a process involving progressive loss of lateral incisors and an increase in the size and height of the central incisor (Alcover et al., 1999; Bover and Alcover, 1999). Eventually this process resulted in the evolutionary loss of the tooth root of the central incisor and the acquisition of an ever- growing mechanism. Myotragus balearicus displays a single, enlarged, monophyodont incisor in each dentary (dI2) with persistant pulp and enamel restricted to the anterior face. With regard to the incisors, Andrews (1915) remarked that only two conditions among living bovids are remotely similar; Ovis central incisors are notoriously higher-crowned than other bovids, and in gazelles the central incisor is larger than the lateral. In addition to the incisors, the molars of M. balearicus are extremely hypsodont (Gliozzi and Malatesta, 1980), and as originally observed by Andrews (1915) and Androver and Angel (1968), attained a degree of molar hypsodonty surpassing that of any other bovid. In addition to increased molar hypsodonty, the taxon is noted for reduced jaw length and proportional increase in insertion scars for masticatory muscles such that occlusion was especially active on the distal portion of M2 and M3 (Bover, 2004). 6.2 Crown height evolution on Mediterranean islands 157

As an explanation for the dental peculiarities, Andrews (1915) proposed that the animal lived on lichens, mosses, and small plants growing on rocks, food that was “exceptionally hard and intractable [a]s shown by the extremely hard wear to which the hypsodont cheek teeth must have been subjected; possibly the inclusion of fragments of the rocks with the food may have added to this effect.” Andrews added in note (Andrews, 1915, p. 303) that Freudenberg (1914) had proposed that the incisors may have been adapted for stripping bark from the stems of heath-like bushes, or of trees, and tough woody fiber. Myotragus balearicus may have gnawed at horns (Reumer and Robert, 2005). Most recently, coprolites of Myotragus balearicus have been collected and their pollen contents revealed. This evidence indicates that the hardy evergreen shrub Buxus balearica (Buxaceae), an abundant plant in the landscape, may have been its habitual diet (Alcover et al., 1999; Yll et al., 2003). Unfortunately, the phytolith content of Buxus has not been described, and despite Andrew’s speculations, Alcover et al. (1999) did not look for soil mineral grains within the coprolites. Bone and antler gnawing is characteristic of many Artiodactyla (Sutcliffe, 1973), especially living on calcium-rich Mesozoic limestones as on Mallorca. Myotragus was not the only mammal to evolve high-crowned teeth on Mallorca. Hypnomys, a glirid rodent lineage, evolved increased crown height and a flat molar occlusal plane typical of a herbivore with an abrasive diet (Bover et al., 2008). The parallel evolution of high-crowned teeth in Myotragus and Hypnomys suggests environmental conditions may have been responsible for driving these parallel dental specializations. Environmental conditions on Mallorca through the Quaternary were highly variable and energetic, dominated by eolian (dunes, sand, loess) and fluvial processes, and soil formation (Rose et al., 1999). In addition, during Quaternary oxygen isotope stages 2 through 6, Mallorca experienced sea-level fluctuations, alternating cold and warm atmospheric temperatures, extensive fluvial erosion, eolian dune formation, high atmospheric dust concentrations with loess accumulation, and vegetation changing between open, arid, and sparse cover to denser cover (Rose et al., 1999). Today, the Balearic islands are from 60 to 200 km from the Spanish coast, but the ancestor of Myotragus is thought to have arrived on the Balaerics during the Messinien Salinity Crisis around 5.9 to 5.5 Ma, and Myotragus occupied the islands continuously until the arrival of humans. The highest elevations on Mallorca today are over 1400 m and the combination of elevation zonation and deep ravines support a fairly rich endemic flora. The area of the island fluctuated between 1000 and 6000 km2 during the time Myotragus lived. Trackways of Myotragus (the Bifidipes aeolis ichnospecies of Fornós et al., 2002) have been found on sand eolianites composed of marine bioclasts that originated from the shallow marine carbonate platform. The Balearic Islands are the emerged topographic highs of the submarine Balearic Promontory. The Southwest Majorca Volcanic Field between the islands of Mallorca and Ibiza includes the alkaline basalt plateau of Emile Baudot Seamount and a hundred or more pinnacles that are also features of the Promontory. Volcanic activity during the early Pleistocene in the Southwest Majorca Volcanic Field was magmatic (Acosta et al., 2004) and there is no evidence that this magmatic activity included the kind of eruptions that produce abundant pyroclastic ash. 158 Crown height and tooth wear on islands

6.2.2 Maremma

The late Miocene islands that today make up the Maremma region of mainland Italy were part of a larger faunal province that included most of Sardinia and probably also Corsica (Rook et al., 2006). Maremmia and other elements of the late Miocene Oreopithecus-Maremmia fauna are known from lignite mines in what is today mainland Italy and also in northern Sardinia (Cordy and Ginesu, 1994). The Oreopithecus- Maremmia fauna is highly endemic and unique to sites in Grossetto province on the Italian mainland and adjacent islands of the Tuscan archipelago. The ungulates of this fauna include as many as four species of bovids, a girafﬁd, and the suid Eumaiochoerus (Hürzeler and Engesser, 1976; Thomas, 1984). Among these ungulates, only Maremmia haupti (Bovidae, Alcelaphinae?) is known to have evolved ever-growing incisors (Hürzeler, 1983). The anterior teeth of the mandibular arcade include a small canine and three incisors très bizarres, with elongate crowns, open pulp cavities, and enamel restricted to the labial aspect, such that la fonction de ces incisives est encore une énigme (Hürzeler, 1983, p. 501). In addition to these highly specialized incisors, Maremmia haupti had exceptionally high molar crowns. The endemic mammals of the Maremma region of Tuscany underwent signiﬁcant morphological change during the estimated two-million-year interval between two distinct faunal levels. The older fauna is thought to have been insular and contains specialized bovids and rodents with a tendency for the development of hypsodonty and large body size. The stratigraphically higher and younger fauna also shows high endemism typical of insular faunas, and shares relatively few species in common with the older level. In addition to the arrival of new immigrants, there also appeared new paleospecies resulting from in situ evolution (i.e., Anthracomys majori from Huerzelerimys oreopitheci and Maremmia lorenzi from Maremmia haupti). Both Maremmia lorenzi and Anthracomys majori have more hypsodont molars than their presumptive ancestors (Hürzeler, 1983; Engesser, 1989;Meinetal.,1993). Until recently, faunal constraints permitted only an approximate correlation of the endemic insular faunas of the Tuscan archipelago to the interval between 9.5 and 6.0 Ma (Rook et al., 1996). More recently, Rook et al. (2000) dated a tuff to 7.55 Ma, the ash originating from the Capraia Islands, a source area in the Tyrrhenian Sea, about 110 km WNW. The source was part of the Tuscan Magmatic Province, an active volcanic center during the late Miocene. Neogene to Quaternary potassium-rich volcanic rocks are widespread along the Tyrrhenian border of the Italian peninsula and offshore from the Tuscan to the Eolian archipelagos (Conticelli et al., 2007).

6.2.3 Sardinia

Sardinia has a long and complex history as an island, largely because of sea-level ﬂuctuations (Cordy and Ginesu, 1994; Van der Made, 1999, 2008). For example, the area of Sardinia may have ﬂuctuated between 20 000 and 32 500 km2,andatlowsea- level, the distance to the mainland is only 10 km. Sardinia and nearby Corsica become joined at low sea-level and have similar faunal histories as islands (Van der Made, 6.2 Crown height evolution on Mediterranean islands 159

1999). The pre-Messinian faunal history of Sardinia includes two distinct levels, reviewed most recently by Van der Made (2008). The several thousand meter sea- level drop associated with the Messinian Salinity Crisis was a key event that allowed new immigrant mammals to colonize the island (Azzaroli, 1981; Spoor and Sondaar, 1986). Pliocene flooding isolated Sardinia from nearby areas, and glacioeustatic sea- level fluctuations of the Pleistocene led to a succession of faunas, the transitions accompanied by extinctions and first appearances (Van der Made, 2005;Masinietal., 2008). One of the oldest insular faunas from the Mediterranean is the early Miocene Oschiri fauna of Sardinia (Van der Made, 2008). Among the large mammals, Sardomeryx oschirensis (of uncertain but possibly giraffoid affinities) had relatively high-crowned teeth, comparable in height to teeth in later ruminants, but higher than contemporaneous early Miocene ruminants (Van der Made, 2008). At least three ungulates from post-Messinian assemblages on Sardinia display dental specializations that also suggest abrasion resistance (Van der Made, 1999). The first is the dwarf suid Sus sondaari, descended from a mainland ancestor of late Miocene–early Pliocene age (Van der Made, 1988). The evolution of increased crown height in the premolars and molars, increased enamel thickness, loss of the first lower premolar, simplification of molar structure, and reduction of premolar size suggest adaptations to abrasives (Van der Made, 1988; Van der Geer, 2005). The second is Nesogoral (Bovidae, Caprinae?) thought to have arrived by sweep- stakes dispersal from a mainland ancestor, possibly Pachygazella, the putative ancestor of both Nesogoral and Myotragus (Gliozzi and Malatesta, 1980; Van der Made, 2005). Although the dental adaptations of Nesogoral are not as derived as those of Myotragus, it has very high-crowned molars (Van der Made, 2005) and has been described as having ever-growing teeth (Arca and Tuveri, 2006), although this needs to be confirmed. The third is the deer Megaloceros sardus. Van der Made and Palombo (2004) note that the enamel of Megaloceros sardus is thick. Thick enamel is common in insular artiodactyls (Van der Made and Rodriguez, 2003; Van der Made, 2004). Another example of this is the Pleistocene cervids from Crete and Karpathos that have thicker enamel and show a moderate increase in hypsodonty over their assumed ancestors (De Vos, 1984). Remains of Megaloceros cazioti in Sardinia and Corsica are known mainly from eolianites or cave deposits attributed to the late Pleistocene (Van der Made and Palombo, 2004). Late Miocene to Quaternary volcanic activity was widespread on the island of Sardinia and included a middle Pliocene to late Pleistocene phase from about 3.9 to 0.1 Ma (Lustrino et al., 2007).

6.2.4 Crete

The Pleistocene endemic deer on Crete display insular modiﬁcations to the postcranium, and are thought to have evolved some moderate degree of increased crown height and thicker enamel than continental deer (De Vos, 1979, 1984). Cervids were common 160 Crown height and tooth wear on islands

colonists to Mediterranean islands and many endemic forms evolved. A large number of cervids of different body sizes are known from Crete, ranging from a dwarf cervid, a species of Cervus, and/or as many as eight species of Candiacervis (De Vos, 1979, 1984). Cranial and mandible characters have been used to distinguish grazing from browsing cervids, and postcranial proportions and stature to distinguish feeding height (Caloi and Palombo, 1995). Features of presumed low-level grazers include a square rostrum, reduced maxilla anterior to P2, rough and large attachment areas for masseter, reduced attachment area for temporalis, and reduced height of the horizontal ramus from m3 to p2. In particular, the teeth of the smaller megacerine Megaceroides cretensis are described as hypsodont and suggest “feeding on Gramineae” (Caloi and Palombo, 1995, p.252).

6.2.5 Ibiza

A caprine (possibly Tyrrhenotragus) and an unnamed very hypsodont small antelope have been reported from the island of Ibiza (Eivissa in Catalan) (Agustí and Moyà-Solà, 1990). The bovids together with two rodents (a girbilid and a glirid) and a leporid comprise the late Miocene–early Pliocene age Ses Fontanelles fauna (Bover et al., 2008). A younger late Pliocene fauna from Cova de Ca Na Reia on the same island contains two glirids, including Hypnomys (Alcover and Agustí, 1985). The island of Ibiza is some 100 km from the southeastern coast of the Iberian Peninsula, at approximately 39 N. Whether Ibiza evolved a unique endemic fauna characterized by the independent acquisition of hypsodonty or was colonized repeatedly from the larger Balearic islands is as yet uncertain (Bover et al., 2008).

6.2.6 Gargano

The Gargano peninsula, in the Province of Foggia of southeastern Italy (the spur), is now part of the Italian peninsula. In the early and middle Miocene, Gargano was connected to the continent, but between the late Miocene and early Pliocene, it was an island. Karst fissure fillings on the peninsula yield middle to late Miocene (11 to 9 Ma) mammals, thought to represent an insular fauna on the basis of taxonomic impoverishment compared with contemporaneous faunas elsewhere in Europe (most notably the absence of Perissodactyla and Proboscidea) and nearly all the mammals (except Artiodactyla) showing a tendency toward either gigantism or dwarfism. The fauna took on qualities attributed to insularity during an interval of isolation, an interval poorly constrained, but extending from the middle or late Miocene until the early Pliocene (Abazzi et al., 1996). During this interval of isolation, Gargano hosted an endemic fauna of herbivores including the burrowing murid (Mikrotia), several species of the giant brachydont cricetid (Hattomys), three species of the huge brachydont glirid (Stertomys), the murid Apodemus, two species of large hypsodont ochotonid (Prolagus), and the “prongdeer” Hoplitomeryx (Hoplitomericidae) with five horns and sabrelike (“moschid” type) upper canines and “variable hypsodonty” (Leinders, 1984; Van der Geer, 2008). Mikrotia, a burrowing rodent as judged by cranial and postcranial 6.3 Environmental change on Mediterranean islands 161

characters and incisor curvature (Agrawal, 1967; Parra et al., 1999), evolved hypsodont cheek teeth during the interval of isolation (Freudenthal, 1976, 1986), and two lineages of Prolagus also show an increase in crown height (Mazza 1987a, b, c). Three lineages of Muridae from the Neogene of Gargano show evolutionary trends of changing skull size, increase in the length and number of lobes on m1 and M3, and progressive hypsodonty, finally attaining a degree of hypsodonty unequaled by any other European murid (Freudenthal, 1971, 1976). Abbazzi et al. (1993) confirmed that increasing hypsodonty, crest number, and relative thickness of enamel characterize each of the three independent phyletic lineages of Mikrotia. The Gargano area was subject to the influence of surface processes mobilizing the products of subduction-zone pyroclastic-rich volcanism (De Astis et al., 2006). During a wet climate phase in the late Pleistocene, there was erosion and transport of soils from surrounding areas and sediment sources originating in the Pleistocene eruptions of Vulture volcano. During a dry climate phase, tephric loess was deposited with mineral composition similar to the Campanian Ignimbrite, with inputs of fresh volcanic ash and pyroclastic material from sources to the west by eolian processes (Cremaschi and Ferraro, 2007). Whether such processes operated during the Miocene and Pliocene is an open question.

6.3 Environmental change on Mediterranean islands

The latitudes of these six islands are just poleward of the 30 N latitude peak of ungulate hypsodonty globally, in the latitudinal zone of Mediterranean climates characterized by hot, dry summers and cool, wet winters. This climate is associated with large subtropical high pressure cells that shift seasonally (poleward in the summer and equatorward in the winter), and that have a major role in the formation of the world’s subtropical deserts. The characteristic vegetation is of the Mediterranean forest, woodland, and shrub biome and distinctive sclerophyll shrublands of woody plants with small dark leaves covered with a thick waxy cuticle. Mediterranean islands underwent significant and continuous environmental change through the late Neogene and Quaternary, including the arid Messinian, three distinct phases of the Pliocene (5.2 to 3.2 Ma; 3.2 to 2.6 Ma; and 2.6 to 1.8 Ma at the onset of glacial-interglacial cycles), and the Quaternary with numerous oxygen-isotope stages of alternating warm (forested), interglacial, and cold (steppe) glacial conditions (Mannion, 2008), numerous alluviation cycles (Macklin et al., 2002), and trenchant slope and eolian processes (Rose et al., 1999). The word volcanism and the technical terms used for different styles of volcanic eruption have their geographic etymology in the Mediterranean. The island of Vulcano (and the island and volcano of Stromboli) gives its name for the characteristic intermittent explosions or fountains of basaltic lava from a single vent or crater; and finally, the term Plinian derives from Pliny the Younger’s description of the eruption of Vesuvius. Plinian eruptions are large explosive events that form enormous dark columns of tephra and eject gas high into the stratosphere, accompanied by pyroclastic flows and extensive ash falls. 162 Crown height and tooth wear on islands

Do volcaniclastic deposit minerals contribute mineral abrasives to the soils or soil parent material on Mediterranean islands, where we find extremely hypsodont ungulates (and other mammals that evolved tooth structures for resisting abrasion), before or during the time extreme hypsodonty evolved? Savelli (2002) provides a comprehensive catalog of K-Ar and Ar/Ar dates for igneous rocks in the Western Mediterranean (including dates, rock type, and eruption mode (ignimbritic, intrusive, and pyroclastic), the site, area, and structural setting, and three post-Messinian magmatic phases were distinguished by age: Phase IV (5–2 Ma), Phase V (2–1.5 Ma), and Phase VI (1.5–0 Ma). Volcanic activity during Savelli’s Phase IV was widespread throughout the Western Mediterranean, Sardinia, Tuscany, the North and West Tyrrhenian, and central Italy. The record of Phase V volcanism is less intense and extensive, but it affected Southern Spain, the Catalan volcanic zone, and the South Tyrrhenian. Phase VI volcanic activity was again intense, and extended from the Catalan volcanic zone to Sardinia, Tuscany, Central Italy, and south to the Eolian Archipelago. On Sardinia, late Miocene to Quaternary volcanic activity was widespread and included an important phase in the middle Pliocene to late Pleistocene (Lustrino et al., 2007). In Tuscany (Maremma), Neogene to Quaternary potassium-rich volcanic rocks are widespread along the Tyrrhenian border of the Italian peninsula and offshore between the Tuscan and Eolian Archipelagos (Conticelli et al., 2007). Based on present evidence, Gargano, the Balearic Islands, and Crete are the only areas of the Mediterranan that were not important source areas of volcanism at the time when morphological adaptations for abrasive tooth wear evolved. Thus, volcanism or volcaniclastic sediments are not a necessary precondition for the evolutionary response observed there. If not, what is? As with the geographic etymology of volcanism, the Eolian Islands are a group of volcanic islands in the Tyrrhenian Sea north of Sicily (including Stromboli and Vulcano) that were named after the Greek keeper of the winds. The middle Pleistocene from about 140 ka to about 770 ka on Mallorca includes seven to eight glacial-interglacial cycles of alternating colluvial and calcareous eolianite deposits (Nielsen et al., 2004). This succession of interbedded eolian carbonates and colluvium indicates that eolian processes prevailed throughout much of the middle Pleistocene. The source and source area for the eolian sediments were marine carbonate sands that the dominantly westerly winds carried inland. As these dunes migrated eastward, they were subsequently eroded by both wind and water. The alternating colluvial deposits are largely comprised of eolian silt and dust. Rhizoconcretions are abundant in the eolianites indicating plant trapping during deposition. Erosion under Mediterranean climates occurs both as rainstorm-induced erosion of hillslopes and channel flooding in wet phases of climate cycle seasons and as eolian processes in dry phases. Source areas for fine-grained windblown dust include accumulated volcaniclastic deposits and regional deserts (Prospero, 1996; Di Sarra et al., 2003). Today, anthropogenic factors of overgrazing, fire, and deforestation are the major contributors to soil erosion (Cerdà, 1998). Sediment cores in the Western Mediterranean document orbital timescale variation in terrigenous dust accumulation (Weldeab et al., 2003). In the Eastern Mediterranean, 6.4 From consequences to processes 163

sources include Saharan aerosol dust and the discharge of suspended matter from European rivers (Larrasoaña, et al., 2008). Surface winds over much of the Mediterra- nean are subject to orographic effects as mountainous land surrounds most of the sea, and remarkably high wind stress and vorticity occur between islands (Zecchetto and De Biasio, 2007). Sufﬁcient dust is deposited from the Sahel and Sahara to form a discrete soil layer in the extreme south of Europe, and loess in the Canary and Cape Verde Islands (Stutt et al., 2009). Today, dust transport events control a signiﬁcant fraction of mineral particle deposition in the Western Mediterranean, including on the island of Corsica (Bergametti et al., 1989). Dust rains have been reported on Mallorca where they are recognized to be an important sedimentary process (Fiol et al., 2005). However, on Mediterranean Islands, such deposits are rarely reported in paleontological contexts.

6.4 From consequences to processes

There are at least six examples of ruminant artiodactyls evolving exceptionally high- crowned cheek teeth and at least two examples of their evolution of ever-growing incisors on islands in the Mediterranean. In addition, diverse dental structures for resisting abrasion evolved in other ungulates (suids and cervids) and rodents (glirids). That such diverse morphological contrivances are found on islands throughout the Mediterranean suggests coincident causation. Explanations advanced in each particular case (specialized food acquisition in Myotragus from the Balearics, feeding on Grami- neae for Megaceroides cretensis of Crete) seem inadequate to explain all the examples. And yet a sweeping claim in favor of a single encompassing explanation involving the earth surface processes of erosion, volcanism, and wind in island ecosystems, while plausible, seems hardly more convincing. The available information on temporal and spatial variation in earth surface processes through the five-million-year history of dental adaptation is frustratingly incomplete, and the fossil and rock records from Mediterranean islands do not permit reconstruction of coincident timing and geography between agency and evolutionary response. Yet the Mediterranean fossil record is impressive in its morphological and taxonomic diversity and in the extent of evolutionary parallelism. Recreating the environment–morphology interaction in the rock and fossil record of islands is very difficult. In addition, humans have altered the Mediterranean island ecosystems so irrevocably that the study of modern processes on these islands would be nearly as difficult. Up to now, everything we know about modern processes of soil erosion and their consequences for soil ingestion and tooth wear in ungulates occurs in anthropogenic landscapes. Sheep were introduced onto the North Island of New Zealand from Europe and deforestation was necessary to establish the industry. As the native forests were felled and the country opened, pastureland expanded, and a thriving modern pastoral agroecosystem developed. The modern system of wool production, especially its intensification in the last half of the twentieth century, has shaped the relationship between soil erosion, soil ingestion, and tooth wear. While the etiology of excess 164 Crown height and tooth wear on islands

tooth wear in sheep is complex, history of its study points to the primary role of soil ingestion, proven ultimately by the success of management strategies that were adopted for its control. Sheep were also introduced into Australia where the process advanced as successfully as in New Zealand. After an initial period of overstocking, the lessons learned eventually led to an intense modern pastoral agroecosystem. As on the North Island of New Zealand, soil ingestion is a feature of sheep ranching in southern New South Wales. In Australia, the grazing of sheep at high densities contributes to surface disturbance. However, the surface processes are distinct, as SE Australia is arid whereas the North Island of New Zealand is wet. So much for intensively managed ecosystems. Can the inﬂuence of earth surface processes on tooth wear be detected in native or feral ungulates in natural settings where human intervention is minimal or nonexistent?

6.5 Feral goats and sheep on islands

During the nineteenth and twentieth centuries, seafarers introduced domestic goats onto hundreds of islands around the world as livestock for ship replenishment and food for shipwrecked sailors (Campbell and Donlan, 2005). Since then, feral goat populations have become the target of eradication because of their devastating effect on native plants (Parkes, 1993, 2001; Campbell and Donlan, 2005; Krajick, 2005). From another perspective, populations of feral goats on islands comprise a priceless resource for the study of population-level variation in tooth wear. Each island has a unique environment, flora, and vegetation, and the goats eat different foods in different ways (Parkes, 2005). More importantly, the soil parent material and the extent of exposed mineral soil at the surface varies with island geography, climate, vegetation, and the activity of the goats (Royle, 2001). Soils on oceanic islands are derived from either volcanism or coral limestone, with a variable addition of windblown dust and volcanic ash depending on proximity to sources (Rolett and Diamond, 2004). Most feral goat populations on islands are descendants of the domestic goat (Capra hircus), and their tooth enamel is assumed to have comparable hardness and similar microstructure in the properties that impart resistance to abrasion. Measurable differences in tooth wear rates between islands are assumed to reflect the role of the mineral abrasives they ingest, and thus, feral ungulate populations provide numerous and varied examples of the relationship between earth surface processes and the role of mineral abrasives on tooth wear. Eradication efforts to remove introduced ungulates and restore insular floras have also targeted feral sheep. Domestic sheep (Ovis aires) were introduced onto fewer islands than goats, and more often as part of concerted efforts at human colonization (Parkes, 2005). As such, sheep introductions have met with varying success (Wilson and Orwin, 1964). Compared with sheep, goats are more successful colonizers at all latitudes (Knights and Garcia, 1997). The reasons for their success include a generally longer time spent masticating and ruminating (Louca et al., 1982); lower water turn-over rates and 6.5 Feral goats and sheep on islands 165

requirement of less water intake (Gihad, 1976; Gihad et al., 1980); enhanced ability to dessicate feces, concentrate and reduce urine volume, and reduce evaporative water loss (McDowell and Woodward, 1982); and having longer digesta retention times (Devendra, 1981), higher counts of cellulolytic bacteria in the rumen microflora (Gihad et al., 1980; Louca et al., 1982), and superior fiber-digesting capability (Domingue et al., 1990). Whereas sheep have a more selective grazing strategy, goats are less discrimin- atory and able to change their harvesting strategy according to the structure of the vegetation. As active browsers, goats travel great distances in search of food and utilize a wider variety of plants, grasses, leaves, and twigs not normally eaten by sheep (Louca et al., 1982). Measurements of ingestive behavior have been made on goats and sheep utilizing prepared grass and legume turf samples from monoculture plots (Gong et al., 1996). These comparisons reveal that bite depth differs markedly between sheep and goats, with sheep penetrating deep within the canopy to take deep bites whereas goats are shallow “top-down” grazers (Domingue et al., 1991). Additionally, in tall and stemmy reproductive grasses, sheep selectively graze leaf components whereas goats prehend reproductive tillers, inflorescences, and stalks as well as green leaves (Gong et al., 1996). On small islands where food scarcity is more common, goats and sheep may be obliged to eat the same things or exploit forest or grassland in ways that contradict the classical dichotomy between browser and grazer. For example, goats survive in harsh environments with low rainfall (under 70 mm/yr), and to survive on a treeless island, goats have to become herbivore grazers. Thus, feral goat and sheep introductions on small islands provide interesting comparisons of the universality of the grazer– browser dichotomy and its consequences for tooth wear. For example, Mainland (2003) found that while fecal phytolith concentrations from open-country-grazing and woodland-grazing sheep were similar, concentrations of extrinsic grit were much higher in open-country grazers and the phytolith to grit ratios much lower. Similar comparisons undertaken between feral populations on islands might reveal more about the environmental agencies underlying rates of tooth wear. The study of tooth wear in island populations confined to particular soil erosion regimes provides insights that are simply not available from studies conducted in the more persistent and unvarying environments of larger landmasses (continents), where animal populations exercise a broader range of behavioral adaptation including migration. Many oceanic islands are volcanic in origin (Darwin, 1842) and this volcanism is of two major types: (1) basaltic shield or mid-ocean ridge volcanoes (e.g., Hawaii, the Galapagos Archipelago, Saint Helena) characterized by low-angle basaltic lava flows, scoria cones, and some pyroclastic material, or (2) island arcs along subduction zones with explosive pyroclastic volcanism of andesitic or rhyolitic composition (e.g., Scotia Archipelago, Kermadec, and islands along the “Andesite Line”) (Stoddart and Walsh, 1992). Volcanic ocean island ecosystems are unstable because of eruption activity and seismicity. After geographic location, island morphology (area, relief), and the time elapsed between eruption events, rainfall is the most important dimension of environmental variability on small islands. Instrument records reveal geographic and latitudinal variation in mean annual rainfall, and there is considerable seasonal, interannual, and decadal variation in rainfall (Stoddart and Walsh, 1992). 166 Crown height and tooth wear on islands

Naturally regulated island populations of domestic sheep and goats have an intrinsic interest to animal ecologists, and some islands and island populations of feral ungulates have been well studied (Jewell et al., 1974; Leader-Williams, 1980, 1988; Clutton- Brock and Pemberton, 2004). Their intrinsic interest to biology may be explained by recalling that, first, there is a wealth of information available about the basic biology of domestic sheep and goats. Second, feral populations of goats and sheep were introduced onto hundreds of islands around the world. Finally, small islands present relatively simple ecosystems, often predator-free, and environmental conditions influencing variation in tooth wear rates are easily compared and contrasted. While islands would seem to be ideal environments to study variation in tooth wear, there have been relatively few studies of interspecific or geographic variation in ungulate tooth wear (Fandos et al., 1993; Hewison et al., 1999). Leader-Williams (1980, 1988) observed dental pathologies indicating the intensity of tooth wear in the ecological accommodation of reindeer to the rigors of South Georgia Island. Mainland (1998) discovered the significance of soil ingestion to tooth microwear in grazing and island- dwelling sheep in the Orkney and Hebrides islands off the coast of Scotland. Why Clutton-Brock and Pemberton (2004) did not look more deeply into the mouths of Soay sheep in the St Kilda archipelago, or Réale et al. (2000) into the mouths of the feral sheep of Kerguelen Island in the Southern Ocean, may be explained by the deep organic peaty soils of these islands and the absence of mineral soil at the surface (Campbell, 1974). Tooth wear has been examined and remarked upon in the literature on feral and domestic ungulates from New Zealand and its surrounding islands (Figure 6.1). In a large collection of goat jaws from Macauley Island in the Kermadec archipelago, Williams and Rudge (1969) noted that almost all of the observed dental abnormalities involved excess wear, described as “m1 worn below bifurcation and roots free”; “excess wear on m2”; “excess wear on p4, m1”; “buccal tilt to p3–4, m1”; “excess wear on p2–4, m1” (p. 22). The most common condition observed was excess wear at p4 or m1. Wear on m1 extended below the root bifurcation in 26% of the mandibles collected and “several mandibles estimated to be over seven years old showed extensive wear along the row but without the deep trough between p3–m1” (p. 23). Pathological specimens from Macauley Island include many where the m1 has structurally failed, a particularly conspicuous pathology in unmanaged populations, as also observed in reindeer on South Georgia (Leader-Williams, 1980, 1988). The pattern of excess wear “probably had its main cause in the extreme abrasiveness of the volcanic dust ingested with the food” (Williams and Rudge, 1969; p. 23). By contrast, the literature on feral sheep of Campbell Island in the sub-Antarctic, uniformly describes their teeth as being in excellent condition (Wilson and Orwin, 1964; Suckling and Rudge, 1977). Suckling and Rudge (1977) established that incisor tooth wear in the Campbell Island feral population was much reduced even by comparison with domestic flocks in the main islands of New Zealand. They attributed this difference to the absence of exposed soil on Campbell Island. Variation in sheep tooth wear on the North Island of New Zealand is attributed to the ingestion of mineral abrasives (Healy and Ludwig, 1965a, b; Ludwig et al., 1966; 6.5 Feral goats and sheep on islands 167

Raoul Kermadec Islands 30°S

Macauley

North Island

40°S

South Island

50°S

Auckland Islands

Campbell Island

Figure 6.1 Map of New Zealand and its surrounding islands. 168 Crown height and tooth wear on islands

Healy, 1967, 1968). Undoubtedly, the concentration of biogenic mineral abrasives in endemic plants is rarely measured and is assumed to be at concentrations similar to closely related plants (Thorn, 2004, but see later). Among ingested mineral particles, given the constant and low concentration of opaline silica in forage or pasture plants (Hodson et al., 2005), the low relative hardness of plant silica under physiological conditions (Sanson et al., 2007), and the temporal and geographic coincidence between tooth wear rates and soil ingestion (Chapter 4), soil ingestion, not the ingestion of mineral particles intrinsic to plants, may be driving most of the observed variation in tooth wear in this interisland comparison. However, in the absence of direct evidence of soil ingestion (soil content in fecal material or some trace in bone or tooth mineral) and better knowledge of the concentration of silica in the insular plants that comprise the diet of these feral ungulates, we are left with only the broadest comparisons of relative soil erosion on each island and speculation about its role in tooth wear. Furthermore, in the absence of a better method of determining individual age, comparisons of tooth wear between islands must be described in relative terms. Until more precise methods are applied to the determination of individual age (at the onset of wear, and at death), and until better methods are used to describe the total mineral particle ﬂux through the animal’s ingesta and environment, we will have to content ourselves with the following comparison.

6.5.1 Material

Collections of feral goat or sheep mandibles were made during eradication operations on three islands administered by New Zealand (Table 6.1).

Table 6.1 Three islands administered by New Zealand with feral goat and/or sheep populations and where collections of mandibles have been made during eradication operations and for which collections were studied

Date of introduction # shot, #jaws collected Island Area (ha) and extirpation (date of sampling) References

(1) Raoul 29 S 2950 Goats introduced in 1286 shot Aug–Oct 1972, Rudge and Clark, (active volcano) the 19th century 155 jaws collected 1978; Parkes, 147 shot Apr–Dec 1983, 1984a, b 81 jaws collected (2) Macauley 30 S 320 Goats 3200 shot, 118 jaws Williams and (extinct volcano, collected, 4236–4353 in Rudge, 1969; pumice substratum) August 1966 Rudge, 1970 (3) Campbell 52.5 S 11 200 Sheep introduced 1281 shot in 1970 and Rudge, 1976; (much dissected in 1895; eradicated 1066 mandibles collected Suckling and extinct volcanic in 1988. by hunters Rudge, 1977; cone) Wilmshurst et al., 2004. 6.5 Feral goats and sheep on islands 169

Figure 6.2 Capra hircus mandibular tooth rows in lingual and occlusal views from Raoul Island at developmental BEW stages 1 (top), 2 (middle), and 3 (bottom). (For a description of tooth wear at these stages, see Table 6.2.)

6.5.1.1 Raoul Island Two collections of the mandibles of feral goats from Raoul Island (Figure 6.2) were examined: (1) a wild-shot collection made between August and October 1972 and housed at the Museum of New Zealand Te Papa Tongarewa (Wellington), and (2) a wild-shot collection made between May and November 1983 (the last year of a sustained 10-year eradication effort) housed at Landcare Research (Lincoln). The Land- care sample was made between May and November 1983, some 10–11 years after the 1972 sample, at the end of an extended intensive eradication program that lasted from at least 1979 to 1984. There are 89 mandibles in total in the Landcare sample, of which 68 are dental juveniles and 21 dental adults. The bias toward juveniles is explained 170 Crown height and tooth wear on islands

Figure 6.3 Capra hircus mandibular tooth rows in lingual and occlusal views from Macauley Island at developmental BEW stages 1 (top), 2 (middle), and 3 (bottom). (For a description of tooth wear at these stages, see Table 6.2.)

by the fact that these animals were wild-shot at the very end of the eradication program, at which point only the most vigorous individuals remained.

6.5.1.2 Macauley Island During eradication operations in 1966, 118 goat mandibles were collected from carcasses and skeletons laying on the soil surface (Figure 6.3). These mandibles were deposited into the collection at Te Papa. These were animals that had died from natural causes prior to the arrival of the extermination expedition. No incisors are found with the mandibles, as they had dropped out of the mandibles postmortem. As a surface collection accumulated from natural mortality, preservation biases are unknown, and potential sampling biases include the intent of the collectors to recover a full range of 6.5 Feral goats and sheep on islands 171

Figure 6.4 Ovis aires mandibular tooth rows in lingual and occlusal views from Campbell Island at developmental BEW stages 1 (top), 2 (middle), and 3 (bottom). (For a description of tooth wear at these stages, see Table 6.2.)

dental wear ages including individuals with “abnormal and excess wear.” Contaminant soil adheres to the mandibles, a very ﬁne dust-like volcanic ash that must be brushed off in order to reveal the details of the occlusal pattern.

6.5.1.3 Campbell Island A large collection of wild-shot feral sheep mandibles from Campbell Island was made by hunters in 1970 (Bell and Taylor, 1970), studied at DSIR (Rudge, 1986), and then donated to Te Papa (Figure 6.4). The collection includes ﬁrst and second permanent incisors sectioned for cementum annuli counts (see Rudge, 1986). According to Rudge (1986) there are 164 juvenile specimens showing m1 erupted (but not m2), 47 juvenile specimens with both m1 and m2 erupted (but not m3), and 514 jaws of young adults with just erupted m3. Of this last group, 91 are somewhat younger and have erupted i1 and i2, but not i3 or c and so m3 is in the earliest stages of wear. 172 Crown height and tooth wear on islands

Table 6.2 Stages of tooth eruption and incipient wear used as benchmarks for “age”–calibration of tooth wear in interisland comparisons

Developmental BEW stage Description

Stage 1 Lower first molar erupted, m1 is the only erupted molar and m1 wear is restricted to the anterior-most crescent or to the buccal crescent of the anterior moiety (i.e., Payne wear stage 2). At developmental BEW stage 1, the stage of dp4 wear is compared between islands Stage 1þ Lower first molar erupted, m1 is the only erupted molar, and m1 wear is somewhat more advanced than in the previous developmental stage. Lower first molar wear is restricted to the anteriormost crescent or to the buccal crescent of the anterior moiety (Payne wear stage 2). At developmental BEW stage 1þ, the stage of dp4 wear is compared between islands Stage 2 Lower second molar erupted, m2 is at the earliest stage of wear, when wear is restricted to the anterior moiety, or more specifically to the precristid on the buccal crescent (protoconid), i.e., m2 wear is at Payne stages 1 or 2. Second molar wear begins on the preparacristid and preprotocristid. At developmental BEW stage, the wear stages of dp4 and m1 can be compared between islands Stage 2þ Lower second molar is erupted and still in early wear but may be at either Payne wear stages 2 or 3, a somewhat more advanced stage of wear than the preceeding developmental stage. While restricted to the anterior moiety, tooth wear extends to the postcristids where either apical polish or dentin may be exposed. At developmental BEW stage 2þ, the wear stages of dp4 and m1 wear can be compared between islands Stage 3 Lower third molar is erupted and in an incipient stage of wear and may be at Payne wear stages 1 or 2. Mandibular third molar wear begins on the precristids of the anterior moiety. At developmental BEW stage 3, dp4, m1, and m2 wear is compared between islands Stage 3þ Lower third molar is erupted, and m3 is in early wear at Payne wear stage 2, but wear is somewhat more advanced than observed in developmental BEW stage 3. At developmental BEW stage 3þ, the wear on dp4, m1, and m2 are compared between islands

BEW, benchmarks of eruption and onset of wear.

6.5.2 Method of comparison

Comparisons among these three islands of relative population-level tooth wear are made using the stage of tooth wear in individual mandibles “age”-calibrated, using benchmarks of molar eruption and incipient occlusion (the onset of molar wear), as described in Table 6.2. In the description of Weinreb and Sharav (1964) of mandibular tooth development in 106 domestic sheep of known ages from birth to 11 years, eruption and occlusion were distinguished. The ﬁrst molar erupts between three and six months of age, and is in occlusion at nine months. Thus, there is at least a three-month interval when the crown has erupted and before it enters into occlusion. There is as much as a half-year 6.5 Feral goats and sheep on islands 173

interval between eruption and occlusion in the m2. The permanent molar and fourth premolar eruption sequences are similar in goats and sheep (Smith, 2000), and to the extent that it is known, the range of individual age at eruption differs minimally (Silver, 1969; Deniz and Payne, 1983). Moreover, goats and sheep differ only slightly in maximum individual age when each molar erupts (Zeder, 2002). For example, in improved breeds of sheep, m1 erupts at about three months of age, m2 erupts between nine and 12 months, m3 between 18 and 24 months, and dp4 is shed before p4 eruption occurs between 21 and 24 months (Silver, 1969). Similarly for Turkish Angora goats, m1 erupts at about three months, m2 at 11 months, m3 at 24–25 months, and dp4 is shed when p4 erupts at 22 months (Deniz and Payne, 1983). The age at first occlusion is also comparable between these two species (Zeder, 2002: Figures 31, 32). How much time elapses between eruption and first occlusion? Obser- vations in domestic Ovis aires indicate that m1 first enters into occlusion sometime between two and six months after birth, m2 before 12 months, and m3 around 18 months of age (Weinreb and Sharav, 1964; Zeder, 2002; Balasse et al., 2003). Thus, age at eruption and the onset of wear are roughly equivalent in sheep and goats. Therefore, judging from what is known about individual variation in age of eruption and the onset of wear, a comparison of the amount of tooth wear between the onset of wear in m1 and the onset of wear in m3 probably represents tooth wear accumulated during 18 months of life. Hence, the following comparisons of population or island modal rates of molar wear are made relative to eruption or the onset of wear (the first exposure of dentin on the tooth surfaces of m1, m2, and m3), and assume approximately equivalent developmental age or comparable developmental time horizons among individuals, populations, and species. For ease of writing and reading, the benchmarks of eruption and onset of wear used here to establish relative rates of tooth wear in interisland comparisons are abbreviated as BEW (Table 6.2). As has been observed previously, the succession of surface configurations (wear stages) is the same in goats and sheep. Early dp4 and molar wear stages involve the expanding exposure of dentin at the occlusal surface. Dentine exposure starts at the apex of the anterior cusps, then widens and extends anteriorly to merge around the anterior fossettid. At about this stage, dentin becomes exposed on the apices of the posterior cusps. With further wear, the dentin exposure of the anterior cusps extends posteriorly to gradually merge with the dentin of the posterior cusps. As the dentin of the anterior cusps becomes confluent with the spreading dentin of the posterior cusps, dentin around the middle or posterior fossettid broadens and gradually extends posteriorly. After the dentin of the anterior moiety merges with that of the posterior cusps, the posterior fossettid becomes completely encircled and isolated. At this stage of wear, all enamel- lined fossettids are isolated. From this stage, wear is characterized by the gradual obliteration of the fossettids, a process that involves their narrowing, pinching, or waisting into a bilobed or dumbbell shape, then gradually being reduced in size into a single small circular fossettid before finally disappearing. With advanced wear, the fossettid of the anterior moiety obliterates first, followed by that of the middle (in the case of dp4), and eventually the posterior moiety. While this succession of surface configurations (wear stages) is the same in goats and sheep, the relationship of the 174 Crown height and tooth wear on islands

plane of wear to the linear height of the enamel crown is not known. Comparisons of the wear stages of anterior teeth at similar stages of eruption and onset of wear is not a comparison of relative wear rates. This does not assume that the temporal interval between eruption and wear benchmarks is similar, only that the pattern of change in tooth shape is similar. Additionally, it cannot be assumed that each change in pattern represents the loss of equivalent volumes of mineral substance, as there are taxonomic differences in tooth shape at the crown apex and through early stages of wear of the mandibular dp4, m1, m2, and m3, and these may have consequences for differences in enamel volume removed by wear. The dp4 crown in Ovis is larger than in Capra, and the enamel crown is higher, such that Ovis dp4 crowns are higher at each wear stage (Payne, 1985). While these differences imply greater total enamel volume in the Ovis dp4, there are other shape differences that compensate. While the dp4 crown is generally higher in Ovis, it is only higher on the buccal side, and actually lower lingually. The dp4 in Capra also displays basal swelling and occasionally interlobular pillars, shape features that increase enamel volume. Thus, dp4 presents special problems of interpretation. With respect to the permanent molars, the mesial face of the m1 crown apex in Ovis is broader buccolingually, and narrower in Capra. While this difference disap- pears with increasing wear, it is a diagnostic feature of early wear stages, and implies greater enamel volume in Ovis. Halstead et al. (2002) point out that in lower molar buccal cusps, the mesial part of the buccal edge is convex in Ovis and concave in Capra, and the buccal edge of the distobuccal cusp points more posteriorly in Capra than in Ovis. An enamel pillar also often occurs on the buccal side of m1 in Capra. What these differences might imply for rates of loss of enamel volume remain to be determined. While these differences in crown shape imply differences in enamel volume lost through wear between comparable wear stages, a comparison of enamel thickness on the distobuccal face of the m1 hypoconid revealed nearly identical absolute enamel thickness in Ovis aries and Capra hircus (Grine et al., 1987). Juvenile mandibles were identified in the collections and specimens were selected that displayed comparable stages of incipient tooth wear at each molar position. On each specimen, the Payne wear stages of dp4, p4, m1, m2, and m3 were recorded. Photo- graphs in multiple views made of each specimen, in addition to high-precision silicon polymer molds from which epoxy resin replicas were made, are used to document the wear stage and developmental stage assignments. The data comprise integer-coded stage of wear of the preceding tooth positions at each benchmark of eruption and the onset of wear (BEW), and the samples are small and unequal (Table 6.3). Wear stages are serial categorical data that express indirectly the amount of tooth crown lost through wear by scoring progress in the changing configuration of enamel and dentin on the occluding surface. The occluding surface at any moment in time describes a plane of wear. Wear stages record an approximate plane of wear, and transitions between successive wear stages mark the end of one interval of tooth wear, during which the configuration of enamel and dentin remained unchanged, and the beginning of the next interval of tooth wear with a distinct configuration. Each 6.5 Feral goats and sheep on islands 175

Table 6.3 Number of juvenile mandible specimens at each developmental BEW stage

BEW stage Raoul Macauley Campbell

1228 1þ 16 4 21151 2þ 71 7 3738 3þ 63 1 Total number of specimens 34 20 29

wear stage represents a different interval of time during the continuous functional life of a tooth, and each change in conﬁguration marks the passing of an unknown interval of time. As has been mentioned, the amount or volume of enamel shed during each wear stage is not known. Although wear stages may be coded by an integer (Payne), integers record the order of the progression of wear, but do not subdivide evenly either the volume of enamel lost or the fraction of total functional lifespan of the tooth. In this sense, wear stages are serial nominal data that mark progress in tooth wear, but neither the interval of time nor the volume of crown shed through wear between successive stages. In the discussion that follows, integer-coded wear stages are dimensionless, and do not represent units of measure (neither time nor volume). For comparison between islands, we are interested in the wear stage of m1 when m2 is erupting and when it ﬁrst shows signs of wear, and the wear stage of m1 and m2 when m3 is erupting and showing incipient wear. We are also interested in comparing the wear stages observed at adjacent tooth positions at the onset of wear of each molar. Finally, we would like to know the range (lowest and highest) of wear stages observed at each tooth position when each molar begins to wear.

6.5.3 Island environments

Environmental features of Campbell, Raoul, and Macauley Islands and their populations of feral ungulates are summarized in Table 6.4. 6.5.3.1 Raoul Island Raoul Island is a very small island, high, steep, and mostly mountainous; the caldera of a submerged volcano. Raoul Island has a surface area above mean sea-level of 29.43 km2, and is a single crater with steep precipitous slopes up to 516 m maximum elevation, with an undulating caldera ﬂoor with three small lakes. Raoul Island is the top of a mostly submerged active volcano with a historical record of 14 eruptions. The island is a succession of basalt and basaltic-andesite lava ﬂows interbedded with red laterite, on top of which rest a thick series of pumiceous tuffs (Brothers and Searle, 1970). While there have been relatively few recent ash showers, the 1872 eruption left a thick ash bed on which recent soils have developed. The tuffs of Raoul Island 176 Crown height and tooth wear on islands

Table 6.4 Environmental features of Campbell, Raoul, and Macauley Islands and their populations of feral ungulates

Campbell (115 km2) Raoul (29.5 km2) Macauley (3.24 km2)

Latitude Sub-Antarctic Subtropical-warm temperate Subtropical-warm temperate zone Geology Old remnant volcanic Volcanic caldera Formed from underwater dome, periglacial caldera eruption 6100 years landforms, alkaline basalts ago, andesitic lava and highly resting on schist vesicular pumice Volcanism Extinct Active volcano, 14 known Extinct eruptions, latest in 2006 Relief, Low ﬂat terrain, four peaks Steep, mountainous terrain, Flat, inclined, between maximum just over 500 m highest point at 516 m 100 and 250 m in altitude altitude Vegetation Tussock (natural) and Forested Grassland, original scrub introduced grasses, burned off shrubland, herbﬁelds Erosion Little exposed soil except Landslip erosion scars on Restricted to perimeter cliff where wind or stock steep topography kept open slopes trampling and unstable by goats Soil, parent Thick peat mantle subject Parent material: andesitic Parent material: andesitic material to mass movement sliding pumiceous tuff pumiceous tuff Climate Rigorous, high humidity, Oceanic climate, mild and Oceanic climate, mild and low temperatures, strong equable, stormy, hurricanes equable, stormy, hurricanes persistent westerly winds (cyclones) (cyclones) Feral Sheep (Ovis) introduced in Goats (Capra) introduced in Goats introduced before 1836 ungulates 1895, half eradicated in nineteenth century, hunted 1970, extirpated yearly from 1972 to completely by 1982 eradication in 1984 Tooth wear Notably: relatively unworn No noted pathologies Many pathologies (see text) and polished tooth crowns (see text)

are unconsolidated and suffer severe erosion from the action of sea and atmosphere. During heavy rains the subsoil becomes saturated and the soil and pumice move downslope in accelerated erosion by land-slipping, especially on the inner wall of the crater. In addition to land-slip erosion on unstable slopes, whole sections of the forest are occasionally overthrown by winds of near hurricane force (Wright and Metson, 1959). At least one event of caldera collapse was followed by rapid erosion that produced a wide apron of redeposited alluvial debris around the caldera rim (Brothers and Searle, 1970). The soil on Raoul Island is a rich, fertile, “exceedingly porous” ﬁne-grained andisol with alluvium additions (Wright and Metson, 1959). Raoul Island has a warm and humid subtropical climate, no permanent streams, but rainfall is high and evenly distributed throughout the year (MAP¼1500 mm), as is temperature (MAT¼19 C), with small seasonal and daily ranges. Except for a limited area on the ﬂoor of the crater, the whole of the island is covered with luxurious forest, from water edge to crater rim (Sykes, 1965). 6.5 Feral goats and sheep on islands 177

Whalers liberated goats on Raoul Island in the early nineteenth century and they were eradicated only recently. Goats were reported to have climbed everywhere on Raoul Island, eating a variety of food items, including bark, leaves of trees, seedlings, and ferns (Parkes, 1984a, b). Their activities thinned the undergrowth, and plants that were once common were nearly exterminated and eventually found only on the steepest cliffs and other places inaccessible to goats. Historically, the goats on Raoul Island were found to have destabilized the ecosystem by altering the understory composition and by slowing succession following avalanching of the Pohutukawa forests during occasional cyclones. Rudge and Clark (1978) give a detailed history of eradication efforts on Raoul Island. Given their assumed value to the study of demographic response, mandibles were collected as a routine part of the eradication efforts. The feral goat population was eradicated from Raoul Island by 1984 after a prolonged campaign that started in 1937 and was intensified in 1972, with yearly hunts extending over a ten-year period. Parkes (1984b) examined the rumen contents of 103 goats shot by New Zealand Forest Service hunters in June–December 1982 and April–December 1983. The rumen contents were first washed in water through a 4 mm sieve; thus, dietary soil content was not assessed. Forty-eight species of plants were identified in the rumen, eight comprised up to 89% of the diet by dry weight. Grasses and sedges made up 10.5% by dry weight, and ranked fourth in abundance, but were found in most (82%) of the samples. The principal foods included Metrosideros kermadecensis (Pohutukawa); the dominant canopy tree comprised 32% of the diet. Blechnum ferns, a common terrestrial plant, were the second most abundant plant food. Coriaria arborea leaves, a widespread shrub, were the third most abundant. The grass Digitaria pruriens and sedge Cyperus ustulatus, common in open places, were the two main species from among the grasses and sedges. Young individuals of Rhopalostylis baueri, the Raoul Island nikau palm; Melicytus ramiflorus (Mahoe), a common subcanopy forest tree that the goats climb; and the fungus Auricularia sp. (a preferred food in goat diet that occurs on tree trunks) complete the list of principal food items. The tree Metrosideros polymorpha forms two-thirds or more of the vegetation, and is closely allied to M. tomentosa, the Pohutukawa of New Zealand. Young trees growing at ground level are very symmetrical in shape, with numerous closely placed branches, but on ridges it attains its greatest stature, although much distorted and gnarled by wind. The next most abundant plants are palms that flourish in the open where they are exposed to sun and wind. On terraces of rich volcanic soil on the northern side of the island, palms form large and nearly exclusive groves. The only true marsh plant on Raoul Island is bulrush (Typha angustifolia). Sedges are rare but plentiful in disturbed areas in the forest, and cutting-grass (Cyperus ustulatus)is everywhere at low elevations, pioneering in abandoned cultivations. Grasses are more abundant, including tropical species not found in New Zealand, and these include Imperata aundinacea, plentiful on cliffs. Ferns comprise over one-fourth of the flora and are the chief undergrowth vegetation. Nothing is known about the phytolith content of the plants on Raoul Island (Table 6.5). 178 Crown height and tooth wear on islands

Table 6.5 Native and introduced plants in the diet of ovicaprines on Macauley, Raoul and Campbell Islands

Phytolith concentration Plant afﬁnities, “common name,” (% of dry Plant species (growth form), and notes weight)

MACAULEY ISLAND Cyperus insularis Poales; Cyperaceae; (sedge); now covers 70% of the land surface Hypolepis dicksonioides Dennstaedtiaceae; (downy ground-fern); forms dense stands in and around gulleys Solanum americanum Solanaceae; “glossy nightshade” Achyranthes velutina Amaranthaceae; “chaff-flower weed,” woody subshrub Lepidium oleraceum Brassicaceae, “Cook’s scurvygrass” (herb) Microlaena stipoides Poaceae; weeping rice grass; most of diet of goats, replaced after eradication by invasive taller sedge and fern Lachnagrostis filiformis Poaceae; “common blown grass” Lachnagrostis littoralis Poaceae Poa polyphylla (small tussock-grass) Polypogon monspeliensis Poaceae; annual “rabbitsfoot grass” Carumbium Stunted bush Myoporum kermadecense Scrophulariaceae; figwort; “Kermadec dwarf ngaios” Homalanthus polyandrous Euphorbiaceae, “Kermadec poplar” RAOUL ISLAND Metrosideros Myrtaceae; “Pohutukawa,” dominant canopy kermadecensis tree; 32% of goat diet Blechnum Blechnaceae; fern; (chief undergrowth in forest); second in abundance in goat diet Coriaria arborea Corariaceae; (widespread shrub); third in abundance in goat diet Digitaria pruriens Poaceae; grass Cyperus ustulatus Poales; Cyperaceae; sedge, “cutting grass” Rhopalostylis baueri Arecaceae; “Raoul nikau” (palm) Melicytus ramiflorus Violaceae; “Mähoe” (subcanopy forest tree) Auricularia sp. Auriculariaceae; (fungus); preferred goat food Imperata arundinacea Poaceae; “bloodgrass,” (cliff-dwelling grass) CAMPBELL ISLAND Danthonia flavescens (¼? Poaceae, Arundinoideae (native tussock grass) 0.61* Chionochloa antarctica) * Poa litorosa Poaceae, Pooideae (native silver tussock grass) 2.29 Poa annua** Poaceae, Pooideae (annual bluegrass) Poa foliosa Poaceae, Pooideae (native grass) Poa ramosissima Poaceae, Pooideae (native grass) Poa sp. Poaceae, Pooideae (native grass) 1.40* Poa breviglumis Poaceae, Pooideae (grass) Poa novae zelandiae Poaceae, Pooideae (grass) ** Festuca rubra Poaceae (introduced red fescue grass) 6.5 Feral goats and sheep on islands 179

Table 6.5 (cont.)

Phytolith concentration Plant afﬁnities, “common name,” (% of dry Plant species (growth form), and notes weight)

Agrostis magellanica** Poaceae (introduced bentgrass) Agrostis leptostachys** Poaceae (introduced bentgrass) Deschampsia chapmani** Poaceae (tussock grass) Trisetum spicatum** Poaceae (oatgrass) Anthoxanthum odoratum** Poaceae (introduced grass) Cerastium vulgatum** Caryophyllaceae (chickweed) Stellaria media** Caryophyllaceae (chickweed) Rumex acetosella** Polygonaceae (herb) Trifolium repens** Fabaceae (introduced clover) Pleurophyllum speciosum Asteraceae (megaherb) Pleurophyllum criniferum Asteraceae (megaherb) Pleurophyllum hookeri Asteraceae (megaherb) Stilbocarpa polaris Apiaceae (megaherb) Myrsine divaricata Myrsinaceae (woody shrub) Ranunculus pinguis Ranunculaceae (poisonous? herb) Ranunculus subscaposus Ranunculaceae (poisonous? herb) Sonchus littoralis Asteraceae (sow thistle) Urtica australis Urticaceae (nettle) Anisotome latifolia Apiaceae (megaherb) Hebe elliptica Plantaginaceae (shrub) 0.09* Cotula plumose Asteraceae (groundcover) Cotula australis Asteraceae (groundcover) Juncus effusus Juncaceae (rushes)

* sampled by wet chemical oxidation of 10 g fresh weight samples of leaves and stems (Thorn, V.C., 2008. New Zealand sub-Antarctic phytoliths and their potential for past vegetation reconstruction. Antarctic Science, 20:21–32); ** introduced species.

6.5.3.2 Macauley Island Another of the Kermadec islands, Macauley Island, is the emergent top of a dormant submarine volcano, the last known eruption of which occurred in 1887 (Lloyd et al., 1996). Macauley Island is small, about 3 km2 in area, and surrounded by vertical cliffs from 45 to 215 m high. The base of the island is andesite lava; the lowest ﬂow is now at or near sea-level. Above the lava is the Sandy Bay Tephra, a 60 m-thick bed of light-colored pumiceous tuff. Above the Sandy Bay Tephra is a suite of basaltic lava, scoria, and tephra of the Haszard Formation, the scoria and ash of which form the soil (Smith, 1887; Lloyd et al., 1996). The climate of Macauley Island is much like that of Raoul Island. The surface of Macauley Island is ﬂat to gently undulating, and at the time of eradication, was covered with a close-cropped sward of natural grass (Polypogon, Poa and Agrostis). No trees or woody plants of any kind were found on Macauley Island, except for stunted bushes of Carumbium and Myoporum, the dwarf ngaio 180 Crown height and tooth wear on islands

(Oliver, 1910), and an occasional exotic (Barkla et al., 2008). When goats were liberated on Macauley Island in the early nineteenth century, colonists burned the scrub to clear it for pasture, and the goats are thought to have effectively prevented its re- establishment. Nothing is known about the phytolith concentration of the plants of Macauley Island (Table 6.5).

6.5.3.3 Campbell Island Campbell Island is a remote mountainous island, the glaciated top of a mostly submerged volcanic cone rising above sea-level. Campbell Island is 115 km2 in area, with four peaks just over 500 m. The island is composed of Pliocene alkaline basalts resting on schist. Campbell Island is a sub-Antarctic island, within the latitude belt of strong and persistent westerly winds. The climate is rigorous, cloudy, bleak, and wind swept, with many rain days, generally high humidity, low temperature, and low sunshine hours especially in winter (De Lisle, 1965). It rains nearly 300 days a year, spread out fairly evenly, and receives only a total of 653 hours of bright sunlight each year. Especially heavy rainfalls accompany the passing of cyclonic depressions and maritime frontal systems. Mean monthly temperature varies only 4.7 C through the year, with comparably small daily variation (McGlone et al., 2007). The most often cited cause of soil erosion on Campbell Island is the random patchiness of sheep grazing disturbances and wind on soil exposed around upland ledges (Meurk et al., 1994). Soil depth is hugely influential on vegetation (Meurk et al., 1994), and the thick organic peat soils (or acid bog soils) under relatively undisturbed vegetation have high water absorption capacity (Thorn, 2004; McGlone et al., 2007). The vegetation is generally shrubland, with tussock grasslands above 120–150 m altitude. The vegetation is low in stature and grasses are a widespread and conspicuous component of the flora. Poa litorosa and Chionochloa antarctica are common and P. litorosa is a “constant dominant taxon.” Some grasses and clover were introduced at about the same time sheep were first introduced between 1865 and 1895. The rumen content of sheep contained mostly fragments of grass cuticle (Wilson and Orwin, 1964) and contained 75%–90% grass (Poa, Festuca rubra,andAgrostis magellanica, all introduced grasses) and a small quantity of the fern Polystichum vestitum.The diet of the feral sheep on Campbell Island includes many plant species (Oliver and Sorensen, 1951). Little can be established about the phytolith concentration in the plants on Campbell Island (Table 6.5). Thorn (2004) analyzed many of the dominant taxa from the vegetation and from the soil surface and concluded that most of the phytolith production is from graminoids. Feral sheep on Campbell Island also fed on some megaherbs of the family Asteraceae, unfortunately not analyzed by Thorn (2004), as this plant family is known to be common or abundant phytolith producers (Piperno, 1988; Pearsall, 2000).

6.5.4 Results

The extent of tooth wear varies among individuals (Table 6.6), but the central tendency (mode) and range of variation (in Payne wear stages) between the three island populations is summarized in Table 6.7 and Figure 6.5. Box plots showing the range and 6.5 Feral goats and sheep on islands 181

central tendencies of Payne tooth wear stages at each BEW (Figure 6.5) confirm the general impression that wear is more rapid in Macauley Island Capra than Raoul Island goats, and somewhat more rapid in Raoul Island Capra than in Campbell Island Ovis. Variation in observed modal wear stages at each BEW is greatest for dp4 (the tooth position with the lowest crown height but greatest divergence in morphology between sheep and goats) and also large in its permanent replacement p4. The extent of tooth wear also varies between islands. Comparisons of dp4 at BEW 1 reveals a generally flatter occlusal surface in Macauley Island goats, and a flatter anterior cusp in Raoul Island goats compared with Campbell Island Ovis (Figures 6.2, 6.3 and 6.4). Note that Macauley Island goats shed dp4 at an earlier wear/eruption stage (BEW 2) than goats on Raoul Island or sheep on Campbell Island (BEW 2þ). This premature wearing out and shedding of dp4 is accompanied by more rapid wear on its replacement (p4). That is, at BEW 3 when m3 is in early wear (Payne stage 2), p4 is already at Payne stage 8 on Macauley Island, whereas p4 is at very early wear stages on Raoul Island (between Payne stages 1 and 3) and Campbell Island (Payne stage 2) (Table 6.7). At BEW 2, dp4 wear in Macauley and Raoul Island Capra is much advanced over wear in Campbell Island Ovis. First molar occlusal surface is flatter in Macauley Island goats at BEW 2 than either Raoul or Campbell Island ovicaprines (Figures 6.2, 6.3, and 6.4). At BEW 3, Macauley and Raoul Island Capra have flatter occlusal tables than Campbell Island Ovis. Comparing modal wear stages at all BEW stages (Figures 6.5 and 6.6), tooth wear is more advanced in goats from Macauley Island, less advanced in goats from Raoul Island, and least in sheep from Campbell Island. When the m1 is erupting into wear (BEW 1), dp4 is at a more advanced wear stage on Macauley Island (Payne stage 8) than on Raoul (Payne stage 7) or Campbell Island (Payne stage 5). When m2 is erupting into wear (BEW 2), both m1 and dp4 are at more advanced wear stages on Macauley Island (Payne stages 8 and 12, respectively) than on Raoul (Payne stages 7 and 9) and Campbell Island (Payne stages 7 and 7, respectively). When m3 is erupting into wear (BEW 3), all three tooth positions (m2, m1, and p4) are at higher stages of wear on Macauley Island (Payne stages 8, 9, 8) than on Raoul (7,8,3) or Campbell Island (6,8,2).

6.5.5 Discussion

With the limitations inherent to simple observation and a quick comparison of the stage of wear in ovicaprines at the same developmental stage of eruption and onset of wear, tooth wear is fastest on Macauley Island, intermediate on Raoul Island, and slowest on Campbell Island. As a reminder, on Macauley Island, a browser (Capra) grazes on a plateau grassland growing on unconsolidated tuffaceous soil. On Raoul Island, a browser (Capra) feeds on low vegetation in disturbed dense forest growing on tuffaceous soils exposed by landslides on the steep slopes of an active volcano. On Campbell Island, a grazer (Ovis) feeds in a tussock-grass low-shrubland growing on a thick organic peat soil with little to no exposed mineral soil (Table 6.8). 182 Crown height and tooth wear on islands

Table 6.6 Feral goat and sheep material from Campbell, Macauley, and Raoul Islands in museum or institution collections in New Zealand

Collection DSIR ledger number BEW m1 length (mm) dp4 m1 m2 m3

Campbell Te Papa 3230 1 15.56 5 2 Campbell Te Papa 3238 1 16.86 5 2 Campbell Te Papa 3248 1 14.87 5 2 Campbell Te Papa 3254 1 15.58 5 2 Campbell Te Papa 3254 1 16.91 5 2 Campbell Te Papa 3300 1 17.44 (est) 5 2 Campbell Te Papa 3313 1 16.59 5 2 Campbell Te Papa 3318 1 16.81 5 2 Campbell Te Papa 2868 1þ 16.43 6 2 Campbell Te Papa 3234 1þ 15.01 5 2 Campbell Te Papa 3246 1þ 16.38 6 4 Campbell Te Papa 3250 1þ 16.29 5 2þ Campbell Te Papa 3256 2 16.4 6 3þ Campbell Te Papa 2872 2þ 13.54 7 7 4 Campbell Te Papa 2874 2þ 14.56 8 8 4 Campbell Te Papa 3241 2þ 14.28 7 7 4 Campbell Te Papa 3278 2þ 16.01 7 3þ Campbell Te Papa 3281 2þ 15.84 7 4 Campbell Te Papa 3282 2þ 17.54 6 2þ Campbell Te Papa 3284 2þ 17.52 7 3 Campbell Te Papa 2891 3 13.46 8 7 2 Campbell Te Papa 2892 3 13.21 8 8 2 Campbell Te Papa 2893 3 15.05 8 7 1 Campbell Te Papa 2896 3 14.99 8 6 2 Campbell Te Papa 2897 3 14.19 8 7 2 Campbell Te Papa 2898 3 14.34 8 7 2 Campbell Te Papa 2905 3 12.71 8 7þ 2 Campbell Te Papa 2912 3 14.84 8 6 1 Campbell Te Papa 2894 3þ 15.79 8 6 3þ Macauley Te Papa 4326 1 na 7 2 Macauley Te Papa 4352 1 13.11 8 2 Macauley Te Papa 4284 1þ 14.28 12 7 Macauley Te Papa 4291 1þ 14.4 9 7 Macauley Te Papa 4318 1þ 13.98 12 7 Macauley Te Papa 4321 1þ 12 4 Macauley Te Papa 4337 1þ 14.81 11 7 Macauley Te Papa 4351 1þ 14.49 12 7 Macauley Te Papa 4267 2 14.3 12 8 2 Macauley Te Papa 4319 2 13.97 12 8 2 Macauley Te Papa 4347 2 12.94 11 8 2 Macauley Te Papa 4349 2 12.82 12 8 2 Macauley Te Papa 4353 2 13.86 12 8 2 Macauley Te Papa 4271 2þ 12.7 8 6 Macauley Te Papa 4308 2þ 12.22 11 8 4þ Macauley Te Papa 4273 3 11.3 8þ 82 Macauley Te Papa 4304 3 11.89 10 8 5 Macauley Te Papa 4306 3 11.45 10 8 2þ 6.5 Feral goats and sheep on islands 183

Table 6.6 (cont.)

Collection DSIR ledger number BEW m1 length (mm) dp4 m1 m2 m3

Macauley Te Papa 4314 3 10.54 9þ 84 Macauley Te Papa 4348 3 11.58 8 7 2 Macauley Te Papa 4281 3þ 11.64 8 8 4 Macauley Te Papa 4288 3þ 9.86 11 8 4 Macauley Te Papa 4300 3þ 11.61 9 8 4 Raoul Landcare N 0652 FS 1 5 Raoul Te Papa 754 1 na 1 Raoul Te Papa 840 1 na 5 1 Raoul Landcare N 0756 FS 1 13.76 7 2 Raoul Te Papa 813 1 13.43 7 2 Raoul Landcare N 0808 FS 1þ 12.71 7 2 Raoul Landcare N 0561 FS 2 14.53 6 4 Raoul Landcare N 0504 FS 2 14.27 9 7þ 2 Raoul Landcare N 0551 FS 2 15.31 7 6 1 Raoul Landcare N 0560 FS 2 14.29 7 7 1 Raoul Landcare N 0567 FS 2 13.97 7 7 2 Raoul Landcare N 0580 FS 2 14.4 7 7 2 Raoul Landcare N 0761 FS 2 12.73 9 7þ 2 Raoul Te Papa 764 2 12.97 5 7 2 Raoul Te Papa 777 2 12.64 7 7 2 Raoul Te Papa 873 2 13.57 12 8 2 Raoul Te Papa 735 or 755 2 14.13 12 7þ 1 Raoul Landcare N 0564 FS 2þ 14.35 11 7þ 2 Raoul Landcare N 0811 FS 2þ 13.68 7 7 2 Raoul Te Papa 783 2þ 13.41 br 7 2þ Raoul Te Papa 785 2þ 14.76 7 7 2 Raoul Te Papa 798 2þ 13.43 12 8 2 Raoul Te Papa 867 2þ 13.38 9 8 3þ Raoul Te Papa 877 2þ 15.31 br 7 2 Raoul Landcare 9 6523 3 13.94 8 6 2 Raoul Landcare N 0706 FS 3 12.31 8 6 2 Raoul Te Papa 751 3 13.17 8 6 2 Raoul Te Papa 773 3 11.58 8 7 2 Raoul Te Papa 791 3 13.12 8 7 1þ Raoul Te Papa 854 3 12.82 8 7 2 Raoul Te Papa 879 3 12.45 8 6 2 Raoul Landcare N 0569 FS 3þ 13.07 8 7 2 Raoul Landcare N 0753 FS 3þ 12.92 8 7 2 Raoul Landcare N 0810 FS 3þ 13.1 8 7 2 Raoul Te Papa 780 3þ 11.9 8 6 2 Raoul Te Papa 784 3þ 13.17 8 6 2 Raoul Te Papa 829 3þ 11.84 8 8 2

DSIR ledger numbers are the original collection numbers of the Department of Scientiﬁc and Industrial Research or Crown Research Institute; mandibular ﬁrst molar (m1) length (mm); Payne wear stages for dp4, m1, m2, and m3; Te Papa, Museum of New Zealand Te Papa Tongawera, Wellington; Landcare, Landcare, Lincoln; na, not available; br, broken. 184 Crown height and tooth wear on islands

Table 6.7 Mode and range of Payne (1973, 1987) wear stages for mandibular dp4 and permanent mandibular molars at comparable stages of eruption and incipient wear (BEW). Modal wear stage is the most common wear stage observed at each developmental BEW Stage.

BEW Raoul Macauley Campbell

1 dp4¼7 dp4¼7or8(7–8) dp4¼5 m1¼2 m1¼2 m1¼2 1þ dp4¼7 dp4¼12 (9–12) dp4¼5or6(5–6) m1¼2 m1¼7(4–7) m1¼2(2–4) 2 dp4¼7(5–12) dp4¼12 (11–12) dp4¼6 m1¼7(6–8) m1¼8 m1¼6 m2¼2(1–2) m2¼2 m2¼3 2þ dp4¼9(7–12) dp4¼11 dp4¼7(5–8) m1¼7(7–8) p4¼ne or 2 m1¼7(6–8) m2¼2(2–3) m1¼8 m2¼4(2–4) m2¼4(4–6) 3p4¼1–3(1–5) p4¼8(5–8) p4¼2(1–6) m1¼8 m1¼8or10(8–10) m1¼8 m2¼6(6–7) m2¼8(7–8) m2¼7(6–8) m3¼2(1–2) m3¼2(2–5) m3¼2(1–2) 3þ p4¼3or7(3–7) p4¼8 m1¼8 m1¼8 m1¼(8–11) m2 ¼ 6 m2¼7(6–8) m2¼8 m3 ¼ 3 m3¼2 m3¼4

ne, not erupted.

6.5.5.1 Raoul Island The Raoul Island goats appear to be wearing down their teeth quite fast. There are individuals with collapsed and failed dp4 and fully functional m1 when m2 is erupting and just entering into wear. The p4 is nowhere to be seen in the socket exposed beneath the structurally failed dp4, and had not formed before dp4 had been worn away. On one specimen, the m1 is beginning to fail (collapsing enamel) and the m3 is only at BEW 3þ with only apical wear on the cusps of the middle moiety. The Raoul Island goats have a flat or planar occlusal table (Figure 6.2), especially in adults where m3 is in complete occlusion. This is not so in the younger individuals, the teeth of which are just coming into wear, but is prevalent in the adults. In Raoul Island goats, a flat occlusal table is not an indication of open-country grazing, as the Raoul Island goats are not grazing in open country. It may be more a reflection and consequence of heavy soil ingestion by a browser living in a forest.

6.5.5.2 Macauley Island Macauley Island goats display the highest relative tooth wear among the three island populations compared here. This is evident by the higher modal wear stages of dp4, p4, m1, and m2 at comparable stages of dental eruption (Figure 6.7). Most signiﬁcantly, on Macauley Island, m1 is at Payne stage 8 when m2 is erupting, and at Payne stage 6.5 Feral goats and sheep on islands 185

Figure 6.5 The range and central tendency of Payne wear stages for mandibular tooth positions in populations of ovicaprines at the same developmental BEW stage from each island. Each column of plots corresponds to a tooth position (dp4 and p4, left column; m1, middle column; m2, right column). Developmental BEW stages are indicated on vertical axes; Payne (1987) wear stages as integers (vertical axis of each box plot). Box plots (Statview v5.0.1, SAS Institute, 1999) for Capra hircus on Macauley (M, middle) and Raoul Island (R, right), and Ovis aries from Campbell Island (C, left). 186 Crown height and tooth wear on islands

BEW stages dp4 m1 m2 m3

Macauley Island

1 8

12 8

9 8

Raoul Island

2 9 7

8 7

Campbell Island

1 5

2 77

8 6

Figure 6.6 Premolar and molar modal Payne tooth wear stages in Macauley (top panel), Raoul (middle), and Campbell (bottom) Island ovicaprines at comparable stages of dental eruption: (1) BEW 1, m1 erupting and entering into wear; (2) BEW 2, m2 erupting and beginning wear; and (3) BEW 3, m3 erupting and showing incipient wear. Modal Payne wear stages are indicated below each tooth (Payne, 1987). (Simpliﬁed tooth wear stages after Grant, 1982; with permission from the author.) 6.5 Feral goats and sheep on islands 187

Table 6.8 Features of erosion on Campbell, Raoul, and Macauley Islands

Variable Campbell Raoul Macauley

Lat/Long 52.566 S/169.15 E 29.266 S/177.919 E 30.233 S/178.433 E Area (km2) 113 29.38 3.06 Highest point (m), 570, even 516, irregular 238, even relief Seismicity low high high Volcanism Pliocene remnant Active stratovolcano Recently extinct remnant Vegetation Continuous dense tussock Continuous canopy Dense coarse Cyperus or grass shrubland subtropical moist forest Microlaena grassland Ungulate impact on Insigniﬁcant? Understory thinned Woody plants eliminated vegetation Relative phytolith High Low High concentration in ungulate diet Goat/sheep eradication 1987 1984 1970 completed Erosion Slow, limited to wave Occasional tropical Flat plateau grassland erosion of windward cliff; cyclone storm-induced thinning to bare ground, fresh slips; localized sheep slipping of steep slopes goat grazing grazing of caldera promoted by goat browsing Climate Windy, cool, moist, Subtropical, humid, Similar to Raoul cloudy, oceanic (station warm, oceanic (station data 1941–1970) data 1954–1990) MAT (C) 6.8 19.4 19.4 Annual Amplitude 4.7 5.4 5.4 MMT (C) Mean daily temp 4.7 - - range (C) MAP (mm) 1404 1558 1558 Raindays per annum 252 - - Surface winds 70% days > 7.5 m/s - - Soils/soil parent 95% organic peat 0.5–4m Andesitic pumiceous Unconsolidated material deep tuffs, low cohesion pumiceous tuff, low cohesion Soil moisture Consistently high Variable Variable EROSION RANK 3 1 2 Human habitation Occupied 1895–1931 Occupied 1800s–1937 Uninhabited References McGlone et al., 2007 Parkes, 1984a, b Barkla et al., 2008

9 when m3 is erupting, while on Raoul and Campbell Island, m1 wear is only at stage 7 (at m2 eruption) and stage 8 (when m3 erupts). Macauley Island goat m2 is at Payne stage 8 when m3 erupts, and only at stages 7 in Raoul Island goats and 6 in Campbell Island sheep. Rudge undertook a more detailed analysis of tooth wear and associated pathologies and made direct comparisons between the mandibles from Macauley Island and Figure 6.7 Four Capra hircus left mandibles from Macauley Island arranged in pseudoage/wear series from oldest (bottom) to youngest (top). First lower molar “trough effect” is seen in the youngest individual, and the largest and last tooth to wear out (m3) is seen in the oldest individual. To prolong the functional life of the dentition, positive natural selection for lengthening reproductive lifespan would include enhancing the mineral volume of m3 through increasing crown height or tooth size. 6.5 Feral goats and sheep on islands 189

mandibles from the North Island of New Zealand. A North Island population of feral goats was hunted between January 1966 and July 1968 in the Rimutaka Range, 20 miles east of Wellington (as reported by Rudge, 1969, see later). Of note, the “trough effect” (extreme tooth wear at p4 and m1, see Figure 6.7) observed on Macauley Island was not observed in the mainland population. Macauley Island jaws have extensive unequal wear along the whole mandibular tooth row, especially at p4 and m1. Rudge observed that “excessive wear on Macauley Island teeth is similar to that seen in sheep on coastal pastures affected by windblown sand, and reﬂects the highly abrasive action of the prevailing pumice substratum” (p. 265).

6.5.5.3 Campbell Island The teeth of domestic sheep (Ovis aries L.) recovered during eradication operations on Campbell Island are in excellent condition. The island surface is covered by soft peat, except on rock outcrops and there is little abrasive soil or dust. Sheep on the island graze on turf-type pasture of Poa litorosa (a tussock) and Chrysobactron rossi. The teeth become covered and stained by dark calcified material and the rumen contents consisted almost entirely (75%–90%) of grass with the remainder being fern. Plant phytolith concentrations are highest among grasses and palms, although the concentration of solid silica in grasses rarely exceeds 5% of plant DM (Hodson et al., 2005), even in experiments designed to boost the concentration. Phytolith concentrations in the genus Chionochloa on the main islands of New Zealand range between 0.72 and 7.02% by dry weight (Marx et al., 2004). Extreme values beyond this range occur on Campbell Island where Chionochloa antarctica grows on a thick organic peat soil and phytolith concentrations are low (0.61%) (Thorn, 2004), and at the other extreme, on the volcanic ash soils of Tongariro National Park, phytolith concentrations in Chionochloa rubra are high (8.85%) (Thorn, 2006). If grass phytoliths contributed to the observed differences in tooth wear on Macauley and Campbell Island, grasses on these two islands may have very different phytolith concentrations, given differences in soil silicon availability. Campbell Island sheep graze grass and one might expect to find flat meso-wear reflecting the abrasive demands of grass consumption in open country. The subjective impression I get from the collection, however, is that occlusal table relief actually steepens with wear and stays high throughout adulthood, perhaps reflecting a pattern of wear driven more by attrition, something that should be looked at in more detail. In 1970, over 1300 individuals were shot on Campbell Island, and over 1000 lower jaws were collected (Bell and Taylor, 1970). From this sample, 373 sets of incisors were selected at random and extracted, and 183 of these were used in a study of wear on the central incisors (Suckling and Rudge, 1977). At the time of eradication, it seemed surprising that no sheep had teeth worn to the gums. This is surprising because on the North Island of New Zealand practically all sheep incisors show signs of heavy wear. On Campbell Island “[t]he island’s surface is not covered with mineral soil but by soft peat...consequently there is little abrasive soil or dust. In any case, the vegetation is washed by rain on more than 300 days in the average year” (Suckling and Rudge, 1977, p. 145). In addition, on Campbell Island, lambs were born throughout the year, and most between August and December, an unusually long interval of lambing (Rudge, 1976). Lambing on Campbell Island was not tightly pulsed (oceanic climate minimizes 190 Crown height and tooth wear on islands

seasonal alternations of plant growth, cloudiness affects circadian entrainment, and animal breeding was unmanaged), unlike on the North Island of New Zealand, where seasonal peaks of soil ingestion and tooth wear coincide chronologically with the season of slowest vegetative growth, highest rainfall, and the increased energetic demands of pregnancy and lactation (see Chapter 4).

6.6 Conclusions

Tooth wear is least rapid on Campbell Island where Ovis grazes tussock grass growing on thick organic peat soil and where no soil minerals are exposed at the surface. In the absence of exposed mineral soil, there must be low soil ingestion. Although the phytolith content of the consumed grasses may be lower than grasses growing on mineral soil elsewhere, it is insufﬁcient to produce excess tooth wear, which is not in evidence among the thousand mandibles examined. By contrast, tooth wear is more rapid on Raoul Island where Capra browses on the slopes of an active volcano. Soil erosion occurs here by storm-induced landslides on steep slopes. This exposes soil in landslip scars that are sites of colonization by low plants. In addition, there are documented episodes of the deposition of volcanic ash onto leaf surfaces. Goats prefer the low pioneer plants that thrive on sun-lit landslip scars, and through their exploitation of these patches, slow natural plant succession and prolong soil erosion. Tooth wear is most rapid on Macauley Island where Capra grazes on low weeping rice grass (Microlaena stipoides) growing on pumiceous tuff soil that is exposed at the surface. While erosion on Macauley Island has not been described, high tooth wear suggests high levels of ingestion of exposed soil off the land surface. Climate conditions may be conducive to mineral particle resuspension by wind and rain onto grass leaf surfaces, especially events associated with subtropical cyclonic storms. The role of goat grazing behavior to soil disturbance is not known, but their direct action may have contributed to soil particle ingestion. Grazing behavior on Macauley Island, but not on Campbell Island, results in high wear. Differences in mineral soil ingestion might explain this difference. Browsing on Raoul Island can also result in high wear, but again, soil ingestion seems to be key here. Soil erosion through natural processes and goat foraging activity and volcanic eruptions are the known mechanisms whereby surface processes contribute to enhance soil mineral particle ingestion. Until a means for measuring soil ingestion from some trace element or isotope within the mineral substance of preserved teeth, or until the phytolith concentrations of the plants the animals fed on are measured, it will be impossible to be sure. Mike Rudge described two conspicuous examples of contrasting tooth wear in island populations of feral ungulates and offered pioneering explanations inspired by the general understanding about tooth wear in New Zealand sheep and the work of Bernard Healy and associates. Rudge went further, and expanded the role of soil ingestion to include a contribution from exposed soil and surface processes that contribute to soil erosion. The comparisons of ovicaprine tooth wear reported here only enhance the intrinsic interest of the results of the work of Mike Rudge. 7 The East African Plio-Pleistocene

7.1 Introduction

Tooth shape is the structural arrangement of mineral substance in teeth, principally enamel, that effectively delivers durable tooth mineral substances at the occlusal surface in a functionally useful conﬁguration throughout the reproductive life of the individual. Of the variety of structural expressions of tooth shape, the most familiar or conspicuous is crown height, or generally hypsodonty. However, many of the characters that impart functional longevity to teeth can be understood as contributions to the total effective volume of tooth mineral substance. Morphological characters that effectively increase tooth volume and thereby prolong functional life may include enamel thickness; megadontia (large tooth size in relation to body size); the number of cusps, cuspules, or pillars; enamel crenulation; increased complexity of occlusal pattern; the total area of enamel exposed on the occlusal table, increasing the relative size of the largest tooth; and total crown height. All of these different morphological contrivances represent solutions to the same general problem: resisting abrasive wear. There are other ways of prolonging tooth functional life that are unrelated to enamel volume. These include increased enamel hardness expressed by enamel microstructure, reduced occlusal relief whereby more enamel is exposed at the occlusal surface and brought into wear at the same time, increased total area of mineral substance exposed at the occlusal surface, delayed tooth replacement and eruption or increasing the temporal span of the replacement and eruption sequence relative to lifespan, delaying the onset of root formation and thereby prolonging tooth mineralization, the addition or deposition of an extra layer of external cementum over the crown, and increasing the rate of formation of tooth mineral substance. All these mechanisms increase the effective volume of tooth mineral substance or prolong the delivery of tooth mineral substance to the occlusal table. When evolutionary (or temporal) trends in multiple, phylogenetically independent lineages in the same geographic area document parallel and coincident change in structural features of tooth shape that increase the volume of enamel and other tooth mineral substances, suspicion arises that this may be in response to selection pressures operating through the general environment.

191 192 The East African Plio-Pleistocene

Glass is the primary constituent of volcanic ash and has a unique combination of attributes that contribute to its high abrasiveness. These include mineral hardness and environmental abundance, but importantly, also microvesicularity that maintains angularity during reduction and enhances its susceptibility to rapid wetting and drying and thus to erosion and ready mobilization by water and wind. Under certain conditions, accumulations of volcanic ash are easily detached, entrained, transported, and redeposited onto plants consumed by mammalian herbivores and ingested as contaminant abrasives. The ingestion of soil mineral abrasives derived from volcanic ash deposits varies at seasonal, interannual, and decadal timescales in accordance with temporal and geographic patterns of climate-induced erosion. In general, as soil erosion intensifies, so does the amount of ingested soil and tooth wear. Similarly, as soil erosion decreases, so does soil ingestion and tooth wear. As we have seen, at ecological timescales, the relationship between the intensity of erosion and the rate of tooth wear is direct. Presumably, this relationship operates at even longer timescales, including timescales that result in evolutionary change in tooth shape. Why should we expect this to be true? Soil erosion is an encompassing phenomenon and occurs everywhere on the earth’s surface, but often not perceived. Earth surface processes that generate mineral particle flux across the land surface and through the environment include surface disturbance, detachment or deflation, entrainment or mobilization, transport, reworking, and eventually final deposition. The intensity of soil erosion is expressed in the sediment record in basins both proximal and distal to sediment source areas. The intensity of erosion in source areas is measured as rates of soil loss, but is also reflected in rates of sediment deposition and mass accumulation in intermediate and sediment basins. Finally, the record of the intensity of surface erosion is found in the terrestrial sediments that ultimately accumulate on the sea-floor. The hypothesis that soil erosion contributes to drive the evolution of tooth shapes that prolong functional longevity predicts congruence between rates of erosion and rates of morphological evolution. The higher the rate of erosion, the higher the mineral particle flux through the environment, the higher become the soil loads on plants, rates of mineral particle ingestion, and rates of tooth wear. If sustained over evolutionary timescales, it can lead to higher rates of evolutionary response and change in tooth shape. To describe the relationship between intensity of earth surface processes that contribute to mineral particle flux, and rates of tooth shape evolution, we require: (1) an age- calibrated record of the terrestrial sediment input to the sea-floor record and an understanding of how this relates to surface conditions in the source area, and (2) an age- calibrated fossil record of tooth shape evolution in terrestrial herbivores that lived in or near the source area of the sediments. We expect to find geographically coherent temporal coincidence between changing rates of mineral particle flux and rates of morphological evolution of tooth shape. The Plio-Pleistocene of the East African rift system in Kenya and Ethiopia is probably the best-known and best-sampled fossil record on Earth. Today, the area of the Horn of Africa is a geographic source area of terrestrial sediments washing and blowing into the Gulf of Aden and beyond. A record of surface erosion off the East 7.1 Introduction 193

African rift system is preserved on the sea-floor of the Gulf of Aden (deep sea drilling project [DSDP] Site 231) and the Arabian Sea (ocean drilling program [ODP] Sites 721/722). The Plio-Pleistocene fossil record of the Turkana Basin and Ethiopian Rift includes early hominins and contemporaneous herbivorous mammals. The phylogeny and biostratigraphy of many of these mammals are sufficiently resolved to reveal continuously evolving monophyletic lineages and the morphological evolution of their teeth. While a broad relationship between climate change and human evolution seems unavoidable (DeMenocal, 1995), there has been considerable debate about the precise nature of the relationship. Understanding the causal pathway has consumed paleoanthropology for most of its history as a discipline (Vrba et al., 1995; Bobe et al., 2002; Bonnefille et al., 2004). Phyletic trends of morphological evolution in those features of teeth that serve to prolong their functional longevity (including tooth shape, tooth size, and enamel thickness) should respond to erosion intensity and change in mineral particle flux. In particular, this relationship should hold for australopithecines until the divergence of Homo from Australopithecus (including Paranthropus and Ardipithecus) and the acquisition and subsequent cultural spread of food processing technologies that reduce the ingestion of mineral abrasives. Dental evolution in Australopithecus can be described as a single general trend toward increasing the volume of enamel delivered to the occlusal table. The phyletic lineage extending from Ardipithecus through Australopithecus afarensis, A. aethiopicus, and terminating with Paranthropus boisei in East Africa lasted about three million years. Homo-like morphology emerges at 2.5–2.4 Ma, and subsequent to this initial appearance about 2 myr ago, two distinct genera of hominin, Homo and Paranthropus appear in the East African fossil record. During this time “hard, abrasive” items became increasingly important “as critical items in the diet” of Australo- pithecus (Teaford and Ungar, 2000). The proposition here is that there may be a role for earth surface processes in hominin tooth evolution. For this to be true, it requires that a portion of the mammalian fauna was responding to the same selective pressure as early hominins, albeit not precisely in the same ways. That is, bovids, papionins, and suids were evolving features to enhance tooth functional longevity at the same time as australopithecines because they occupied the same abrasive environment. If true, the proposition would offer a single explanation for much of mammalian dental evolution in the Plio-Pleistocene of East Africa, a single elegant proposition that leads to predictions that are easy to test definitively against the known record and future enhancements of the record. Would this explanation differ from past explanations? Invoking single unitary environmental causation is common in anthropology; for example, terrestrial habits, diet change, climate change, etc. What may be novel about the proposed explanation is not unitary agency, but rather that the agency is direct. That is, changes in the rate of soil erosion and mineral particle flux are predicted to relate directly to rates of evolution in features of dental morphology that serve to resist abrasive wear. In this way, it should be possible to relate global and regional measures of soil erosion, including the climate variables that drive variation in rates of erosion, directly to rates of evolutionary change 194 The East African Plio-Pleistocene

in fossil mammals (including australopithecines), without passing this relationship through more complex and intractable intermediate filters of “diet” or “vegetation.” It is not altogether surprising that such a simple agency has not been recognized before. It generally is known to have been “much dustier” during the Last Glacial Maximum than today, and eolian deposition rates at high latitudes were up to 20 times greater during glacial periods than today. During most of the Quaternary, dust deposition rates downwind of major source areas were up to 10 times greater than at present. Over the last 400 000 years, intervals of high atmospheric dust loading, high levels of dust input into ice cores and sea-floor sediments, were much longer than the relatively very brief and benign interglacial intervals like today. Glacial period conditions of greater “dustiness” were sustained over tens and even hundreds of thousands of years. Then too, on shorter timescales, the variation in atmospheric dust burden may have been even greater than average conditions during glacial times. Second, we generally understand volcanic activity in terms of our myopic infatuation with “catastrophic events,” rather than an appreciation of the relentless eolian transport of volcanic ash as atmospheric dust, its deposition and accumulation near source vents, its subsequent erosion and transport downwind and across the land surface, and its eventual repose on the sea-floor. These surface processes operate at timescales that are not part of our experience. We may witness a dust storm, and for a moment feel the grit between our teeth and wipe the dust from our eyes, but this experience is only momentary and transient. For animals that live and feed outdoors, and have no industry to wash the dust off their food, the grit between the teeth is much worse for wear. Beyond an inability to imagine the unimaginable, perhaps the most pernicious reason for the obscurity has been an insistence that “vegetation” and/or “diet” be reconstructed as the intermediary between the environment and dental morphology. Reconstructions of “vegetation” at fossil hominid localities during the Plio-Pleistocene are notoriously inconsistent (Wood and Strait, 2004), and it appears that nobody agrees on anything about paleovegetation. The same can be said about the reconstruction of “diet,” another endeavor plagued by a devotion to the physical properties of discrete items among the nutritious elements of food intake. Isotopic evidence suggests great dietary variability, even in the most morphologically “specialized” Paranthropus robustus (Sponheimer et al., 2006). What matters in this context is not what foods animals ate, nor the physical properties of the nutritious components of their diet, but rather the abrasives that were ingested. These abrasive mineral particles are sometimes intrinsic to the foods themselves, but more often they occur as contaminant grit that comes directly off the land surface. For dental evolution, what matters most about vegetation is not as a source of food nutrients or shade, or as a source of stable carbon isotopes, but how it influences rates of soil erosion through exposure of soil at the surface, the entrapment of soil mineral particles by plants, and soil load adhering to the surfaces of their edible parts. The proposition here requires neither the reconstruction of vegetation nor diet, but instead proposes a direct relationship between variation in the intensity of surface processes that drive erosion and the mobilization of soil mineral particles and evolutionary rates of morphological change in tooth structures that serve to resist abrasive wear. 7.2 The terrestrial fossil record 195

7.2 The terrestrial fossil record

That soil erosion might relate directly to the evolution of tooth structures that enhance functional longevity implies that the mechanism must hold true for mammals that lived together during the Plio-Pleistocene of East Africa, especially among terrestrial herbivores that fed close to the soil surface, such as Suidae and Theropithecus.

7.2.1 Suidae

Among the terrestrial mammals that fed close to the land surface during the Plio- Pleistocene of East Africa is Metridiochoerus, an advanced member of the clade Suinae. Metridiochoerus displays an evolutionary trend in the mandibular third molar of increasing crown height, crown lengthening through the addition of cusps (pillars), and elaboration of the cingulum (Figure 7.1) (Harris and White, 1979; Bishop, 2010).

Stable carbon isotope studies demonstrate a commitment to a C4 grass diet throughout the interval of interest (Harris and Cerling, 2002). Nyanzachoerus–Notochoerus is a second lineage of Suidae, the tooth evolution of which is examined here. Unlike Suinae such as Metridiochoerus, Tetraconodontinae (including Nyanzachoerus and Notochoerus) generally have thick enamel (Pickford, 2001; but see also Van der Made, 2004). Nyanzachoerus had simple bunodont third molars, but its descendant Notochoerus evolved increasing crown height and enlargement of the third molar (Figure 7.2) (Harris and White, 1979; Bishop, 2010). During this evolution, the stable carbon isotope record indicates a shift away from mixed feeding to a more grass-dominated diet (Harris and Cerling, 2002).

7.2.2 Theropithecus

Theropithecus, the gelada baboon and its nearest relatives, is characterized by reduced incisors and high-crowned/high-relief molars and were probably derived from a papio- nin ancestor sometime between 3.5 Ma and 4.0 Ma (Jablonski and Frost, 2010). Theropithecus brumpti and T. oswaldi are temporally successive species in the Turkana Basin, the former ranging in age from 3.5 Ma to 2.0 Ma, and the latter after 2.0 Ma (Leakey, 1993). In the Shungura Formation, the two species co-occur between Units E-3 and G-12, between approximately 2.4 Ma and 2.0 Ma. The oldest material of T. oswaldi comes from the Hadar Formation (about 3.9 Ma), the youngest material in East Africa comes from the Olorgesailie Formation (0.7 Ma) (Eck, 1993; Frost, 2010). The T. oswaldi lineage (T.o. darti, T.o. oswaldi, T.o. leakeyi) shows a progressive increase in body size along with an increase in the relative size of the posterior cheek teeth. T. oswaldi molars rapidly wear to a ﬂat occlusal plane. An evolutionary trend in dimininishing surface relief culminates in the latest “subspecies” T. oswaldi leakeyi. The continued evolution of more high-crowned and complex molars with additional clefts and fossae forming an intricate pattern of enamel ridges is “similar to adaptive complexes found in the molars of grazing mammals such as equids, 196 The East African Plio-Pleistocene

Phacochoerus aethiopicus

M. compactus M. hopwoodi

M. andrewsi III

M. modestus

M. andrewsi II

Metridiochoerus andrewsi I

Figure 7.1 Metridiochoerus, a well-supported clade of Suinae (Artiodactyla) with a paleospecies lineage extending from Metridiochoerus andrewsi through M. compactus. Dental evolution is characterized by the relative enlargement of m3 compared with other tooth positions, increasing m3 crown complexity, and crown height. (Figures of tooth morphology, clockwise from lower right, Figure 103, Figures 106 and 107, Figures 112 and 113 reversed, and Figures 118 reversed and 119, from Harris and White (1979), reprinted with permission from the American Philosophical Society.)

bovids, suids, elephantids, and microtines” (Leakey, 1993; p. 87). In addition, Leakey (1993) claimed that “delayed eruption of the molars, their oblique angle on eruption, and the reversed curve of Spee together provide a mechanism which increases the longevity of the molars” (p. 86). Grass rhizomes account for a good part of the grass intake of the living T. gelada (Dunbar and Bose, 1991). Stable carbon isotope results show Theropithecus to have

experienced an increase from about 65% to 80% C4 plants in its diet between 4 Ma and 1 Ma (Cerling et al., 2013). 7.2 The terrestrial fossil record 197

Not. scotti

Not. euilus

Not. capensis

Notochoerus jaegeri

Ny. kanamensis

Nyanzachoerus syrticus

Figure 7.2 The paleospecies lineage extending from Nyanzachoerus syrticus to Notochoerus jaegeri and N. scotti (Tetraconodontinae) characterized by a pattern of third lower molar evolution involving (1) crown elongation, (2) increasing cusp number through the addition of posterior cusps, (3) increases in crown height, and (4) m3 megadonty whereby the m3 crown enlarges relative to the other molars. (Figures of tooth morphology, from bottom to top, Figures 12 and 13, Figures 22 and 23, and Figures 51 and 52, from Harris and White (1979), reprinted with permission from the American Philosophical Society.)

7.2.3 Australopithecus

Many trends in dental evolution in Australopithecus can be understood as an increase in the functional longevity of the dentition. These trends include: (1) increasing molar enamel thickness (Beynon and Wood, 1986; Grine and Martin, 1988;Beynonetal., 1991),(2)increasingm3sizeinrelationtom1(Lucasetal.,1986), (3) increasing mandibular postcanine (p4–m3) area, (4) megadontia (McHenry, 1984a, b), and (5) the molarization of the premolars. All ﬁve postcanine trends serve to increase the total volume of enamel in the dentition and sustain the area of exposed enamel at the occlusal surface. The megadontia quotient of McHenry is postcanine tooth area in relation to body mass. As McHenry (1984a, b) showed, the phyletic series of australopithecines from Australopithecus anamensis to Paranthropus boisei show strong positive allometry 198 The East African Plio-Pleistocene

indicating increasing megadontia through time, whereas Homo from H. habilis to H. sapiens shows strong negative allometry or a reduction in the relative size of the postcanine teeth. The evolutionary trend in increasing megadontia has been extended to even earlier, from Ardipithecus ramidus through Australopithecus anamensis to A. afarensis (Lockwood et al., 2000; White et al., 2000). The molar tooth wear gradient in the earliest A. anamensis is very low; that is, the extent of ﬁrst molar, third molar, and premolar wear is essentially similar (KNM-KP 29283). By contrast, in P. boisei, the gradient is steep, suggesting that mandibular m1 wear is so rapid that it appears that m3 and p4 eruption occurs “late in life” or late in the functional lifespan of the m1 crown.

7.3 The record of soil erosion from source to sink

Terrigenous sedimentation has increased dramatically around the globe in the last five million years, especially in areas within and adjacent to mountains (Hay et al., 1988; Peizhen et al., 2001; Molnar, 2004). Crustal deformation creates elevated regional terrain and provides potential energy to rivers and glaciers, the main agents of erosion. In addition, continental margin subduction and hotspot activity are often associated with mountain building. The mountainous topography and active volcanism of the East African Rift system is attributed to the northward migration of the African plate over a giant mantle plume (Pik, 2011)(Figure 7.3). Climate controls the intensity of erosion in mountainous regions, often through the mechanism of the type and distribution of vegetation that impedes surface erosion. As both active and inactive mountain belts show accelerated erosion beginning three to four million years ago, change in climate rather than active mountain building has been implicated (Clark et al., 2006). Erosion rates were also accelerated in mountainous areas not influenced by glaciation, but still under the indirect influence of climate through the global hydrological budget. Plio-Pleistocene-age sea-floor sediments from ODP Sites 721 and 722 on Owen Ridge in the northern Arabian Sea and DSDP site 231 in the Gulf of Aden preserve a record of erosion through the windborne mineral dust that originated in the Ethiopian rift system and other source areas around the northern Arabian Sea. Sea-floor sedimentsatODPSites721and722,farfrom the surrounding continental margins and at intermediate depth, do not include a hemipelagic contribution. Instead, the allogenic terrestrial inorganic crystalline materials in these sediments are dust grains delivered by winds. The portion of this eolian dust that comes from the East African volcanic highlands includes volcanic glass shards (DeMenocal and Brown, 1999), air-fall tuffs (Feakins et al, 2007a), and clay minerals (smectite, palygorskite, and kaolinite) derived from weathered volcaniclastic soils in the rift system (Krissek and Clemens, 1991). The Turkana Basin and Ethiopian Rift System contribute to eolian dust flux to the northern Arabian Sea, and this contribution reflects the intensity, mode, and variability of surface processes in the source area. It also has a direct bearing on mammalian tooth B

A C

Red Sea

Site 721/ 722 Gulf of Aden

Flood Site 231 basalts

TurkanaTu Basin rk an a B as in C

Figure 7.3 Turkana Basin and Ethiopian Rift. Active volcanoes, the extent of plateau basalt surfaces, tracks of monsoonal winds, and DSDP/ODP Sites 231 and 721–722. Inset, top right (C), streamlines of the Turkana Low-Level Jet through the Turkana Basin (from Indeje et al. (2001), copyright American Meteorological Society, used with permission). Among the most intense winds in Africa, this summer monsoon wind, enhanced by channel effects, blows through the Turkana Basin, deflating fine-grained sediment delivered by the erosion of the surrounding volcanic uplands, and transporting this ash, dust, and pollen out over the Gulf of Aden and Arabian Sea, where it rains-out onto the sea surface and eventually drifts down through the water column to accumulate on the sea-floor. 200 The East African Plio-Pleistocene

evolution. The most detailed studies of the terrestrial component of the ODP 721 and 722 record were undertaken shortly after the cores were drilled and the initial scientific results were reported (Prell et al., 1989). The original studies focused on the most recent 800 000-year portion of the record. These studies fall into three broad categories: (1) determination of mass accumulation rate as an indicator of aridity in the source area (Clemens and Prell, 1991a, b), (2) the description of grain size as an indicator of transport energy or wind strength (Clemens and Prell, 1991a, b), and (3) the mineral and particle size composition of the dust to determine the geographic provenance more precisely (Krissek and Clemens, 1991). Somewhat later, the Gulf of Aden and Arabian Sea sediment records were extended back in time to document climate conditions in NE Africa throughout the entire Plio-Pleistocene (DeMenocal, 1995, 2004). Most recently, this work has also included biomarkers of vegetation (Feakins et al., 2007a) and microtephra for geochronology and correlation (Feakins et al., 2007b). The study of more complex interactions between the Arabian Sea floor sediments and climate were enabled by refinements in astronomical tuning (Trauth et al., 2005, 2009; Cleaveland and Herbert, 2007; Liu et al., 2008), all of which make this erosion record more meaningful to the fossil mammal record from the Turkana Basin and Ethiopia. During the Plio-Pleistocene, the Ethiopian rift to Arabian Sea sediment cascade operated through a combination of fluvial and eolian routing systems that continuously deposited a varied suite of fluviolacustrine and tuffaceous sediments in intermediate basins and windblown dust in more distant records (Prospero et al., 2002; Washington et al., 2003). The best source area sediment record of the fluvial portion of this cascade comes from the Turkana Basin (Cerling, 1986). Less is known of conditions around the volcanic source vents in the surrounding uplands and the monsoonal wind and erosion regime that mobilized these products into the sediment cascade (but see later). Elemen- tal and rare-earth compositions of the aerosol dust show that the volcanic source vents of tephra in the Turkana, Middle Awash, and Hadar areas were located within or adjacent to the central sector of the Main Ethiopian Rift (Hart et al., 1992). However, there has been no attempt to characterize surface conditions or estimate the mineral particle flux along this sediment cascade, and no attempt to characterize the surface and near-surface flux into and through the mammalian herbivore habitat. This task will not be easy.

7.3.1 Terrigenous sediments on the sea-ﬂoor

A smoothing function treatment of the record of terrestrial sediment delivery on the sea- floor (terrigenous percentage, sedimentation rates, lithogenic flux) at ODP 721/722 is a very crude indication of time-averaged erosion intensity or average atmospheric dust flux at ground level in the sediment source area. At orbital timescales, smoothing functions subsume contributions from both humid and aridland processes, plus their interactions. The ODP 721/722 record is crude in the spatial dimension as well; the terrestrial fraction is a composite record of many different minerals, each with distinct geographic origins and a distinct relationship to weathering and erosion. 7.3 The record of soil erosion from source to sink 201

The ODP 721/722 record of terrigenous dust flux from Owen Ridge in the NW Arabian Sea is based on whole-core magnetic susceptibility measured every 5 cm (or 1.2 kyr) and converted to percentage of terrigenous dust using a regression model based on a training set of both magnetic susceptibility and terrigenous percentage measurements (Bloemendal and DeMenocal, 1989; DeMenocal et al., 1991). Ten samples of ocean floor sediment were taken between 61 m and 90 m below the sea-floor at susceptibility peaks and troughs. The value for terrigenous percentage in each sample was calculated after sequentially removing calcium carbonate, opal, and organic carbon, leaving calcite, quartz, dolomite, and minor plagioclase. Clay mineral analyses were conducted on the terrigenous extraction residues, and smectite, palygorskite, illite, chlorite, and kaolinite were found to be the dominant minerals. The DeMenocal website [http://www.ldeo.columbia.edu/~peter/site/Data.html] provides the original data from ODP 721/722 in the following forms: (1) 4109 samples astronomically tuned with terrigenous percentage, linear sedimentation rate, and terrigenous dust flux (gm/cm2/kyr) calculated using a constant dry bulk density; (2) 358 samples analyzed for ash abundance back to 4.4721 Ma using glass shard counts and log transform values of these; and (3) raw susceptibility data for 4312 samples. Later, Trauth et al. (2009) rendered some of these data into a true time series, and using running tests computed for sliding windows of 100 data points, identified periods of significantly less dust flux and major and minor transitions to higher or lower dust flux (Trauth et al., 2009; Figure 7, bottom). Beyond the basics of data generation, there are at least three sources of complexity in this marine sediment record; temporal, spatial, and mineral particle size composition.

7.3.1.1 Temporal complexity The intensity of erosion varies across all timescales, and reconstructing surface processes over the Turkana Basin and NE African Rift system in the Plio-Pleistocene requires understanding something about NW Indian Ocean monsoon history and the operation of this sediment cascade today. Average annual fluxes at century and millennial timescales have been studied over the last eight thousand years of the record compared with satellite data for modern conditions. The average Holocene terrigenous accumulation rate on the Owen Ridge is about 0.4 gm/cm2/kyr (Clemens and Prell, 1990) and annual terrigenous influx estimated from sediment trap data today is 0.26 gm/cm2/kyr (Nair et al., 1989). Bloemendal and DeMenocal (1989) argued from satellite imagery and analyses of pollen and mineral aerosols over the Arabian Sea, that modern dust entrained during the summer monsoon originates in arid NE Africa and the Arabian peninsula. It is thought that dust transport occurs mainly during the boreal summer when NW winds loft dust off the Arabian peninsula and blow it off the Horn of Africa in the SW Asian monsoon (Clemens, 1998; Prospero et al., 2002). This monsoon circulation reverses during boreal winter, when the NE Asian monsoon begins to transport moisture onto the Horn of Africa and dust transport becomes neglible (Clemens, 1998). Longer-term dust records of the last one million years show that the mass accumulation rate of land-derived dust correlates positively with the marine oxygen isotope record of global ice volume, and is thought to reflect the influence of global climate on source area aridity and vegetation cover. Based on analysis of the terrigenous 202 The East African Plio-Pleistocene

(eolian) grain size record over the last 3.5 Ma at Site 722, Clemens et al. (1996) documented discrete shifts in the intensity and phase of the Indian monsoon. During glacial times, maximum deﬂation potential (the combination of maximum aridity and minimum vegetation cover) results in maximum dust transport (Krissek and Clemens, 1992). Eolian dust variations in the sediments document the onset of large amplitude regional aridity cycles closely linked to the development of high-latitude glacial cycles (Clemens and Prell, 1990, 1991a), and during glacial maxima, were three to ﬁve times higher than observed for interglacial periods (Bloemendal and DeMenocal, 1989).

7.3.1.2 Spatial (geographic) complexity In the lands surrounding the northern Arabian Sea, two distinct wind systems contribute to the dust record, the southwest monsoon winds and the northwest Shamal winds. Potential dust source areas include Rajasthan and Pakistan, Iran and the Persian Gulf, central Arabia, the Red Sea, and East Africa. The contribution to this dust from East Africa and the Red Sea can be distinguished from other source areas by some specific elemental enrichments such as Zr/Hf and Ti/Al (Sirocko, et al., 2000) that increase with intensification of the SW monsoon. Perhaps the purest signal of specifically East African geographic provenance is the volcanic ash that occurs as macrotephra, microtephra, and glass shards in the DSDP 231 and ODP 721/722 cores. Sarna-Wojcicki et al. (1985) described volcanic ash beds in the DSDP 231 in the Gulf of Aden. These tuffs are easily identified by their high Si content (35%), are mostly Pliocene age, and stem from explosive volcanism in the Turkana Basin and the Hadar region of the inner East African rift, 1000–2000 km away (Sirocko et al., 2000)(Figure 7.3). In addition, microscopic analysis of ODP Site 721 revealed 25 discrete horizons or eruption events (DeMenocal and Brown, 1999) and Feakins et al. (2007a) identified 68 microtephra in DSDP 231. Counts of volcanic ash shards (vesicular bubble wall fragments) describe significant variation in the amount of ash being incorporated into sea-floor sediments. Interestingly, there were relatively few levels (80 out of 357) with background shard counts of zero that indicate eolian input unrelated to either reworking or eruption events in East Africa. Eolian transport of ash was either relatively rapid following each eruption event, or absent during inactive intervals, perhaps reflecting the role of basalt surfaces on the speed of deflation. The implication of zero counts may also be that some long-term volcanic ash input into the Arabian Sea may have been scavenged by biological productivity. In DSDP Core 231 and the Turkana Basin there appear to have been major pulses of volcanic activity at: (1) 4.0–3.2 Ma, (2) about 2.75–2.25 Ma (or 2.5 Ma), and (3) between 1.7 Ma and 1.3 Ma (Feibel, 1999; Feakins et al., 2007a). The most recent pulse corresponds with high frequency of tephra in the Turkana and Konso Basins, where a trend of increasing frequency occurs in the southern Main Ethiopian Rift between 1.91 Ma and 1.4 Ma (WoldeGabriel et al., 2005). The third pulse in the Turkana Basin involved high-frequency, low-volume eruptions. As these tuffs are easily identified, and are not evident in the late Pleistocene and Holocene age portions of the sediment cores, it was concluded that the intensity of volcanism in this region decreased after the middle Pleistocene (Sirocko et al., 2000). 7.3 The record of soil erosion from source to sink 203

7.3.1.3 Complexity in mineral composition Krissek and Clemens (1991, 1992) identified mineral assemblages reflecting both arid and humid source conditions. Mass accumulation rates (MAR) measure the sum of all fine particle input, whether it is dust from continental sources or volcanic ash from a more specific source, or both. Bulk sediment MAR is calculated from linear sedimentation rates (LSR) (calculated from depth below the sea surface and an age model) and dry density, and take the form: MAR (gm/cm2/kyr) ¼ LSR (m/m.y) dry density (gm/cm3)/10 Total dust MAR and two of three arid assemblages (and minerals associated with these) are consistent with the marine isotopic record of global ice volume (maxima during glacial times), while by contrast, wind strength indicators exhibit maxima during interglacial or humid portions of these cycles (see later). The average Holocene terrestrial sediment accumulation rate on the Owen Ridge is about 0.4 gm/cm2/kyr (Clemens and Prell, 1990), and annual influx today, estimated from sediment trap data, is less; about 0.26 gm/cm2/kyr (Nair et al., 1989). ODP 722B dust MAR (gm/cm2/kyr) varies between just a trace (>0) and 4.0 over the last 800 000 years (Krissek and Clemens, 1992). Sun and An (2005) provide an MAR curve for ODP 722 extending between 3.6 Ma and today. On its own, marine MAR from the Arabian Sea may not be a very useful guide to terrestrial erosion intensity in NE Africa through the interval of most interest to mammal evolution. Is there an equivalent to marine sediment MAR for continental sediments in Rift Valley basins, and if so, how would they compare with sea-floor sediment MAR under the influence of the same regional erosion regime? Reconstruction of sediment supply is hampered by the incompleteness and discontinuity of the terrestrial record. This problemmaybepartlycircumventedbystudying mass accumulation rates in closed systems; that is, basins in which no sediment has bypassed the site of deposition over the time interval of interest, as for example, Cerling’s(1986) calculation of a mass balance for fluvial sediments in the paleo-Omo river system. These calculations assume that the paleo-Omo was a closed system and thus ignore eolian sediments that were blown out of the hydrographic basin. If there were no interaction between fluvial and eolian processes, a mass balance for fluvial sediments could be considered a closed system, but fluvial-eolian interaction must have been present. How then could a record of the eolian erosion of silt and finer terrestrial sediments and their transport by wind out of the paleo-Omo Basin be reconstructed?

7.3.2 From sea-floor to source area 7.3.2.1 Lithogenic flux Atmospheric dust flux is a variable of much interest in modern studies of fine-particle transport by wind (Table 7.1). In paleoceanography, atmospheric dust flux is estimated from the eolian input to sea-floor sediments, assuming there is little scavenging of mineral particles by plankton. As such, lithogenic flux in the DSDP/ODP cores 721/722 204 The East African Plio-Pleistocene

Table 7.1 Surface (/m2) and atmospheric (/m3) dust ﬂux in NE Africa and the Arabian Sea

Dust ﬂux or concentration Geography Source

1–1000 μg/m3 Range of long-term surface dust Ginoux et al., 2004. concentrations at the surface 10–100 μg/m2/s Small to moderate surface dust UPOS-BC3–05 SDF Model v.1 flux in desert regions (Hasselbarth et al., 2002) 500–2000 μg/m2/s Surface dust flux in dust storm UPOS-BC3–06 SDF Model v.1 conditions (Hasselbarth et al. 2002) 7–178 μg/m3 Range of atmospheric dust Pease et al., 1998 (sampled from a concentrations over NE Arabian moving ship, not fixed sampler, thus Sea in 1995, winter does not distinguish between stable dust-bearing winds and individual isolated air masses) 12–117 μg/m3 Range of atmospheric dust Pease et al., 1998 (mean¼50) concentration over NE Arabian Sea in 1995, spring 8 μg/m3 (mean) 1995 summer atmospheric dust Pease et al., 1998 concentration during SW monsoon 26 μg/m3 (mean) 1995 autumn atmospheric dust Pease et al., 1998 concentration 50 gm2/y May 1986 to Nov 1991 particle Ramaswamy and Nair, 1994 dust flux over Western Arabian Sea 27 gm2/y May 1986 to Nov 1991 particle Ramaswamy and Nair, 1994 dust flux over Central Arabian Sea 2.7–141.6 gm/m2/yr Modern eolian dust flux to Sirocko et al., 1991 in Mahowald [from 0.3–3.6 marine sediments in the et al., 1999. greater at LGM] northern Indian Ocean

sediment cores from the northern Arabian Sea may be a more useful proxy for atmospheric flux. Terrigenous sediment flux is calculated using a constant dry bulk density. The ODP 721/722 record has been expressed as dust flux (gm/cm2/kyr) extending back to 5 Ma (Trauth et al., 2009).

7.3.2.2 Surface winds Surface wind velocity in a sediment source area can be deduced (or estimated) directly from the grain-size of sea-ﬂoor sediments using a method developed by Parkin (1974). Sarnthein et al. (1981) provide an example of how this is done in the context of winds bringing eolian sediment from NW Africa into the marine sediments of the equatorial Atlantic. Similarly, relative wind intensity in the source areas around the northern Arabian Sea is reﬂected in the lithogenic grain size of ODP 722 sediments (Krissek and Clemens, 1992). 7.3 The record of soil erosion from source to sink 205

The mean characteristics of 18 diurnally variable nocturnal low-level jets around the world shows their core speeds to vary from 9.3 m/s to 18.9 m/s (Ethiopia 12.0; Australia 12.3; Great Plains 14.6) (Rife et al., 2010). The basic physiographic and thermal forcing mechanisms that give rise to nocturnal low-level jets give them an outsized effect and influence on the transport of dust over long distances in arid regions such as Ethiopia. Today, two low-level wind jets operate over East Africa: (1) the East African (or Somali or Findlater) low-level jet, and (2) the Turkana Channel jet. The first of these operates along the coast, from south to north, and because it is embedded in the Asian monsoon circulation, functions during the northern hemisphere summer. The second, the Turkana Channel jet has a southeasterly flow and persists throughout the year, with speeds exceeding 50 m/sec (Kinuthia and Asnani, 1982; Kinuthia, 1992; Indeje et al., 2001). Today, it is windy in Ethiopia, a mountainous country with highly erodible soils. Ethiopia has some of the highest erosion rates in the northern hemisphere of Africa and soil loss occurs at a rate of between 1.5 billion and 2 billion cubic meters (53–70 billion cubic feet) a year, with some 4 million hectares (about 10 million acres) of highlands considered irreversibly degraded. The current recorded annual soil erosion (surface soil movement) in Ethiopia ranges from a low of 16 t/ha/yr to a high of 300 t/ha/yr, depending mainly on slope, land cover (vegetation), and rainfall intensity. The World Resources Institute (1992) claims that highland Ethiopia loses 42 tons (soil)/ha/yr on cultivated land and 5 t/ha/yr on pasture (by comparison the loess plateau of China loses 251 t/ha/yr, and Nepal 70 t/ha/yr) (Hurni, 1990). Measured erosion rates in Ethiopia range between 5.33 mm/yr and 7.4 mm/yr (Mesfin, 1972; Hurni, 1985). By comparison, measured soil erosion rates in the circum-Mediterranean range from 0.0006 to 0.106 mm/yr (Kosmas, 1997); on the Loess Plateau of China, rates vary from 1.48 mm/yr to 7.4 mm/yr (Wen, 1993); and on the West African savanna, between 0.37 mm/yr and 3.7 mm/yr (Lal, 1993). Using a soil erosion model, annual soil erosion in highland NE Africa ranges between 0.005 mm/yr and >2 mm/yr (Zhang et al., 1998). The Lake Turkana Basin has the strongest winds in all of Kenya. These winds are generated by the Turkana Channel Jet stream, discovered in 1981 by Kinuthia of the Kenyan Meteorological Department (Figure 7.3). The Turkana Channel jet blows all year round, from the SE through the valley between the East African and the Ethiopian highlands, over the deserts in Sudan, and then turns eastward to the Arabian Sea. It is locally accelerated between Mt. Kulal (2300 m.a.s.l.) and the Mt. Nyiru Range (2750 m. a.s.l.). It is a nocturnal jet, in that the wind slows at midday, but is in full force at night. Average wind speed is 11 m/s, among the highest recorded in the world. The average wind speed of the Lake Turkana Channel jet is higher than the threshold velocity of fresh ash, and approaches the threshold velocity of consolidated and relic ash (Table 7.2). Erosion in the Lake Turkana Basin includes gully, rill, and stream bank erosion from rains in the surrounding uplands. Erosion products are routed by surface flows that lead down to the lake, where these fresh sediments are then deflated and lofted by these strong winds (Table 7.3). The deserts in the floor of the Turkana channel are at an elevation of 500 m.a.s.l. and are surrounded by volcanic highlands where maximum elevations reach 4000–5000 m. 206 The East African Plio-Pleistocene

Table 7.2 Average wind speed of Lake Turkana Channel Jet, wind erosion threshold friction velocities for fresh volcanic ash and relic deposits, and theoretical threshold friction velocities for small particles

Windspeed (m/s) Geography Source

11 m/s at 10 m.a.g.l. Lake Turkana Channel Jet Indeje et al., 2001 3.33 m/s at 2 m.a.g.l. Newly deposited fresh ash from Mt St Fowler and Helens, collected at Moses Lake, Lopushinsky, 1986 determined in wind tunnel 19.168 m/s at 2 m.a.g.l. Volcanic ash consolidated by wetting and Fowler and drying in wind tunnel Lopushinsky, 1986 15.4–21.8 m/s Gap winds resuspending Katmai relic ash Hadley et al., 2004 0.2–0.4 m/s Experimental samples of Grimsvötn and Cashman et al., 2013 at grain sizes 4–6 ϕ Eyjafjallajökull (Icelandic) ashes (16–64 μm) 0.2 m/s at grain size Theoretical Marticorena and ϕ¼4 Bergametti, 1995 0.2 m/s at grain size Theoretical for loose spherical particles on Shao and Lu, 2000 ϕ¼3 dry bare surface 0.1 m/s at grain size Theoretical for compact, rough, irregularly Goldasteh et al., 2012 ϕ¼3 shaped particles by turbulent ﬂow

1 m/s¼3.6 km/hr; m.a.g.l., meters above ground level.

Table 7.3 Erosion rates in the Turkana Basin and elsewhere in Ethiopia from Sundquist (2011), and others

Erosion rate Geography Source

16–300 t/ha/yr Total annual surface soil loss in Ethiopia Hawando, 1997 1 billion t/yr Total annual topsoil loss by rain in Ethiopia Brown, 2006 900 million t/yr Total annual topsoil ﬂow from Ethiopian Brown, 1978 (1978 US highlands AID mission) 45 195 t/km2/yr Annual soil erosion rate in Ethiopia Mahamed and Ram, 1987 44 100 t/km2/yr USLE estimated Vertisol erosion rate in Virgo and Munro, 1978 northern Ethiopia 22 050 t/km2/yr USLE estimated Cambisol erosion rate in Virgo and Munro, 1978 northern Ethiopia 3 billion t/yr Total annual soil loss rate for Ethiopian MacKenzie, 1987 highlands (Ministry of Agriculture) 1.5 billion t/yr Total annual soil loss rate for northern Tamene and Vlek, 2008 Ethiopian highlands 1.653–3.858 t/yr Sediment ﬂux through the Omo River Cerling, 1986 hydrographic basin, southern Ethiopian highlands

Wind streamline flow patterns show the Turkana jet to be a branch of the East African jet during the northern hemisphere summer. During that season, southeasterly flow divides around the Ethiopian highlands, with a western branch flowing through the Turkana channel, and the eastern branch flowing to the northeast parallel to the axis of 7.3 The record of soil erosion from source to sink 207

the eastern flank of the Ethiopian plateau. The wind speed of the Turkana jet accelerates where the channel narrows and decreases where the channel widens over Lake Turkana (Indeje, 2000; Indeje et al., 2001). These winds influence the distribution of tephra. Judging by the geographic distribution of tephra originating from volcanic centers in Kenya and Ethiopia, the Turkana Channel jet blocks most of the SW to NE transport of tephra across the Turkana Basin (Figure 7.3). How so? The correlation of tephra throughout East Africa has been a feature of late Cenozoic rift-valley volcanology, tephrostratigraphy, and geochronology for a long time. The geographically longest correlation of an East African tuff is certainly the discovery of tuff from the youngest Toba eruption, the YTT Tuff in Lake Malawi lake core, of Indonesian origin (Chorn, 2012). Within the East African rift system, many Turkana Basin tuffs (Silbo, Chari, Kale, B-Tulu Bor, Lokochot, Kokiselei, Wargolo, Lomogol, Malbe, KBS, Black Pumice, and Moiti) have been traced to the Middle Awash Valley, to Hadar, and to DSDP sites in the Gulf of Aden and beyond (Sarna- Wojcicki et al., 1985; Brown et al., 1992). Meanwhile, tuffs from farther south in Kenya and Tanzania cannot be traced north of the Turkana Basin. For example, neither Kanjera in the western rift of Kenya (Behrensmeyer et al., 1995), nor Kedong–Olorgesailie in the south Kenya rift (Baker and Mitchell, 1976), nor the Kapthurin Formation Bedded Tuff complex (Tryon and McBrearty, 2002), nor Olduvai (Pyle, 1999) can be chemically tied to the Turkana Basin and Ethiopian tephrostratigraphy. While there are some tuffs of similar age, geochemical identity has not been well established. For example, there are two tuffs at Olduvai in Kenya that are similar in age to tuffs in the Turkana Basin: Olduvai Tuff 1 (1.33 Ma) and Olduvai Tuff 1B (1.85 Ma). These two tuffs correspond in age to the Gele Tuff (1.33 Ma) in the Koobi Fora Formation and the Malbe Tuff (1.85 Ma) in the Shungura (as Tuff H-4), Nachukui, and Koobi Fora formations (Wood and Constantino, 2007). While these two tuffs provide important chronological tie points, they represent very few of the eruption events that characterize the Turkana Basin and Ethiopian sequences. There are a few other tuffs that may be traced across the Turkana Basin. The Kayampanga Tuff (UG90–1) from the Albertine Graben (the northernmost arm of the Western Rift) in Uganda was correlated to the Lokochot Tuff in the Turkana Basin, to Tuff A from the Shungura Formation, and beyond to a tuff from the Gulf of Aden (Pickford et al., 1991). In general, Gulf of Aden DSDP 231 microtephra composition- based correlations, with only one exception (the UG90–1 Tuff in Uganda), are made to Turkana Basin tuffs, and the age model for this marine core relies exclusively on temporal correlations to Silbo, Kokiselei, B-Tulu Bor, Lomogol, Wargolo, and Moiti tuffs, which have not been reported from south of the Turkana Basin (Brown et al., 1992; Feakins et al., 2007a). Does this pattern of geographic dispersal say anything about the volcanic source area of these tuffs or indicate that the Turkana Channel jet operated continuously for most of the Plio-Pleistocene? There are other exceptions to this pattern. Four blue-gray tuffs in the Chemeron Formation of the Baringo Basin in the Western Rift of Kenya have been identified chemically in the Turkana Basin: (1) the Lokochot Tuff (also known at Koobi Fora, the Nachukui Formation, and as Tuff A of the Shungura Formation), (2) the B-Tulu Bor 208 The East African Plio-Pleistocene

Tuff (known as Tuff B-b in the Shungura Formation and Nachukui Formation, and the Sidi Hakoma Tuff at Hadar), (3) the Lokalalei Tuff (known also at Nachukui and Koobi Fora Formations, and Tuff D of the Shungura Formation), and (4) BF91008 or the Suteijun Tuff also known from Kanapoi in the Turkana Basin (Namwamba, 1993; Uno et al., 2011). The mechanisms of tuff dispersal are not well characterized. Where encountered, these tephra may be water laid (brought by the paleo-Omo River or any of its affluents, for example) or air-fall, and the source volcanoes have not been identified in all cases. The source area of many of the distal pyroclastic deposits in sedimentary basins within the Ethiopian volcanic province have been identified using combined elemental and rare earth isotope signatures. These results show that tephra source areas for Turkana, Middle Awash, and Hadar tephra are within or adjacent to the central sector of the Main Ethiopian Rift (Hart et al., 1992), not volcanic centers farther south in Kenya, Uganda, or Tanzania, or anywhere else south of the Turkana Basin. There are two reasons why most of the tuffs in Rift Basin sediment sequences in Kenya and Tanzania south of the Turkana Basin may not be found in sequences in the Turkana Basin and Ethiopia. First, the wind systems are different. The Turkana jet flows through the channel of the Turkana Basin where it deflates fine-grained sediment (and ash) and blows it northeastward to the Gulf of Aden and Arabian Sea, while at the same time blocking the dispersal of ash from volcanoes erupting south of the Turkana Basin. Second, the Plio-Pleistocene volcanism of the Kenyan plateau and more southern parts of the rift system included flood lavas, basalts, and trachytes throughout the interval from 1.9 Ma to 0.8 Ma, and these lavas blanketed or covered the erodible sediments around the vents. By contrast, around Lake Turkana, flood basalt production ended around 4 Ma (Haileab et al., 2004), and subsequent tephra had their distribution influenced by the monsoon wind erosion regime. These Turkana and Ethiopian flood basalts provide a hard, relatively smooth, and impermeable surface that facilitates the entrainment by wind of ash- fall deposits and accumulations. The Turkana jet seasonally brings increased aridity to the Turkana Basin and it also entrains dust into the monsoon circulation that eventually gets transported over the Gulf of Aden and Arabian Sea. If this wind operated in the past as it does today, it would have provided a routing system for deflated fine-grained dust from East Africa into the monsoon winds that transport it over the northern Arabian Sea.

7.3.2.3 Volcanism and surface processes in northeast Africa In the northeast African Rift system, mountain uplift has produced complex topography and high relief (Pik, 2011), with a low semiarid Turkana Basin surrounded by humid mountain uplands and complex, mostly tree-less rift valley environments (Figure 7.3). The tectonism that drove the uplift and rifting was also accompanied by volcanism. Volcanism began in the middle Cenozoic (Rochette et al., 1998). Ethiopian volcanism during the Plio-Pleistocene was a mixed modality, and this bimodal basalt-rhyolitic volcanism began at approximately 7 Ma and continued into recent times (Chernet et al., 1998). It has included catastrophic eruptions (Le Turdu et al., 1999). 7.3 The record of soil erosion from source to sink 209

While they do not compare in scale with the large continental-scale deserts in area or contribution to total global atmospheric dust, volcanic highlands are important local source areas for atmospheric dust around the world. The valley of Mexico (Ventura and Norton, 2001), the altiplano and puna plateaus of the Central Andean volcanic zone (Prospero et al., 2002), the Cascade range and Columbia plateau in North America (Nammah et al., 1986; Busacca et al., 2001), and the volcanic mountains at the northwest end of the Wrangell–St Elias wilderness and Alaska Peninsula (Hadley et al., 2004) are all important local dust source areas. Within orogens, local dust source areas also occur in topographic lows characterized by arid basin floors with drying winds, episodic or monsoon rains, and prolonged seasonal drought. In such basins, relatively large surface areas of fresh sediment become exposed in stream catchments extending down from surrounding uplands, along channels, and in alluvial deltas and playa lakes. The Turkana Basin is one of these. The Turkana Basin is surrounded by the volcanic Ethiopian plateau to the north, and the Kenyan plateau to the south, and is topographically low and arid. Active volcanism occurs within the basin as well as in the surrounding highlands (WoldeGabriel et al., 2000). Part of the reason volcanically active areas in high plateaus surrounding topographic lows are important dust source areas relates to the erodibility of the pyroclastic ash deposits and ash-derived soils exposed on the land surface. Volcanic ash is a unique soil parent material (Leamy, 1984). When contrasted with other soil orders, volcanic ash soils (andisols or andosols) are generally more highly susceptible to erosion (Dangler and El-Swaify, 1976). When composed of non-welded and incohesive glass particles and fine-grained minerals, andisols (or andosols) and ash deposits are more susceptible to weathering than crystalline sedimentary minerals. Volcanic ash is low density and volcanic ash soils have pore-sized properties very different from normal crystalline mineral soils; these include larger total porosity and broader pore size distributions. These properties imply high water retention, good drainage, and high nutrient availability where precipitation is adequate. In semiarid and arid climates, these same properties make volcanic ash soils more susceptible to rapid evaporation and soil moisture loss, surface disturbance, and erosion (Ugolini and Zasoski, 1979; Shoji et al., 1993). The modern distribution of volcanic ash soils has been described and mapped (Frei, 1978; FAO, 1997), but the isopach thickness of modern andisol parent material, relic ash, and older pyroclastic accumulations has not been mapped. In Ethiopia, andosols are mapped only within the central or main rift valley around lakes Koka, Zway, Abijatta, Langano, and Shala, and the active volcanoes of Fentale, Kone, and Tullu Moje (Batjes, 1997; FAO 1997; Berhanu et al., 2013). The vegetation cover in the Turkana depression is nearly nonexistent, whereas by contrast, the vegetation cover in the Ethopian highlands is much more significant (Beyene, 2010). Although less than 3% of Ethiopia is covered with trees today, 40% was forested a century ago. Ethiopian andosols or vitric derivative soils (FAO, 2001) support diverse open woodland and forest vegetation today. Across the Main Ethiopian Rift from the area of mapped andosols and into the Bale Mountains, forests or woodlands vary with increasing altitude from Acacia-savanna on foot-slopes at 1900 210 The East African Plio-Pleistocene

m, Juniper–Podocarpus-dominated forest at 2300 m, highland savanna plain at 2700 m, Hypericum-forest at 2900 m in volcano mid-slopes, and Erica shrub-dominated vegetation at 3200 m (Fritzsche et al., 2007). Late Pleistocene and Holocene pollen histories recovered in lake sediment cores show that these forests are all sensitive to water balance (Umer et al., 2007), and highland vegetation is known to have changed dramatically along with lake levels (Bonnefille and Mohammed, 1994; Mohammed and Bonnefille, 1998). Another feature of these East African dust source areas is that much of the surface of the Ethiopian plateau (600 000–750 000 km2) and floor of the Turkana Basin is covered by basalt flows (Mohr, 1983). These widespread lava flows form a hard, relatively smooth surface, off which sediments are easily deflated. Volcanic eruptions in the rift valley loft ash into the atmosphere and it settles on the basalt surfaces of the surrounding plateaus. Off these surfaces, rains and seasonal surface and channel winds associated with the monsoon entrain and mobilize it into rivers and eventually the atmosphere. Rivers draining these upland plateaus (like the Omo) carry some of the ash into the Turkana Basin, and the atmosphere transports some of it. The role of basalt surfaces on the susceptibility of subsequent ash-fall deposits to deflation by wind is notorious in other parts of the globe, in particular, Patagonia. Where these lava surfaces are roughened, they also trap windblown sediment often sufficient to support sparse grasses grazed by mammalian herbivores. Of the dust source areas around the Northern Arabian Sea and Gulf of Aden, those of Arabia (southern Oman and the Saudi border) and SW Asia (coastal Baluchistan and the Makran coast of SE Iran and Pakistan) are probably the most important contributions in terms of their volume (Pease et al., 1998; Prospero et al., 2002; Washington et al., 2003). However, the Horn of Africa contributes as an important dust source area. Bloemendal and DeMenocal (1989) argued from satellite imagery and analyses of pollen and mineral aerosols over the Arabian Sea that modern dust entrained during the summer monsoon originates in arid NE Africa and the Arabian peninsula. More significantly for tooth evolution, the Central Ethiopian plateau is the geographic source area for the volcanic ash beds in Plio-Pleistocene sediments in the Afar region and Turkana depression (Hart et al., 1992), and the volcanigenic sediment portion of the DSDP 231 and ODP 721/722 cores (Sarna-Wojcicki et al., 1985; Feakins et al., 2007b). The Turkana region is one of the harshest and least productive areas of East Africa. It is characterized by extreme heat and wind, aridity, and periodic drought. Rainfall and aridity are controlled by the thermal and dynamic stability of the two monsoons, called the Indian Ocean dipole (Nicholson, 1996). Aridity on the floor of the Turkana Basin is enhanced by the low-level Turkana jet. These winds also control the spatial and temporal variability of rainfall over Ethiopia (Riddle and Cook, 2008; Viste and Sorteberg, 2013; Zeleke et al., 2013). Today, geomorphic processes of fluvial gullying dominate in the highlands and wind erosion dominates down in the Rift Valley and change in land-cover influences both these processes (Nyssen et al., 2004). The Turkana Basin today supports almost no vegetation or is only thinly vegetated (Beyene, 2010) and the climate is semiarid to arid. Yet along the Omo River, there is lush vegetation year-round. The explanation for this 7.4 Data analysis 211

local contrast relates to the high relief (relief in this part of Ethiopia goes from 500 m to 4200 m), rainfall in the Ethiopian highlands delivering permanent water in the Omo River, and the otherwise very dry and windy conditions in the bottom of the Turkana depression. The Omo River drains the highlands, and flows into the lake at the bottom of the depression. The soils in this part of Ethiopia are derivatives of tephric or glass- rich parent material, and the sediments in the Omo River Delta and north Turkana Basin are derived from the basalt flows and rhyolitic tephra of the Ethiopian plateau (Yuretich, 1979). During much of the temporal interval that the windborne terrestrial sediments of DSDP/ODP cores 231 and 721/722 were accumulating downwind, fluvial deposits of the Omo Group were accumulating downstream in the Turkana depression. Basin deposition began with a brief pulse of basalt production that ended at 3.94 Ma (Hart et al., 1989; Haileab et al., 2004). Subsequently, approximately 700 m of fluviolacustrine sediment accumulated in the Turkana Basin, including the Omo Group and its component formations (Mursi, Shungura, Nkalabong, Koobi Fora, Nachukui, and Usno). These sediments were deposited in a single sedimentary basin or set of closely related sub-basins. Cerling (1986) estimated sediment input to Lake Turkana from erosion off 73 000 km2 of the Ethiopian highland surface drained by the Omo River (between 10 and 35 1012 gm/yr), and speculated that this may have been true for the last few million years. This is relatively high compared with modern local flux rates and rates in modern rivers around the world. Erosion rates in tectonically active regions are high, but even higher where tectonism is accompanied by volcanism. Short-term erosion rates (sediment yield) are up to two orders of magnitude higher for rivers draining areas of active volcanism (Koppes and Montgomery, 2009).

7.4 Data analysis

7.4.1 Method 7.4.1.1 Erosion rates from the marine record The percentage of terrestrial sediment in samples from age-calibrated DSDP/ODP Cores 721 and 722 is argued here to proxy Plio-Pleistocene erosion rate variation in the sediment source area. Terrestrial sediment input to the Arabian Sea ﬂoor at Sites 721 and 722 is windborne dust. Particulates include volcanic glass shards and tuff layers tied to volcanic sources in the East African Rift system. While not all the terrestrial sediment exported from the land surface to the Arabian Sea originates from northeast Africa, the pyroclastic contribution can only have been sourced from the zone of active volcanism of the East Africa Rift system and this contribution was continuous throughout the Plio-Pleistocene. In general, the terrestrial sediment in these cores has a regional source in the northern part of the circum-Arabian Sea and represents time-averaged sediment accumulation. The sediments were sampled at intervals suitable for the study of climate-induced variation at orbital timescales, and so provide a record of time- averaged erosion intensity at evolutionary timescales. 212 The East African Plio-Pleistocene

The original astronomically tuned data was captured from the DeMenocal website (http://www.ldeo.columbia.edu/~peter/site/Data.html) and the shorter timescale variation was effectively removed using the smoothing function utility of JMP (v3.2.1). With no a priori expectation about which smoothing function would capture evolutionarily meaningful variation in erosion rates, the data were explored using cubic spline smoothing at a variety of lambda values (Table 7.4; see Figure 7.4 for a depiction of the smoothing function curves for the terrestrial percentage record between 4.5 Ma and 0 Ma at ODP sites 721 and 722).

Table 7.4 Smoothing spline lambda (λ) values for the East African Time Series

Sum of Lambda (λ) R-square square error

Theropithecus oswaldi std log m3 area 0.000067 0.514424 52.44216 Most flexible 0.01 0.431769 61.369 Straight line 0.000001 0.546494 48.97861 164816.2 0.366941 68.37042 Australopithecus std log m3 area 0.000406 0.818439 7.62556 Most flexible 0.01 0.783333 9.100002 Straight line 3.327e-6 0.878987 5.082552 3326596 0.746127 10.662596 Notochoerus–Nyanzachoerus std log m3 area 0.090573 0.25758 131.4084 Most flexible 0.01 0.312101 121.7582 Straight line 0.000001 0.384857 108.8804 164816.2 0.209997 139.8306 Metridiochoerus std log m3 area 0.000223 0.501621 33.88977 Most flexible 0.01 0.468011 36.17524 Straight line 0.000001 0.525917 32.23761 548277 0.433553 38.51837 Terrigenous % (orbitally tuned) 548277 0.393478 77513.56 1 0.149223 121646.7 0.01 0.27927 103052.2 0.001 0.34993 92948.98 Terr (lithogenic) flux (gm/cm2/ka) 300607.6 0.559278 172.549 1 0.218393 322.7565 0.01 0.366986 261.3967 0.001 0.476368 216.2285 Sedimentation rate 3326596 0.5626596 1338.311 1 0.315938 2146.438 0.01 0.488627 1604.577 0.001 0.62106 1189.031 log ash abundance 1.824e-6 0.753005 26.84815 1 0.128997 111.967 0.01 0.230482 98.92115 0.001 0.345307 84.16044 7.4 Data analysis 213

7.4.1.2 Evolutionary rates in the terrestrial record Tooth size data have been compiled for four evolving lineages of terrestrial mammals characterized by tooth shape evolution in crown structures plausibly related to prolonging tooth functional longevity under high abrasion. The four lineages are: (1) Metridiochoerus andrewsi I, II and III–M. compactus (Suidae), (2) Nyanzachoerus devauxi–N. syrticus–N. pattersoni–Notochoerus jaegeri–N. scotti (Suidae), (3) Theropithecus oswaldi darti–T. o. oswaldi–T. o. leakeyi (Cercopithecidae), and (4) Ardipithecus ramidus–Australopithecus anamensis–A. afarensis–A. aethiopicus–Paranthropus boisei (Hominidae) (Table 7.5). Each lineage represents a continuously evolving lineage or sequence of paleospecies supported by phylogenetic analysis and biostratigraphy. For the analysis, fossil material of the two suid lineages was examined. This material was restricted to intervals of time between 0 Ma and 4.5 Ma and geographically to Turkana Basin localities of Nachukui, Koobi Fora, Kanapoi, Lothagam and Omo, and Ethiopian localities including Hadar. The Nyanzachoerus–Notochoerus lineage is represented by 178 specimens extending in age between 4.22 Ma and 2.13 Ma, and the Metridiochoerus lineage by 69 specimens ranging in age from 3.3 Ma to 1.43 Ma (measurements kindly provided by Rebecca Cuddahee). The phylogenetics of these two suid paleospecies lineages follow Harris and White (1979), and the geochronology follows Bobe and Eck (2001) and Bobe et al. (2002). Theropithecus oswaldi (with three chronospecies or subspecies: T. o. darti, T. o. oswaldi, and T. o. leakeyi) is essentially a single anagenetic lineage. Measurements of mandibular m3 length and breadth were taken from Eck (1977), Frost (2001), and Jablonski and Leakey (2008). To avoid conﬂating evolutionary trends in T. oswaldi and T. brumpti, tooth size measurements from the interval of temporal overlap of these two species were excluded from the analysis. Only patterns in the T. oswaldi lineage during one segment of its anagenetic trend are examined here. This is the segment between 3.42 Ma and 2.41 Ma before the interval of temporal overlap with T. brumpti. The Australopithecus lineage used in the analysis extends thus: Ardipithecus ramidus–Australopithecus anamensis–A. afarensis–unassigned material from the Tur- kana Basin–Australopithecus (or Paranthropus) ethiopicus–Paranthropus boisei, and

Table 7.5 Sample sizes and age range of Turkana Basin and Ethiopian Plio-Pleistocene mammals

Taxon/lineage (localities) N Age range (Ma) Specimens/myr

Metridiochoerus 69 1.43–3.3 36.9 (Nachukui, Koobi Fora, Omo) Nyanzachoerus–Notochoerus 178 2.13–4.22 85.2 (Nachukui, Lothagam?, Koobi Fora, Hadar, Kanapoi, Ethiopia) Australopithecus (Middle Awash, Lower Omo, 43 1.43–4.4 14.5 Hadar, Dikika, Laetoli, West Turkana, Kanapoi, Koobi Fora) Theropithecus 109 2.41–3.42 107.9 (Omo, Koobi Fora, Hadar) 214 The East African Plio-Pleistocene

60 Lambda = 1 Lambda = 0.1 Lambda = 0.01 Lambda = 0.001 50

10 ODP Sites 721–772 % terrigenous

0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 4.5 Age (Ma)

Figure 7.4 The percentage of terrigenous sediment on the sea-ﬂoor at ODP Sites 721–722 on Owen Ridge in the Arabian Sea, with smoothing spline functions that capture long-term average ﬂuctuations in the intensity of soil erosion in the source areas around the Arabian Sea (http://www.ldeo.columbia.edu/~peter/site/Data.html).

is based on published material collected in basins within the East African rift system (including the middle Awash, Hadar, Dikika, Konso, and the Omo Basin in Ethiopia; West Turkana, Allia Bay, Kanapoi, and Koobi Fora in Kenya; and Laetoli and Olduvai in Tanzania) within the age range from 4.4 Ma to 1.42 Ma. (For an excellent recent review of the evidence for and against this anagenetic lineage, see Wood and Leakey, 2011.) This dataset includes measurements taken from the literature for 274 specimens, of which 43 include complete m3, of which 35 are used in this analysis (measurements kindly provided by Steve Churchill). While the bulk of the evidence for australopithecine evolution comes from the Turkana Basin, some of the data for australopithecines used here come from Laetoli and Olduvai, localities that are south of the Turkana Basin. The basic data are linear measures of m3 shape or area; that is, simple linear tooth length and width, and tooth area (length width), standard tooth crown measurements from the published literature or unpublished datasets made available to me by generous and curious researchers. Only m3 size is used in the analysis. This tooth, the largest and last molar to erupt, would be the tooth position most likely targeted by natural selection to increase the functional longevity of the dentition. Raw measures of m3 area in mm2 were transformed into z-scores or standardized log transformed m3 area to minimize the effects of outliers and body size differences on the comparisons.

7.4.1.3 Analysis On bivariate plots of the standardized natural log (ln) of m3 area on time, smoothing splines were ﬁt at various lambda values to provide a continuous record of time- averaged predicted m3 area. Such rendering makes these terrestrial records of evolutionary change visually comparable to the record of soil erosion intensity in sea-ﬂoor 7.4 Data analysis 215

sediments. There is considerable variation in both erosion and tooth shape records, and a cubic smoothing spline interpolates values into the temporal gaps between marine sediment samples and land mammal fossil-bearing levels. While smoothing splines are a method of interpolation that usually connect actual data points, the scatter in the data influences the shape of the curve. For the terrestrial fossil record, individual specimens of intermediate age between especially rich levels influence the shape of the curve. However, smoothing is used to simplify the data and facilitate comparison between two quite different kinds of data (cause and effect, as it were). Conventionally, the sea-floor sediment record comprises environmental dependent variables and the record of tooth shape evolution comprises the response or independent variable (Table 7.4). There are very important differences in how fossil teeth and sea-floor sediments are sampled. The environmental variables were sampled at uniform intervals along a marine sediment core recovered from the floor of the Arabian Sea. It is a downwind record of environmental conditions in the source area expressed as the terrigenous percentage, sedimentation rate, lithogenic flux, and volcanic ash shard counts. Percentage of terrigenous is the percentage of sediment of terrestrial origin in the total mass of each sample. All four variables from the marine sediment record have a lot of noise. That is, there is a lot of data and the underlying processes are highly variable. This is because erosion occurs at all timescales: seasonal, interannual, decadal, centenary, millenial, and orbital (among others). This “noise” is real and reflects the behavior of earth surface processes. As the resolution of the sampling reaches limits in its ability to resolve shorter timescale cycles, distinguishing between noise and cycles becomes more difficult. The smoothing splines fit to terrigenous percentage and lithogenic flux reveal the orbital timescale variation in average long-term erosion. Volcanic ash shard counts respond to two different processes, eruption and erosion, and only the erosion fraction might be expected to vary at orbital timescales. Thus, the orbital signal in ash shard counts is not as obvious as eruption intensity and frequency obey other laws of nature. Linear sedimentation rates might be expected to co-vary with both lithogenic flux and productivity (also see later). I assume that the terrestrial sediments in the marine cores document erosion of the land surface; that is, the deflation, entrainment, transport, and deposition of dust blown off the land surface in the area the animals inhabited. Each sample of sediment represents a unique point in time, whereas one or many fossil teeth may be found in a single stratum, and therefore, not every tooth can be assigned to a unique age in the timescale. In addition, the temporal interval between fossil teeth is variable and the sample size and temporal continuity of the record of tooth shape evolution for each mammal species is different. While fossil teeth document evolutionary change and are presumably sampled from individuals that were part of an evolving lineage, fossil preservation and discovery are unpredictable, and the fossil record is relatively discontinuous and irregular.

7.4.1.4 Smoothing splines and time series analysis Smoothing splines have been ﬁt to both the sediment record and the tooth size record (Table 7.4), and the stiffness of the splines is adjusted in order to “reveal” or “discover” similar shaped curves. Smoothing splines impose a conﬁguration on the data, and in effect 216 The East African Plio-Pleistocene

they filter the data, simplifying noise and revealing average or long-term trends. Smoothing splines are “running averages” that track the central tendency in both the records of erosion and evolutionary response to erosion (tooth shape or crown surface area). The smoothing splines first fit to the four fossil mammal records are of comparable flexibility (lambda¼0.01), but higher temporal resolution can be obtained by changing the flexibility. While this captures more of the variation in evolutionary rates, it also reflects the influence of sampling density on evolutionary rates, and how the influence of these two is distinguished becomes an important issue. Smoothing splines vary in smoothness according to a running parameter lambda (l). As the value of lambda decreases, the error term has more weight and the fit becomes more flexible. The shape of the spline reflects the expected values of the distribution of y through time (x). Values of lambda can be adjusted until the form of the spline approximates the form of another spline that theory suggests might be in a direct or causal relationship. R2 measures the proportion of variation accounted for by the spline model. The sum of square error is the sum of squared distances from each point to the fitted spline, and is the unexplained or residual error after fitting the model. For true time series data, each value of a variable has a unique time or age. Fossil mammal occurrences, such as for Theropithecus oswaldi, are not true time series data, as each time slice has one or multiple values of m3 crown area, each value being individual specimens collected at the same stratigraphic level. In the case of m3 crown area, the spline is fit to a central tendency for the specimens (or measurements) collected at that stratigraphic level or time slice. This is analogous to the oxygen isotope results from tooth enamel when plotted against the oxygen isotope curve for Southern Ocean DSDP/ODP cores (Kohn et al., 2010).

7.4.2 Results 7.4.2.1 Metridiochoerus The Metridiochoerus tooth evolution record is very sparse before about 2.3 Ma, but between 2.3 Ma and 1.4 Ma, m3 tooth size evolution increases monotonically. The interval of steadily increasing m3 tooth size coincides with a large peak in the terrigenous percentage record from DSDP-ODP 722 (Figure 7.5). The monotonic trend of directional evolution extends in duration beyond the peak of terrestrial sediment input, and this trend continues to about 1.4 Ma without showing any change in slope.

7.4.2.2 Nyanzachoerus–Notochoerus Third lower molar tooth size evolution in the Nyanzachoerus–Notochoerus scotti lineage is documented through a much longer interval than Metridiochoerus. What we observe could also be described as a continuous monotonic trend extending from 4.25 Ma to 2.1 Ma. A smoothing spline ﬁt to the data reveals some apparent change in evolutionary rates that might be described as pulses of directional evolution punctuated by intervals of evolutionary stasis. Within the long-term trend, there is an interval of increasing tooth size beginning about 4.1 Ma and ending about 3.8 Ma, and another from about 3.3–3.2 Ma, followed by a much more gradual increase in m3 tooth size 7.4 Data analysis 217

0.5 m3 occlusal 0

-0.5 Accelerated

surface area (z-score) directional evolution -

Metridiochoerus 1

Metridiochoerus andrewsi I, II, III and Metridiochoerus compactus

25 (% terrigenous)

ODP Sites 712–772 Change in erosion intensity/dust flux regime 20

1 1.52 2.53 3.5 Age (Ma)

Figure 7.5 Evolutionary trend of increasing m3 crown area in Metridiochoerus (Suinae, Artiodactyla) through time and long-term average erosion intensity from the sea-floor record. The evolutionary trend began at a time of change in the erosion regime triggered by orbital controls on climate. beginning sometime after about 2.5 Ma (Figure 7.6). Between these three intervals of directional evolutionary change in m3 crown size, the rate of evolutionary change appears to slow or remain constant. Matching the chronology of pulses of increasing evolutionary rates are three intervals of increased delivery of terrestrial sediment to the marine sea-floor record. No body of theory has yet been proposed that provides an expectation of what we ought to see in a relationship between soil erosion and mammal tooth evolution. In the Nyanzachoerus–Notochoerus scotti lineage, we might be seeing periods of directional evolution alternating with periods of relative evolutionary stasis. The pulses of direction evolution might be in response to increasing dust flux. When we project these changes in evolutionary rates to the marine record of terrigenous percentage sediment (the erosion curve), we find they coincide with changes in the intensity of erosion. The two coincidences between accelerated directional evolution of m3 at corresponding peaks of high erosion intensity occur at about 4.1–3.76 Ma and again at about 218 The East African Plio-Pleistocene

2.5 Directional evolutionDirectional evolution Directional evolution Stasis Stasis 2

1.5

0.5

0 Nyanzachoerus-Notochoerus -0.5 m3 occlusal surface area (z-score) 243

25 ODP Site 722 % terrigenous Erosion/dust flux threshold 20

243 Age (Ma)

Figure 7.6 Trend of increasing m3 tooth size in Nyanzachoerus–Notochoerus (Tetraconodontinae, Artiodactyla) plotted against the record of erosion intensity showing alternating intervals of evolutionary stasis and directional evolution. Three coincidences of accelerated directional evolution of m3 with peaks of high erosion intensity (indicated by gray-shaded rectangles) occur at about 4.1 to 3.76 Ma and another at about 3.3 to 2.83 Ma. Directional evolution is triggered when erosion intensity or dust ﬂux exceeds a threshold value of about 23% terrigenous.

3.3–2.83 Ma. The fit between the evolution and erosion splines is not precise, and there are conspicuous deficiencies in the continuity and density of the terrestrial fossil record. Appropriate to the novelty of discovery, we are looking at a record of alternating stasis and directional evolution, with directional evolution responding to periods when erosion or dust flux exceeded a threshold value that triggered a change in the direction and rate of tooth evolution. The change in direction is always consistent (at the same time intervals and in both records of erosion and evolution). In both cases, the erosion threshold value seems to be about 23% terrigenous.

7.4.2.3 Theropithecus Theropithecus oswaldi (with three chronospecies or subspecies: T. o. darti, T. o. oswaldi, and T. o. leakeyi) is essentially a single anagenetically evolving lineage. While this lineage is characterized by an evolutionary increase in body size, the body size 7.4 Data analysis 219

trend can be distinguished from anagenetic change in m3 shape by assuming that m1 crown size tracks body size evolution more faithfully than m3. In fact, as m1 enlarges through time, it does so at a slower rate than m3, which we assume tracks the adaptive response to soil ingestion and soil erosion more faithfully. This is an example of body size and m3 shape being evolutionarily “decoupled.” To avoid conflating evolutionary trends in T. oswaldi and T. brumpti, all tooth size measurements from the interval of temporal overlap between these distinctive species were deleted and only patterns in the T. oswaldi lineage are examined. Thus, the pattern of change in evolutionary rates of m3 tooth shape described here occurred during one segment of the longer anagenetic trend, the segment before the interval of temporal overlap with T. brumpti between 3.42 Ma and 2.41 Ma. Lower third molar evolution in Theropithecus oswaldi can be described as a simple monotonic trend of increasing tooth size between about 3.4 Ma and 2.35 Ma (Figure 7.7). Fitting a smoothing spline to the same data reveals some variation in evolutionary rates. There are three intervals of acceleration in directional evolution: the first between about 3.4 Ma and 3.25 Ma, a second between about 3.1 Ma and 2.9 Ma, and a third starting from about 2.8 Ma and ending about 2.5 Ma. These three accelerations are coincident with peaks in the terrigenous percentage record. There are also three peaks of highest evolutionary rates in the smoothing function plot of Theropithe- cus oswaldi m3 crown area between 3.42 Ma and 2.41 Ma. These three peaks correspond roughly with three consecutive peaks of erosion intensity in the ODP 722 terrigenous percentage record. As in the case of the Nyanzachoerus–Notochoerus scotti lineage, there seems to be a threshold of erosion intensity at about 22%, above which Theropithecus oswaldi tooth shape evolution becomes directional, and below which the evolutionary trend either stabilizes or reverses. Directional evolution is sustained as long as erosion remains above this threshold. During the interval from about 3.4 Ma to 2.35 Ma, there are four inflections or changes in the shape of the curve of erosion intensity, representing probably climate- driven changes in the erosion regime. These four inflections are coincident with change or inflections in rates of tooth shape evolution. In all cases, the direction of evolutionary response is consistent with the direction of change in erosion intensity. That is, when the intensity of erosion increases, tooth size begins to increase, and when the intensity of erosion decreases, tooth size stabilizes or begins to reverse.

7.4.2.4 Australopithecus Australopithecines are not abundant in the fossil record. The fossil record of Ardipithe- cus ramidus to Paranthropus boisei mandibular m3 tooth size evolution is discontinuous and not very dense. Despite all the effort of collectors and all the millions of dollars and other currencies spent in their collection, the available record of australopithecine evolution at best describes a long-term generally monotonic trend of increasing m3 tooth size between about 4.3 Ma and 1.4 Ma (Figure 7.8). A smoothing spline ﬁt to the original data reveals some subtle variation in the rate of evolutionary change. During this long interval, there are three shorter intervals of slightly more accelerated directional evolution, 220 The East African Plio-Pleistocene

Stasis Stasis Directional Directional Directional evolution evolution evolution 3

1 m3 occlusal

0 surface area (z-score) Theropithecus -1

Theropithecus -2 2 2.5 3 3.5 4 40

30 Erosion/dust flux threshold

20 ODP Site 722 % terrigenous

10 DSDP-ODP 722

2 2.5 3 3.5 4 Age (Ma)

Figure 7.7 Trend of increasing m3 tooth size in Theropithecus oswaldi in the Turkana Basin and southern Ethiopia between about 3.4 Ma and 2.35 Ma, and the intensity of erosion as evidenced by the percent of terrestrial sediment on the sea-floor of the Arabian Sea. Smoothing splines fit to the record of evolutionary change, and terrestrial sediment on the sea-floor reveals either coincident peaks, intervals of acceleration, and inflections, or change in the shape of the curves of evolution and erosion (gray-shaded rectangles).

interrupted by intervals of slower change or evolutionary stasis. These three intervals of accelerated direction evolution occur roughly between 4.25 Ma and 3.75 Ma, between 3.25 Ma and 2.75 Ma, and again between about 2.25 Ma and 1.5 Ma. Given the generally poor record of australopithecine dental evolution, and the contentious atmosphere surrounding their taxonomy, this may not be a very compelling story, but these 7.4 Data analysis 221

3 Directional StasisDirectional Stasis Directional evolution evolution evolution A. boisei 2 +A. aethiopicus 1 ++ xUnknown + x x 0 x x A. anamensis x xx xx -1 x surface area (z-score) A. afarensis Ard. ramidus

Australopithicene m3 occlusal -2 1 234 35

25 Erosion/dust ODP Site 722 % terrigenous flux threshold 20

1 234 Age (Ma)

Figure 7.8 Trend in australopithecine m3 tooth size evolution plotted against the curve of long-term average soil erosion. There are three intervals during the Plio-Pleistocene when australopithecine tooth size evolution accelerated coincident with high erosion intensity (indicated by gray rectangles). In australopithecines, m3 tooth enlargement occurs in response to soil erosion above a threshold value of about 24% terrigenous.

intervals of accelerated evolutionary change coincide with the corresponding intervals of more rapid change in Metridiochoerus, Nyanzachoerus–Notochoerus,andTheropithecus oswaldi. Not only is the temporal coincidence shared, but the direction of evolutionary change is as well. Moreover, as with Metridiochoerus, Nyanzachoerus–Notochoerus,and Theropithecus oswaldi, the three intervals of more rapid evolution in australopithecines correspond to peaks in the terrigenous percentage input to the sea-ﬂoor with a threshold value of about 24% initiating directional change in australopithecine m3 size evolution.

7.4.3 Discussion

The results relate a marine sediment record of erosion to tooth shape change in four different terrestrial herbivorous mammals (Figure 7.9). The sea-floor terrestrial sediment record describes environmental conditions in the dust source area and the surface processes that deliver that dust to the sea-floor, and the record of tooth shape change comprises the evolutionary response to change in the same surface processes that deliver mineral grit onto their foods. For an environmental cause such as soil ingestion driven by soil erosion, we ought to find evidence of tooth shape evolution in diverse 222 The East African Plio-Pleistocene

2.5

1.5 Theropithecus 1

0.5 Nyanza- 0 Notochoerus

-0.5 m3 occlusal surface area (z-score) -1 Australopithecus -1.5

-2

-2.5 Metridiochoerus

20 ODP Site 722 terrigenous %

1.5 2342.5 3.5 4.5 Age (Ma)

Figure 7.9 Synchrony between evolutionary trends of increasing m3 tooth size in four lineages of mammals from the Turkana Basin and Ethiopia (Metridiochoerus, Nyanzachoerus–Notochoerus, Theropithecus oswaldi, and australopithecines), plotted with terrigenous percentage from ODP Site 722, used here as a proxy for erosion intensity. Congruences (and the absence of congruence) are indicated by shaded rectangles.

mammals, and detailed coincidences among these records and between them and the invoked environmental drivers. Not all mammals are equally likely to respond evolutionarily to soil erosion intensity (or ﬂux). The four lineages examined are among the most likely candidates. These are 7.4 Data analysis 223

well-known lineages that evolved higher crowns, larger teeth, and/or increasing enamel volume, and that have good fossil records. The species data or mammal tooth shape data come from the published measurements of their teeth, from original material in the terrestrial fossil record of the East African rift valley, in the general source area of the atmospheric dust and volcanic ash that was entrained by the wind and ended up being deposited on the sea-floor. They are measurements (crown length and width) of the last or third molar in the lower tooth series (noted as m3), because evidence of cause and effect will most likely be found in the last or third molar, the tooth whose functional longevity is most intimately tied to reproductive lifespan. Thus, m3 is the tooth position that will be the most active target of natural selection for reproductive fitness in the face of premature dental senescence. The product of length and width is crown surface area, an estimate of the volume of mineral substance in the crown. Because each mammal is a different body size, m3 crown area is log transformed and standardized to mean¼0 and standard deviation¼1. The environmental variables were sampled at uniform intervals along a marine sediment core recovered from the floor of the Arabian Sea. It is a downwind record of environmental conditions in the source area expressed as four different variables: (1) the terrigenous fraction of the marine sediments (expressed as a percentage), (2) linear sedimentation rate, (3) lithogenic flux, and (4) volcanic ash shard counts (Figure 7.10). The linear sedimentation rate is a measure of the rate of sediment accumulation on the sea-floor. Lithogenic flux is the amount of terrestrial sediment falling through the water column per unit time, and is related to the amount of mineral dust that rains out of the atmosphere onto the sea surface less the amount scavenged at the surface by phytoplankton. The count of volcanic ash shards is the number or abundance of fragments of volcanic ash in the terrestrial sediment fraction. Which of these is the better predictor of evolutionary response? When I follow the vertical lines, the shaded swaths that “connect” peaks in the dust archives to the curves of evolving tooth size, there seems to be more congruence between evolutionary change and lithogenic flux than with either terrigenous percentage or shard count (Figure 7.10). The congruences are not perfect. Terrestrial sediments in the marine cores are documenting erosion of the land surface; that is, the deflation, entrainment, and transport of dust off the land surface in the area the animals inhabited. Not all mineral dust that rains out of the atmosphere onto the sea surface winds up as terrigenous sediment on the sea-floor. Some is dissolved by sea-water and some is taken up by marine microorganisms and converted to biogenic sediment. The variable terrigenous percentage is not a pure record of erosion intensity, because it is influenced by the amount of biogenic marine sediment that occurs with it (the other fraction of the total), and the amount of biogenic marine sediment ultimately depends on the productivity of the plankton living near the sea surface. The abundance of plankton varies with fertilization of the sea surface by upwelling and windblown mineral dust; thus as more dust falls onto the ocean surface, marine productivity increases. As sediment thickness is a measure of the total accumulation from all sources, linear sedimentation rate is also influenced by marine productivity. 3

2 Theropithecus 1 Nyanza- 0 Notochoerus

-1 area (z-score) m3 occlusal surface -2 Australopithecus Metridiochoerus

3 ) -1 2 ka -2 1 Litho. flux (gcm 0

6 )

-6 5 4 3

rate (m/yr 2

Linear sedimentation 1

4 3 2 1 abundance

Std. log shard 0 -1

20 Terrigenous % 10

1.52 2.53 3.54 4.5 Age (Ma)

Figure 7.10 Synchrony between evolutionary trends of increasing m3 tooth size in Turkana Basin and Ethiopian samples of Metridiochoerus, Nyanzachoerus–Notochoerus, Theropithecus oswaldi, and australopithecines, and with four renderings of the sea-ﬂoor sediment record at ODP Site 722, lithogenic ﬂux, linear sedimentation rate, volcanic ash shard abundance, and terrigenous percentage. Congruent peaks (and the absence of congruence) are indicated by shaded rectangles. 7.4 Data analysis 225

Of the four variables from the sea-floor sediment record, lithogenic flux may be the best record of erosion intensity in the dust source area. Volcanic ash shard count is especially interesting in this regard because it certainly was eroded off the surface of the land where the animals lived. Whereas terrestrial sediment may be sourced from areas all around the Arabian Sea, volcanic ash is only produced by volcanism in the Ethiopian rift system; and the same is true for the geographic source of the accompanying pollen rain. However, as volcanic ash is only a fraction of the erosion products coming off the land surface, a shard count is not a complete record of erosion intensity in Ethiopia. Volcanic ash shard counts include shards produced by eruption events and also shards deflated and entrained into winds by surface erosion, and the fluctuation in their abundance over time is a reflection of variation in the frequency and intensity of volcanic eruption plus long-term average erosion. These are two different processes. Theropithecus oswaldi evolutionary rates seem to show some congruence with shard count, and this might be expected given the foraging behavior of the modern gelada baboon for low herbaceous plants growing in depressions on the basalt surface of Ethiopia that trap and deflate volcanic ash. How should evolutionary response be related to the intensity of erosion? Nobody knows, nobody has thought much about it, and nobody has looked for it in coupled marine and continental records. Should we expect evolutionary rates to vary with erosion intensity, accelerating when erosion rates climb, and decelerating (or even reversing) when erosion intensity moderates? Every time erosion intensity increases during the interval for which we have tooth size data, we see evidence of directional evolutionary response in each of the four lineages. Not only is the timing of onset similar, so is the duration of response. The hypothesis we entertain requires coincidence between changing rates of tooth shape evolution with changing intensity of erosion. As erosion accelerates, tooth shape evolution should also accelerate. Morphological evolution driven by excess tooth wear, when it occurs, should be in response to a change in erosion regime or in erosion intensity, and directional evolution should be triggered at some threshold of erosion intensity. There should be a threshold value of soil erosion (mineral particle flux across the land surface) above which erosion begins to drive directional morphological evolution. Morphological evolution should continue as long as erosion intensity is above the threshold value. Whenever erosion intensity passes through a threshold, and is sustained at intensities greater than threshold, we should expect to see evolutionary response, and, for as long as the intensity of erosion is above the threshold value, morphological evolution should continue. There could very well be a peak in erosion intensity above the threshold value, but that will not necessarily correspond to a peak in rates of evolution. Even higher intensities of erosion might not lead to still higher rates of evolution. There is, after all, a maximum soil load that plant surfaces can support, and a level of erosion above which animals will simply become extinct. Morphological evolution should not vary in time precisely or instantaneously with erosion intensity, but their onset ought to be delayed. How much delay? Who knows? Moreover, we do not know if expected delay will be detectable in the fossil record as a 226 The East African Plio-Pleistocene

departure from a precise ﬁt with the erosion record. The available evidence for evolution in T. oswaldi seems to be sufﬁciently dense to reveal delays in evolutionary response. In a general sense, all four lineages display unidirectional cumulative change in increasing tooth size. This is accompanied by parallel increases in crown complexity, enamel thickness, and crown height. However, as measured, the analysis only captures a small part of tooth shape evolution. Nevertheless, it is remarkable that the story has been captured in the fossil record, given that premature dental senescence leads eventually to mortality by tooth mechanical failure.

7.4.4 Objections 7.4.4.1 Controlling for body size We compare m3 tooth size evolution to erosion intensity, but the observed evolutionary trend in increasing crown size could be a byproduct of evolution of body size for other reasons. As far as I know, there is no body of theory relating body size evolution to soil erosion, whereas this book presents a body of theory relating tooth enamel volume to soil erosion. Regardless of the absence of a coherent theory of agency for body size evolution, criticism may suggest that the coincident time series are not demonstrating direct agency, but something else; for example, the spread of grasslands and grazing morphology. Regardless of the fact that there exists a theory relating soil erosion to excess tooth wear, there really is no theory relating soil erosion to the evolution of aspects of tooth shape that serve to resist abrasive wear. This is an adaptation that is presumed, not proven. The best choice of morphological variable would be, of course, tooth volume (length width height or liquid displacement) or a megadonty or a ratio (e.g., HI) that uses an independent skeletal measure for body size and controls for body size (height/length or width). There is no good published data for crown height in the East African Plio-Pleistocene suid third lower molar. Available published data are exposed crown height measured from the alveolar margin (with no control on wear stage), not measurements of total tooth crown height in the complete and unworn crowns of juveniles or young adults. Obtaining such measurements, if it were possible, would signiﬁcantly reduce the total number of specimens in the dataset. As a broad generalization, body mass evolution does respond to environmental quality. As environmental quality decreases, mammals evolve larger body size, as an accommodation to lower quality or limited food resources. This seems counterintuitive, but the allometric scaling is thought to reﬂect energetics and the physiology of the digestive system. All other things being equal, larger mammals require less energy than smaller mammals. Thus, if high erosion represents degraded environments and lower environmental quality, mammals might evolve larger body sizes to compensate for the decreased productivity (or lower energy availability). If so, would you not expect the teeth to evolve isometrically with body size? In Suidae, there appears to be a decoupling of tooth size with body size, and this relationship varies with each tooth position. For example, in the Nyanzachoerus syrticus–Notochoerus scotti 7.4 Data analysis 227

lineage, m1 length remains the same, m2 length increases somewhat, and m3 length increases notably. At the same time, the relative size of the premolars changes from large in Nyanzachoerus syrticus to small in Notochoerus scotti. Using an independent proxy for body size (femur head diameter, femur mid-shaft diameter, cranial length), can we tell whether the molars are scaling isometrically or allometrically with body size? Armed with a prediction of body size, can departures from prediction be argued as evidence for another causal pathway? Even if we could, would it matter for our argument? We are talking about tooth functional longevity and its relationship to reproductive longevity, not whether the teeth are satisfying physiological demands. They obviously were during this evolution, or we would not see the continuous evolutionary trends. That body size might be part of the accommodation to high erosion is also plausible. After all, the whole animal is evolving, not just the m3. We are examining m3 not because it is in some way independent of body size, but because it is the functional longevity of this particular tooth that is so crucial to reproductive ﬁtness that evolutionary change obviously concentrates at this locus. Reducing the physiological demand on this tooth (through increasing body size) could have been part of the adaptation.

7.4.4.2 Temporal resolution There are very important differences in how fossil teeth and sea-floor sediments are sampled. Each sample from a marine sediment core represents a unique point in time, whereas fossil teeth are attributed to stratigraphic units demarcated by a lower and upper tuff or marker bed of known age, and each unit represents the temporal interval between these two dated tuffs. The units are not of uniform duration and in the Turkana Basin they range from 1.74 myr to 0.16 myr in duration. As each tooth is assigned to a stratigraphic unit of variable duration, the evolutionary response variables are not true time series. As a consequence of the inherent differences between terrestrial fossil and marine sediment sequences, the temporal interval between fossil teeth is variable, whereas that between samples of sea-floor sediment is more-or-less uniform. Further- more, there are many more samples of sea-floor sediment than there are fossil teeth. The temporal resolution of the Indian Ocean (DSDP/ODP 722) marine record depends upon the sampling interval and the age model, and these records are astronomically tuned to remove inherent variation attributed to sediment compaction. The temporal resolution of the East African (Turkana Basin) continental mammal record depends on the 40Ar/39Ar age of tuffs and the assumed age of the fossil-bearing sediments between them. These are two very different scales of temporal resolution. The only way you can legitimately compare evolutionary patterns in a continental record with agency (soil erosion) captured in a marine record, would be to render both in comparable temporal resolution by binning the data into 50 000 year intervals. This is a popular approach (see Cerling et al., 2011a) that, when used, reveals long-term monotonic background trends. However you elect to render the marine and terrestrial records, long-term background trends emerge. Feakins et al. (2005) plotted DSDP 231 mean d13C isotope values for

C30 n-alkanoic acid for eight brief intervals in the last 4 myr and showed a background 228 The East African Plio-Pleistocene

trend of decreasing values between 3.37 Ma and 1.4 Ma (see following discussion). 2 Martinez-Garcia et al. (2011) plotted ODP 1090 C23-C33 n-alkanes MAR (µg/m /yr) over the same interval between 3.37 Ma and 1.4 Ma and showed a similar background trend of increasing MAR. There are other gradual monotonic trends of environmental change through this same interval; for example, the fraction of woody cover reconstructed from δ13C in pedogenic carbonate and tropical soil organic matter in the Awash Valley and Turkana Basin (Cerling et al., 2011a). By the standards of mammalian paleontology, the fossil-bearing terrestrial sediments in the Turkana Basin and Ethiop- ian rift are considered to be relatively continuous sequences, and tooth shape evolution in all four lineages describes monotonic trends of increasing tooth size and crown height. The astronomically tuned terrestrial component of the sea-ﬂoor sediment record is primarily a record of surface erosion that occurs at all timescales. The smoothing function ﬁlters this “noise” by effectively “binning” the data through a running average. If it were possible to adjust the temporal interval of the running average continually such that it matched the changing temporal intervals of the stratigraphic units of the terrestrial fossil record, perhaps this would be helpful. The fossil mammals are already binned by the manner in which paleontologists record provenience. Whatever approach we might take, rendering the two kinds of data in the same way does not introduce new noise.

7.4.4.3 It could be grass! It might be said that atmospheric dust contaminates everything in the environment, including the pelage of herbivores, the surfaces of their lungs, the exposed carcasses eaten by scavengers, the wings of insects, the exterior surfaces of soft fruit, hard seeds, and nuts, and all the leaves of all the plants, even the tallest trees, and hence its presence should be detected in the diets of all mammals. Additionally, if this contamination does not inﬂuence tooth shape in all mammals, the proposition made by this book cannot be invoked to explain any particular evolutionary pattern. I am intentionally not interested in unlikely candidates, and do not plot the lack of evolutionary change in other mammals as “tests” of the general hypothesis. Instead, I am interested only in examining lineages that document tooth shape change that is plausibly related to resisting abrasive wear, in order to see whether evolutionary rates in these characters relate to the intensity of soil erosion. Congruent response in independently evolving lineages is important to the plausibility, but in the form of an expectation that the same process should inﬂuence tooth evolution in all mammals, I would ask the reader to return to earlier chapters. A more appropriate negative test would be to discover a lineage that evolved

structural changes in these same features coincident with the adoption of C4 feeding, but not coincident with changes in erosion intensity. Another meaningful test would be to examine other mammal lineages that ought to respond (such as equids, Loxodonta, Elephas), to see whether their evolutionary response is more consistent with erosion

intensity or isotopic evidence of grazing on C4 grasses. Consequently, it could be grassland expansion and grass consumption; that is, grass phytolith consumption or direct soil ingestion through grazing behavior in grasslands 7.4 Data analysis 229

(without the intervention of extrinsic surface processes) during arid phases of grassland expansion when dust delivery to the sea-floor peaks naturally. We really do not need to invoke any external agency nor contrive a complex source-to-sink mineral particle transport and delivery system. The most continuous record of the vegetation in NE Africa during the time these lineages evolved are the pollen spores preserved in the Gulf of Aden DSDP 231 sediment core (Bonnefille, 2010; Feakins et al., 2013), and the soil carbonate record from the sedimentary basins of the volcanically active Turkana Basin and Ethiopian rift system (Cerling et al., 2011a). In the sea-floor record, the geographic source area for this pollen is the same as the source area of the volcanic ash, and this source area includes the area occupied by the mammals that were evolving large and high-crowned teeth (Figure 7.11). The marine record of pollen and stable carbon isotope from paleosols and tooth enamel yield a confusing mix of general trends and fluctuations between 4.5 Ma and the present. For example, the continuously high soil temperatures (between 30 C and 40 C after about 4 Ma) reconstructed for paleosols in the Turkana Basin were originally thought to indicate persistent open vegetation throughout the Plio-Pleistocene (Passey et al., 2010). Yet this conclusion was in apparent conflict with paleovegetation records that implied significant woody cover and shade (Bonnefille, 2010). Using other data, relatively open conditions at 4.5 Ma yielded to increasing woody cover after about 3.6 Ma (Cerling et al., 2011a). A trend of increasing abundance of halophytic herbs or shrubs culminated at about 2.5 Ma, following the long trend of forest expansion from 5.5 Ma to 3.5 Ma and stepwise tree cover decline between 3.5 Ma and 2.7 Ma (Bonnefille, 2010). The interval between 3.6 Ma and 1.4 Ma is thought to document the return of open environments until a peak in the extent of open grasslands was reached at 1.8 Ma (Cerling et al., 2011a). The trends described by this scenario conflict with significant variation in the abundance of grass pollen in marine sediments throughout this interval, and although the amplitude of the fluctuations increases, there is no progressive trend in grass pollen percentages (Bonnefille, 2010; Feakins et al., 2013). Instead, the marine record of fluctuating grass pollen percentages differs from the smoothly progressing increase in aridity and a general shift from C3 woodlands toward regularly increased C4 grasslands starting about 2.7 Ma (Cerling et al., 2011a). However, again, the “dynamic of vegetation and climate over East Africa appears more complex than the unidirectional increasing aridity trend” (Bonnefille, 2010). Part of this confusing picture is a consequence of data handling; that is, the difference between a smoothing function fitted to continuous time series (Feakins et al., 2013) and a linear trend line fitted to data binned into coarse and varying temporal intervals (Cerling et al., 2011a). Another problem has been matching geographic source areas, but this has nearly been resolved by restricting the geographic scope of the terrestrial record and making it more consistent with the sea-floor records that capture the products of surface processes, volcanic eruption products, plant cuticle, and pollen. While all this agreement and disagreement about fluctuations and trends in changing vegetation is interesting, a rendering of the data in time series does not provide any insight into the evolutionary patterns revealed here (Figure 7.11). Obliquity-driven 3

2 Theropithecus 1 Nyanza- 0 Notochoerus (z-score) -1

m3 occlusal surface area -2 Australopithecus Metridiochoerus

3 ) -1 2 ka -2 1 (gcm Lithogenic flux 0

# Pollen types 10

50 40 30 20

% Poaceae 10 0 -22 -24 (‰)

30 -26

C–C -28 13

d -30

0 -2 -4 -6

C (mean) -8 13 d -10 -12 1.52 2.53 3.54 4.5 Age (Ma)

Figure 7.11 Synchrony between evolutionary trends in tooth size in four lineages of terrestrial mammals from the Plio-Pleistocene of the Turkana Basin and Ethiopia, the downwind record of erosion intensity (lithogenic ﬂux), and various “vegetation” proxies including the number of 13 pollen types and % Poaceae in pollen samples, and δ C–C30 from leaf wax in DSDP Site 231 (Gulf of Aden) sediments (all data from Feakins et al., 2013), and the terrestrial paleosol stable 13 carbon isotope δ CPDB trend (from Cerling et al., 2011b). 7.4 Data analysis 231

glacial-interglacial cycles appear to be the dominant mode consistent with variation in the rate of tooth evolution. Higher-frequency, precession-driven change in water balance and lake levels (Joordens et al., 2011) probably drives the fluvial-eolian interaction that explains at least some of the record of erosion intensity (see later), and the sea-floor record of lithogenic flux makes a better fit to changing rates of tooth shape evolution than any of the data used to reconstruct vegetation. Obviously, it could be that the animals themselves are disturbing the soil surface during their feeding activities, and therefore are contributing to soil erosion and the contamination of low plant surfaces by soil. The erosion fluctuations may be driven by herbivore activity (without any climate influence), and the intensity of this induced erosion increases and decreases with population density in response to something quite different, such as variation in the productivity of vegetation. My preferred hypothesis is that tooth shape (the amount of tooth mineral substance) reflects the intensity of tooth wear determined by the amount of ingested abrasive mineral grit in the diet. This causal relationship leads to a set of predictions about the coincidence between the environmental variables and the evolutionary response. These predictions are: (1) as the rate of erosion changes, so should there be change in tooth shape, (2) the direction of change in each should be coincident, (3) if there is any offset or lag, the evolutionary response should occur after the change in erosion, (4) of the four environmental variables, lithogenic flux should provide the best fit to the evolutionary response, (5) the proposed environmental process should drive coincident change in the lineages examined, and (6) any lack of coincidence may be related to sampling deficiencies, and temporal coincidence should improve with the quality of the fossil record (increasing abundance of fossils).

7.4.4.4 Fluvial-eolian interaction? The broad trends of variation in terrestrial sediment delivery to the sea-floor revealed by smoothing splines (lambda¼0.1, 0.01, 0.001) simplify the underlying variation in terrestrial sediment input to the Arabian Sea floor between the interval from 4.5 Ma and the present. Depending on the “tolerance” of the spline functions, the curves reveal many briefer or fewer prolonged peaks in total terrestrial sediment input to the Arabian Sea (Figure 7.12). The three youngest of these peaks agree with intervals of deep freshwater lake sediment accumulation (2.7–2.5, 1.9–1.7, 1.1–0.9) preserved in the fluviolacustrine and eolian fill of the last 2.9 Myrs in rift basins from Olduvai in Tanzania, the Turkana Basin, and the Afar Basin in Ethiopia (Trauth et al., 2005). The temporal coincidence between peaks of terrigenous input to the sea-floor and deep-lake sediment deposition in rift valley basins suggests that fluvial-eolian interaction peaked at these times. Finally, given the eolian mechanism proposed here, one might wonder why there are no significant accumulations of fine-grained windblown sediments or remnants of eolian sediments anywhere in the Turkana Basin or adjacent rift valleys or the surrounding uplands and countryside. Where are these deposits? Do the basalt surfaces allow only the most temporary and ephemeral repose? Was the vegetation inadequate to trap 232 The East African Plio-Pleistocene Insolation (W/m 30°N June-July Index ( Precessional Eccentricity Obliquity ε

South North sin

-2 -1 ω 2 )

Lithogenic flux (gcm ka ) Turkana Ethiopian Afar )

0 1 2 3 Basin Rift Basin 0 0.5

0.72 0.8-1.0 Basalt 1

1.5 1.38 1.38 1.44

1.66 1.85 1.88 1.87

2 2.0 2.0-2.1 Basalt

2.35 2.5 2.51 2.58 2.68 2.71 Basalt

3 3.01

age data lava, tuff deep freshwater lake 3.5 shallow alkaline lake no lake

4 Humid periods: lakes present, terrigenous influx high (=high erosion intensity) 4.5

Figure 7.12 The changing intensity of fluvial-eolian interaction captured in astronomically tuned variation in lithogenic flux to the sea-floor (http://www.ldeo.columbia.edu/~peter/site/Data.html), smoothed by a fitted spline, correlated temporally with the mode of terrestrial sedimentation in the Turkana Basin and southern Ethiopia (from Trauth et al., 2005, with permission from Elsevier), and nested orbital timescale cycles (from Kingston et al., 2007, with permission from Elsevier).

the eolian particle flux? Or is the implied accession of windblown dust to surface soils undetected in the Turkana Basin because nobody does detailed grain-size analysis anymore? The mechanism proposed here, that is the action of the Turkana low-level jet and the deflation, entrainment, and transport with final deposition on the Arabian Sea floor, is a simple mechanism. However, it operated at a time when both fluvial and eolian processes were active. Whenever the Omo River sediments and delta in Lake Turkana 7.5 Conclusions 233

during dry seasons and drier climate phases received fresh deposits, these were susceptible to deflation by the jet. In addition, fresh ash deposits washing downriver or falling directly onto the floor of the Turkana Basin with its extensive flood basalts, would also become easily deflated and entrained by the jet.

7.5 Conclusions

Two lineages of suids, australopithecines and Theropithecus, both seem to respond in the same way to change in mineral particle ﬂux. All are terrestrial mammals, and the suids and Theropithecus presumably fed close to the ground, and roots and tubers have been mentioned as part of some australopithecine diets (Laden and Wrangham, 2005). Theropithecus was probably an open-country feeder, based on its closest living descendant the Gelada baboon, and enamel stable carbon isotopes indicate that Thero- pithecus as early as 4 Ma, the Nyanzachoerus–Notochoerus lineage at about 2 Ma, Metridiochoerus as early as 3 Ma, and Paranthropus boisei between 2 Ma and 1.5 Ma

became consumers of C4 grasses (Harris and Cerling, 2002; Cerling et al., 2011a, 2013; Uno et al., 2011). In the Nyanzachoerus–Notochoerus lineage, as well as T. oswaldi and the australopithecines, much of the evolutionary response to changing erosion intensity

occurred before there is evidence that a C4 diet was adopted. Did all these four lineages actually evolve in the Turkana Basin and Ethiopia; that is, the area under the influence of the proposed mechanism? It does not appear that the T. oswaldi lineage evolved elsewhere; there are no earlier occurrences of any of the three subspecies (T.o. leakeyi, T. o. oswaldi,orT. o. darti) at another latitude, such as in South Africa. However, subsequent to their first appearance in East Africa, the subspecies of T. oswaldi moved to inhabit other parts of Africa, notably North Africa and South Africa, as if the dental adaptations conferred competitive advantages and opened opportunities for them. The australopithecines are also known from other latitudes. While Paranthropus boisei is a characteristically East African hominin, and the culmination of the evolutionary trend described here, there do not appear to be older occurrences elsewhere of any of the species that comprise the australopithecine lineage as used here. This implies that the observed evolutionary changes are being driven by erosion intensity in the source area of the terrestrial sediments in the marine cores; that is, the Turkana Basin and Ethiopia. Is the apparent response to mineral particle flux spurious? Are the animals evolving in relation to something else, and the apparent coincidence of change with mineral particle flux an artifact? For example, are the teeth of suids, Theropithecus and Australopithecus, evolving in response to spreading grasslands, or climate variability, or other kinds of hard objects in their diet, or things that influence population density and reproductive lifespan and artificially “magnify” the influence of grit and dust, or any one of a zillion other possibilities we cannot imagine? Spreading grasslands? You might think that spreading grasslands would slow soil erosion, and that as grasslands spread, net erosion would diminish and the consequences 234 The East African Plio-Pleistocene

for tooth evolution would become muted. Unless accompanied by increased aridity and more soil exposure at the surface, grasses slow soil erosion, whether by wind or water. Thus, high mineral particle flux is more an indicator of aridity and/or exposed soil at the surface than open grasslands. The highest mineral particle flux is found during temporal intervals when there is fluvial-eolian interaction. Impressive fluvial-eolian interaction occurs in all climates and vegetations, from cold temperate forests in generally wet climates such as around the Gulf of Alaska, to sparse grasslands around arid deserts such as in SE Australia. Climate variability? The more variable the climate, the higher the erosion. You can appreciate the many temporal scales of variability in erosion intensity by looking at the marine sediment record. Remember that this record only resolves down to millennial timescales, and does not come close to capturing decadal, interannual, or seasonal variation. There are two very different records of surface processes in East Africa, the East African Rift Basin fluviolacustrine sediment sequences and the Arabian Sea terrestrial sediment record. The first is predominantly fluvial (punctuated by periods of lacustrine sedimentation); the second is predominantly eolian. The Arabian Sea floor sediment record shows cycles at all timescales. The Rift Basin sediment record also shows cycles, but at a more limited range of timescales. At orbital timescales significant to mammalian tooth evolution, there is a curious and seemingly contradictory coincidence between deep lake lacustrine diatomite sediment accumulation in the basins and the intensity of eolian processes delivering fine-grained sediment and volcanic ash to the Arabian Sea. One might expect that significant diatomite deposition in deep lakes could occur only when eolian activity was minimal. Therefore, why are there coincident peaks in the long-term average eolian flux (as captured by the smoothing splines) and Rift Valley Basin diatomite deposition? Why should eolian erosion and transport (dustiness) coincide with “humid period” pure lacustrine sedimentation in the Rift Basins? Should these things not be “opposites”? Well, on closer inspection, they are opposites, temporal opposites, but at a timescale distinct from that of the evolutionary response in tooth shape. At this point, you may ask, what am I talking about? Some dominant mode of long-term orbital variation drives long- term average erosion intensity (that, in turn, appears to drive tooth evolution), while at the same time, shorter timescale climate cycles drive fluvial-eolian interaction in the Rift Valley basins (Figure 7.12). It appears that while eolian erosion occurs in the surrounding volcanic uplands, in the Turkana Basin, fluvial and lacustrine sediments are being deposited. In both settings, upland and basin, the finest fraction becomes windborne, leaving the coarser fraction to become the fluvial sediments in which we find the fossil mammals. While this is going on under long-term average conditions, at a finer timescale, very fine-grained diatomite is deposited while eolian processes are quiet. How does this happen? In the basin, diatomite deposition in deep lake settings during “humid” periods follows variation in insolation. Meantime, variation in eolian flux to the Arabian Sea obeys a different mechanism. At roughly the same time all this is happening, perhaps at similar or perhaps at different timescales, fluvial sediments are being deposited without any fine-grained eolian contribution. 7.5 Conclusions 235

Hard objects in the diet? In my way of thinking, the only hard objects of importance to the evolution of tooth shape adaptations for resisting abrasive wear, are the particles of mineral grit. Were pigs, australopithecines, and Theropithecus all eating these same hard objects? Are the evolutionary trends in tooth size tracking parallel trends of increasing hardness in the nuts, seeds, or fruit they eat, or in the soil particles they ingest? What modern environmental gradients correlate with the hardness of nuts and seeds, and would these physical or mechanical properties of foods increase stepwise in tune with orbital variation in climate? Population density? If population density is cyclical, and evolutionary rates are being driven by changes in density, what might be the mechanism? If peaks in eolian dust flux reflect aridity and arid-phases of climate, we might predict that population density would decrease. A decrease in population density is not consistent with our understanding of the effects of density on tooth wear. Both soil ingestion and tooth wear increase with population density. Fluctuations in density, like everything else, occur at all timescales. Is it even plausible to propose that orbital timescale change in dust flux would change population densities in a way that could be meaningful for the evolution of tooth shape? 8 The middle Cenozoic of Patagonia

8.1 Introduction

From the late middle Eocene to the early Miocene, many South American herbivorous mammals, including Notohippidae, Interatheriidae, Archaeohyracidae, Notostylopidae, and Toxodontidae (among Notoungulata), Astrapotheriidae (Astrapotheria), Argyrolagoidea (Metatheria), and various clades among Caviomorpha (Rodentia) evolved higher tooth crowns. A substantial part of this evolutionary change appears to have occurred in Patagonia. Although lineages of South American fossil mammals are difficult to track, higher crowns evolved in multiple lineages independently. Over time, each clade accumulated higher numbers of high-crowned taxa and the overall proportion of high-crowned herbivores in faunas increased. This evolutionary transformation in tooth shape was more or less continuous between the middle Eocene and early Miocene, but three brief intervals or pulses of more rapid simultaneous change in more than a single lineage can be discerned: (1) between 39 Ma and 38 Ma, (2) between 31 Ma and 30 Ma, and (3) between 24 Ma and 21 Ma (see Figure 2.8). In addition, the overall proportion of hypsodont taxa among meridiungulates increased to 50%, with step-wise accelerations in this general trend coinciding with the first two pulses. While changes in the rate of crown-height evolution in the middle Cenozoic are what we aspire to explain, there are many problems linking surface processes with tooth evolution in deep time. Most of what has been established to this point comes from an inquiry about processes. The deep fossil and rock records are defective because they preserve very little of the process. Evolution leaves a deficient record of lineages, and erosion leaves little record at all. Consequently, I have struggled with this chapter more than any other. For example, it is not clear what, if anything, the Southern Ocean record of changing marine paleotemperature tells us about earth surface processes in Pata- gonia, yet the benthic foraminiferal paleothermometer is the foundation of everything we think we know about Southern Ocean environmental history. Hence, here, a stage is set for what we know and need in order to understand the evolution of precocious hypsodonty better. Although discontinuous, the richness, quality, and diversity of the Patagonian fossil mammal record in the middle Cenozoic is well known (Ameghino, 1904, 1906;

236 8.1 Introduction 237

Simpson, 1948, 1967;Maddenetal.,2010). In addition, a more continuous phytolith record provides a means to reconstruct temporal patterns of plant diversity (Zucol et al., 2010; Strömberg et al., 2013). The rock record in Patagonia and the rock and fossil records of the Antarctic Peninsula provide broader geographic and geologic context (Malumian, 1995;Casadio, 1998;Caminos,1999; Náñez, 1999). Finally, by analogy, just as the sea-floor of the north Arabian Sea is the ultimate repose of the terrestrial sediments that drove the evolutionary response in tooth shape among East African mammals through the Plio-Pleistocene, the sediment record on the sea-floor of the Southern Ocean will eventually have direct significance to an understanding of terrestrial conditions over Patagonia. This sea-floor record might reveal many new things about the terrestrial environments and changing sediment transport conditions over Patagonia. While modern sediments off Patagonia have been traced to the high- resolution deep ice cores of Antarctica, where they are shown to preserve a remarkable record of Patagonian surface processes and climate coupling (Albani et al., 2012), and this same record is now known from Quaternary sea-flooroftheSE Atlantic (Diekmann and Kuhn, 2002;Diekmannetal.,2003; Martinez-Garcia et al., 2011), the middle Cenozoic SE Atlantic and Southern Ocean records are not well constrained temporally and nowhere directly tied to sediment source areas in Pata- gonia. The Patagonian sediment and fossil records at Gran Barranca are age- calibrated by magnetic polarity stratigraphy, Ar/Ar (Ré et al., 2010) and U/Pb (Dunn et al., 2013) geochronologies, and although well constrained, this record is temporally discontinuous. The climate intimacy between Patagonia and the surrounding oceans is such that the history of Drake Passage (its paleolatitude, width, and bathymetric configuration) bears hugely on the intensity of atmospheric flow (with its wind and moisture) across Patagonia, and marine flow from the Pacific to the Atlantic around the Patagonian peninsula. General atmospheric and ocean surface circulation at the latitude of Gran Barranca generally sweeps across the South Pacific, and the exchange between atmosphere and ocean surface is what determines conditions of temperature and humidity over Patagonia, variables that drive the intensity of surface processes. Much of the evidence for significant change in deep ocean temperatures (Zachos et al., 1996; Bohaty and Zachos, 2003;Liuetal.,2009) and planktonic foraminiferal turnover (Aze et al., 2011) across the Eocene–Oligocene Transition (EOT) comes from the Southern Ocean, and naturally, one might expect this particular event to have left an appreciable imprint on the Patagonian fossil record. Yet, despite the fact that mammalian paleontologists have ascribed great significance to the EOT in Patagonia (Goin et al., 2010), to date, little to no change has been detected in key terrestrial indicators. Neither δ18O from phosphate in enamel apatite (Kohn et al., 2004, 2010), nor vegetation as reconstructed from conventional phytolith biostratigraphy (Ström- berg et al., 2013), nor sedimentology of the Vera Member at Gran Barranca (Bellosi, 2010a), have been found to change appreciably across the EOT. None of these sources of evidence suggests that Patagonia was sensitive to and responded to the sorts of changes seen in the southern high-latitude marine record or coincident with the abrupt threshold-like onset of glaciation in Antarctica (Lear et al., 2008). Why nothing seems 238 The middle Cenozoic of Patagonia

to have happened across the EOT in terrestrial environments in Patagonia is an enigma, attributed to the buffering effect of the ocean on terrestrial climate (Kohn et al., 2010). To date, nobody has looked at the coupling of the Patagonian terrestrial and Southern Ocean marine records through the lens of surface processes. The stratigraphy and sedimentology of the fossil-bearing sediments of the Sarmiento Formation at Gran Barranca document major shifts between rain-dominated (fluvial) and wind-dominated (eolian) climates (Bellosi 2010a, b; Bellosi and González, 2010). Given the high erodibility of volcanic ash accumulations and the surface soils they support, one might expect to find variation relating to wet versus dry climate erosion. All other things being equal, variation in the rate of wet climate erosion (or erosivity) depends ultimately on rainfall amount and especially rainstorm intensity, runoff, and overland flow, and the sediment yield, in turn, is influenced by topography and vegetation cover. Under dry climates, variation in rates of erosion by wind depends on soil moisture, wind speed, windstorm intensity, and the unsheltered fetch of the southern South Pacific that links atmospheric conditions over the sea surface to conditions over land. The horizontal and vertical particle flux generated by this erosion is influenced by surface roughness, in particular, vegetation cover. Once mobilized by rain or wind, the eroded sediment load is transported, and when the load under transport exceeds transport capacity, deposition occurs. Thus, the terrestrial record of erosion in Patagonia is preserved only under conditions favoring deposition. The marine record may be different. During intervals when there was no active sedimentation in Patagonia, the products of surface erosion may have been transported away and out over the southwest Atlantic and beyond. The long-distance transport of these pyroclastic minerals may be preserved on the sea-floor as terrigenous sediment or evidence of their fertilizing effect on marine productivity. It will be through the lens of surface processes and temporal coincidence that I will attempt to show that the marine and terrestrial records provide important evidence of coupling and marine conditions in the Southern Ocean that may eventually be related to the rhythms of increasing hypsodonty in Patagonian mammals.

8.2 Climate intimacy between Patagonia and the Southern Ocean

Patagonia is a narrow peninsula projecting southward into the vast Southern Ocean (Figure 8.1) and oceanic climate prevails across Patagonia. Atmospheric temperatures overhead are closely tied to ocean surface temperatures and seasonal temperature ﬂuctuations are characteristically moderated by proximity to the sea. Although air masses off the Paciﬁc warm somewhat as they move eastward across the semiarid steppes of central Patagonia (compare mean annual temperatures [MATs] for Puerto Aysen, Sarmiento, and Comodoro Rivadavia), MATs are closely tied to mean annual sea surface temperatures (SSTs), and the range of atmospheric mean monthly temperatures (MMTs) is constrained by the annual range of mean monthly SSTs in the adjacent oceans (Figure 8.2). 8.2 Climate intimacy between Patagonia and the Southern Ocean 239

Puerto Aysén Sarmiento Comodoro Rivadavia Gran Barranca

Figure 8.1 Shaded relief map of southern South America by the NASA Shuttle Radar Topography Mission (SRTM) and courtesy of the SRTM Team NASA/JPL/NIMA, converted to grayscale (http://photojournal.jpl.nasa.gov/jpegMod/PIA03388_modest.jpg). Rectangle indicates general vicinity of Gran Barranca. 240 The middle Cenozoic of Patagonia

25 Pacific Ocean Mean annual SST 30 Winter & summer SST Annual SST range 35 Atlantic Ocean Winter Summer Mean annual SST 40 Winter & summer SST Sarmiento Comodoro Annual SST range 45 Latitude (°S) Puerto Aysen Global mean SST Atmospheric 50 MAT & MMT amplitude (winter in gray) 55 0 5 10 15 20 25 Temperature (°C)

Figure 8.2 Climate intimacy between Atlantic and Pacific sea surface temperatures and atmospheric temperature over Patagonia. Mean annual temperatures for Puerto Aysen (Pacific coast), Sarmiento (central Patagonia), and Comodoro Rivadavia (Atlantic coast) (large black filled circles) are close to global mean sea surface temperature for their latitude (thick dark gray line). Annual range of mean monthly temperatures for the three terrestrial stations indicated by horizontal bars. The annual range of sea surface temperatures for Atlantic and Pacific Ocean are indicated by rectangles. The annual range of sea surface temperature records are records from a single voyage, not compilations of the mean of all available surface temperature records over the annual cycle for these latitudes.

Between 25 S and 60 S latitude, monthly SSTs range from 6 Cto17C in the Pacific and from 6 Cto23C in the Atlantic Ocean. The difference in latitudinal range and seasonal range reflects both the flow of cold water northward along the Pacific coast and the strike of the Atlantic coastline with respect to the flow of the warm Brazil current and seasonal change in the intensity of the cold Malvinas current that displaces the warm tropical waters from along the eastern coast of Patagonia. The annual range of SSTs in both oceans diminishes southward toward Drake Passage, where Atlantic and Pacific sea surface temperatures converge. The intimacy between SSTs and atmospheric temperatures at 45 S latitude is evident in the instrument records from three meteorological stations: Puerto Aysen on the Pacific coast, Sarmiento in central Patagonia, and Comodoro Rivadavia on the Atlantic coast. The range of atmospheric MMTs at Puerto Aysen is less than the range of MMTs at Sarmiento and Comodoro, a reflection of the more limited seasonal range of SSTs in the Pacific Ocean. Coldest month MMTs at all three stations are less than SSTs, and this reflects the northward movement of cold air with the South Polar Front during the austral winter. Sarmiento and Comodoro MATs are a little warmer than mean annual SSTs at the same latitude, and their total ranges are greater than those of Puerto Aysen, both being expressions of the modest but real “continental” effect over land. The seasonal range of MMTs for Sarmiento is greater than that of Puerto Aysen and fairly closely matches the seasonal range of SSTs in the Atlantic Ocean, except for the coldest month MMTs of the austral winter and the warmest months of the austral summer. MMT range and MAT for Comodoro on the Atlantic coast are shifted or even warmer than Sarmiento, 8.2 Climate intimacy between Patagonia and the Southern Ocean 241

reflecting a further enhanced “continental” effect on atmospheric temperatures as westerly air masses terminate their run over the Patagonian land surface. Given the fundamental fact of climate intimacy and the dominantly westerly flow at these latitudes, southern Pacific Ocean surface conditions are the most important influence on Patagonian climates today, and this was probably so throughout the middle Cenozoic. This assumption seems unavoidable from first principles, regardless of the degree of Southern Ocean continuity through Drake Passage. That is, the westerly flow so characteristic of Patagonia today was a fundamental feature of southern climates throughout the middle Cenozoic. Variation in the latitude of westerly flow and in the intensity of this flow were related directly to the history of Drake Passage. Constraints on the timing of the opening of Drake Passage are few, with estimates of the transition from shallow to deep conditions ranging between 41 Ma and 23.5 Ma, with some estimates for shallow opening as old as the middle Eocene, between 50 Ma and 45 Ma (Livermore et al., 2005, 2007). This lack of constraints has given rise to much speculation about the influence of Drake Passage on the terrestrial biota of Patagonia (Kohn et al., 2010; Figure 23.2). While the opening of this gateway was a “protracted affair,” it has been shown through modeling that even shallow opening results in cooling of the Southern Ocean and the establishment of marine and atmospheric circulation patterns similar to modern ones (Sijp and England, 2004). Just prior to the time Drake Passage began to open in the middle Eocene, westerly flow across the south Pacific was probably north of the latitude of Gran Barranca. Upon reaching the continental shelf and coast of Patagonia, this flow divided into two parts, one limb pushed southward along the coast of Patagonia to the Antarctic Peninsula, and another limb flowed northward. The latitude at which this split occurred has changed through time with the development and influence of the Polar Front. Are there any reasons to suppose that atmospheric conditions along the South Atlantic coast of Patagonia were markedly different from conditions along the Pacificcoast through the middle Cenozoic? There must have been some differences given that Pacific circulation toward Patagonia comes from the west, and Atlantic circulation toward Patagonia came from the north, but the magnitude of this difference is not known. On the Atlantic coast, through much of the middle and late Eocene, the warm Brazil current flowed south along the coast and its influence reached all the way to the Malvinas Plateau. So much for temperature, what about moisture? While the modern Andes interrupts the flow of atmospheric moisture from the west, this orographic influence was less strongly felt during the time of deposition of the Sarmiento Formation. The persistent low mean altitude of the large sediment basins of central Patagonia is testified by the episodic occurrence of marine deposits that extended between coastal Patagonia and Gran Bar- ranca, and the nearly continuous outcrops of marine deposits between the Pacificand Atlantic Oceans (Malumian, 1995; Casadio 1998;Caminos,1999;Náñez,1999). Was there a significant orographic influence from the Patagonian Andes between the middle Eocene and early Miocene? Evidence for Eocene–Oligocene tectonic deformation of a magnitude that would result in ecologically significant orographic effects is not particularly abundant in Patagonia (Ramos, 2005). The configuration of large sediment basins (Austral and San Jorge) and intervening uplands in central Patagonia 242 The middle Cenozoic of Patagonia

has been fairly stable, and the geographic distribution of middle to late Eocene marine invertebrate faunas from east to west across Patagonia (Zinsmeister, 1981; Griffin, 1991; Griffin and Hünicken, 1994; Del Río, 2004) suggests that the floor of the basins was at or near sea-level. An extensive area of uplands existed to the north of Gran Barranca, namely the Northern Patagonian High Plateau, and this feature has existed since the middle Eocene and reached its maximum elevation (>1200 m, or 500 m with respect to the surrounding land) in the late Oligocene (Aragón et al., 2011). Furthermore, the configuration of the Sierra de San Bernardo at this time is not well established. While there is evidence for middle to late Eocene basaltic plateau magmatism, only the abundant pyroclastic material of the Sarmiento Formation (assumed to have originated from sources in western and northwestern Patagonia, but also likely from local sources) suggests the presence of volcanic edifices or uplands (Baker et al., 1981;Mazzoni,1985). It might be argued that source edifices were unlikely to have generated pronounced orographic effects during the middle and late Eocene, as slightly older and contemporaneous paleofloras are floristically rich and provide evidence that abundant moisture reached areas east of the modern axis of the Andes (Hünicken, 1966;Wilfetal.,2003, 2005). However, even modest volcanic topography can produce channel effects that result in ecologically significant local variation in rainfall, wind intensity, and soil moisture.

8.3 Drake Passage

Given the facts of climate intimacy, understanding the chronology and development of westerly atmospheric ﬂow and its ultimate expression in the West Wind Drift and Antarctic Circumpolar Current seems to be at the heart of an appreciation of climate change in Patagonia and environmental inﬂuences on mammalian tooth shape evolution through the middle Cenozoic.

8.3.1 Geometry and history

The most constricted geometry in the circum-Antarctic is the narrow gap between the southern tip of South America and the northern tip of the Antarctic Peninsula. Today, the channel of Drake Passage, between 57.5 S and 64.8 S, has a depth of 3000 m. It attained its modern configuration by widening and deepening over millions of years in the middle Cenozoic. The continent of Antarctica separated from South America and Drake Passage opened to deep water sometime between about 42 Ma and 22 Ma (Scher and Martin, 2006; Livermore et al., 2007). A detailed interpretation of the kinematics and timing based on major change in the motion of South America and Antarctica suggests small ocean basins and a shallow gateway opened during the middle Eocene (Livermore et al., 2005). By this interpretation, the first influx of shallow Pacific water into the Atlantic sector of the Southern Ocean occurred between 45 and 42 Ma, well before the opening of the Tasmanian Gateway (Scher and Martin, 2006). In the interval between 34 Ma and 31 Ma, Australasia 8.3 Drake Passage 243

separated from East Antarctica and major plate motion moved the tip of the Antarctic Peninsula away from southern South America (Lawver and Gahagan, 2003).

8.3.2 The formation of ice in Antarctica

The climate implications of the process leading to the establishment of an Antarctic Circumpolar Current were probably profound (Barker and Thomas, 2004). The opening of Drake Passage to deep circulation is thought to have led to an abrupt and pronounced cooling of deep ocean water and accumulation of glacial ice on Antarctica (Kennett, 1977; Cristini et al., 2012)reflected, at least in part, by the pronounced positive oxygen isotope excursion at the EOT (Zachos et al., 1996). Complex coupled models confirm that opening Drake Passage cools the high-latitude southern hemisphere by about 3 C, at least (Nong et al, 2000; Toggweiler and Bjornsson, 2000). However, the most sophisticated climate modeling of the early history of the Southern Ocean to date reveals greater complexities (Huber, 2001; Huber and Nof, 2006), and that changes in atmospheric carbon dioxide concentrations, followed by ice albedo and weathering feedbacks, could have led directly to the magnitude of change in Antarctic climate at the EOT in the absence of any influence from gateway configuration. Atmospheric carbon dioxide concentrations have been associated with transient SST warming in the middle Eocene (Bijl et al, 2011) when surface currents had a very different pattern of flow and the cooling accompanied ice sheet expansion in Antarctica across the EOT (Liu et al., 2009). It now appears that some combination of atmospheric

pCO2 (Liu et al., 2009), orbital variation (Coxall et al., 2005), circum-Pacific volcanic arc flare-up (Jicha et al., 2009), and changes in the configuration of surface circulation (Katz et al., 2011) accompanied the development of an Antarctic Circumpolar Current. Individually or in some combination, these drove the marine temperature drop that led to the development of an Antarctic ice cap (De Conto and Pollard, 2003; Lear et al., 2008). When did Antarctic ice form? The initial formation of isolated glaciers that reached the sea may have started as early as the late-middle Eocene (41.3–37 Ma), as suggested by the presence of gravel and terrigenous sand (Hambrey et al., 1991; Zachos et al., 1996). Direct records of ice sheet-scale glaciation appear in the late Eocene and at the Eocene–Oligocene boundary (Barker et al., 2007). Ice-rafted debris at ODP Sites 744 and 738 (Kerguelen Plateau) indicates significant permanent ice in East Antarctica along the Waddell Sea in the early Oligocene, beginning about 33 Ma (Ehrmann, 1991; Wise et al., 1992). At that moment, the ice sheet grew to 40% or more of its present size (Barker et al., 1999). In West Antarctica, at the tip of the Antarctic Peninsula, semi- permanent ice reached the coast in the latest Eocene or at the Eocene–Oligocene boundary (Ivany et al., 2006). Much of the general scenario of gradual climate deterioration is documented around the Southern Ocean, and in the Antarctic Peninsula and nearby islands. Climate changed from warm, “non-seasonal,” and wet at about 47 Ma, to strongly seasonal wet conditions at about 42 Ma, followed by generally cool and humid conditions that finally deteriorated further to a cold, frost-prone, and relatively dry climate after about 34 Ma (Dingle et al., 1998). This broad pattern of change from strongly seasonal wet conditions at 42 Ma, to 244 The middle Cenozoic of Patagonia

cold, frost-prone, and relatively dry after signiﬁcant ice formation in Antarctica around 34 Ma, generally is consistent with what can be established in the Sarmiento Formation at Gran Barranca. Finer timescale temporal ﬂuctuations in the balance between polar ice and Patagonian aridity are simply not available in current records.

8.3.3 Deep time climate variability in Patagonia

The most continuous portion of the record at Gran Barranca extends from the base of the Sarmiento Formation up through the Gran Barranca Member and ending with the Lower Puesto Almendra Member. This interval extends from 42.1 Ma to 36.7 Ma, and includes the middle Eocene Climate Optimum. It was a time of a relatively warm and humid climate, dominated by fluvial sedimentation, when temperatures in Patagonia were hospitable to crocodilians. During this time of warm and humid climate, there was a brief interruption when a relatively dry climate appeared over central Patagonia between 38.16 Ma and 37.96 Ma, represented by the eolian-dominated sedimentation of the Rosado Member. It is difficult to find either a Southern Ocean or circum-Antarctic record of this event. Following this brief episode of dry climate, warm and humid climates returned. Following this, there is a hiatus of 1.4–2.6 million years before a longer interval of dry climate and eolian-dominated sedimentation began. These semiarid conditions prevailed during the time the thick tephric loessites of the Vera Member accumulated, between 35.35 Ma and 33.23 Ma. A record of the EOT and Oi-1 is preserved in the sediments of this unit. Following the Vera Member, there was a three-million-year hiatus in sediment accumulation. After this hiatus, the Sarmiento Formation documents the return once again of humid climates to central Patagonia between 30.8 Ma and about 19.0 Ma. Although the continuity of the terrestrial record during this long interval is broken by interruptions and hiatuses of unknown duration, it was during this time that the Antarctic Circumpolar Current became established. A third brief interval of wind-dominated dry climate is revealed by the sediments of the upper Colhue-Huapi Member, ranging in age from 19.04 Ma to 18.62 Ma. Thus, sediments of the Sarmiento Formation at Gran Barranca preserve three intervals of eolian-dominated deposition (Table 8.1). These three dry climate periods were relatively brief, the Rosado Member (38.16–37.96 Ma), the Vera Member (35.35–33.23 Ma), and the upper Colhue-Huapi Member (19.04–18.62 Ma). Age control on these terrestrial units permits tying them to particular times and conditions in the surrounding oceans.

8.4 Paleotemperature and paleoprecipitation

Today, MAT and seasonal atmospheric temperature over Patagonia are an intimate reﬂection of SSTs in the adjacent oceans. This was probably true in the past. During the middle Cenozoic, paleotemperature data from the marine record comes in two forms, 8.4 Paleotemperature and paleoprecipitation 245

global compilations that have yielded the iconic record of global mean deep ocean paleotemperatures (Zachos et al., 1996) and higher resolution records of Southern Ocean deep and surface water paleotemperatures for intervals of the Eocene and Oligocene (Bohaty and Zachos, 2003; Liu et al., 2009). In addition to these, there are equator-to-pole latitude temperature gradients for time slices in the middle Eocene, late Eocene, and Oligocene (Bijl et al., 2009; Hollis et al., 2009). Climate intimacy predicts that SSTs in the surrounding oceans should agree with estimates of MAT over Patagonia. Estimates of MAT and constraints on the range of MATs have been obtained from the middle Eocene and Oligocene record of paleofloras in Patagonia (Hinojosa, 2005) and thresholds of mean atmospheric temperature from the occurrences of crocodilians and palms. However, temperature alone will not account for the intensity of surface processes. Rainfall is equally important. For the purpose of characterizing the alternation of wet and dry climates (and fluvial and eolian depositional environments), paleoprecipitation estimates from paleosol characteristics, stable carbon isotopes, and macrofloras are also required.

8.4.1 Marine paleotemperatures

The highest resolution oxygen isotope paleotemperature records are from benthic foraminifera in the Southern Ocean ODP/DSDP holes 689 and 690 on the Maud Rise in the SE Atlantic sector of the Southern Ocean, and holes 738, 744, and 748 on the Kerguelen Plateau in the Indian Ocean sector (Bohaty and Zachos, 2003). These records include oxygen isotope curves for the “fine fraction” (SSTs) of ODP/DSDP Holes 738 and 748 that are about 1.0 ppm lower (or 5 C warmer) than deep water temperatures. These records reveal a general trend of surface water cooling by as much as 7 C between 49 Ma and 37 Ma (Bohaty and Zachos, 2003), the interval represented by the oldest sediments of the Sarmiento Formation. This general trend is broken by (1) a significant warming event between 42 Ma and 41 Ma (peaking at 41.4 Ma) termed the middle Eocene climatic optimum or MECO (Bohaty and Zachos, 2003), represented by the lower part of the Gran Barranca Member in central Patagonia; (2) a weaker late Eocene warming between 37 Ma and 35.5 Ma (with peak warm temperatures at around 36.25 Ma), represented by the Lower Puesto Almendra Member; (3) the Vanhof cooling event between 35.5 Ma and 35.0 Ma (see Bohaty and Zachos, 2003) that occurred during the hiatus of Discontinuity 5; and (4) the initiation of rapid cooling and/or an increase in ice volume at 34.0 Ma (Zachos et al., 1996; Coxall et al., 2005) with Oi-1 glacial maximum from 33.5 Ma to 33.0 Ma (Zachos et al., 1996; Bohaty and Zachos, 2003) or 33.6–33.5 Ma (Coxall et al., 2005), represented by the Vera Member. The transition between wet and dry climate in the early Miocene Colhue-Huapi Member is not well represented in the Southern Ocean record. Liu et al. (2009) compiled sea-surface paleotemperature records using alkenone unsaturation and tetrather indices at DSDP/ODP sites 277, 511, and 1090 from latitudes comparable to Gran Barranca around the Southern Ocean. The DSDP Site 511 SST cooling trend begins at about 37 Ma, and describes a smooth descent all the way to 33 Ma, involving a nearly 10 C drop in SST. This confirms that the transition to Oi-1 was 246 The middle Cenozoic of Patagonia

Table 8.1 Alternation of rain- and wind-dominated climates during the middle Cenozoic of Patagonia

Unit/age range (Ma) or duration (myr)1,2 Fluvial (wet climate) Eolian (dry climate)

RAIN WIND Upper Colhue- Eolian. Thick tephric loessites3; Huapi Mbr calcic entisols, aridisols, sparse 19.04–18.62 Ma grasses, MAP¼200–400 mm4; permanent ice in Antarctica6 Lower Colhue- Bed-load fluvial system with Huapi Mbr lenticular clast-supported intra- 21.11–19.04 Ma formational conglomerates, cross- bedded tufoarenite channel bodies3; moderately developed alfisols, MAP¼700–1000 mm4 Discontinuity 10 Deep fluvial erosion, vertical relief 0–1.17 myr 25–50 m2 Upper Puesto Fluvial. Lenticular clast-supported Almendra Mbr intra-formational conglomerates and 30.77–21.11 Ma cross-bedded tufoarenites, basalt breccias3; moderately developed stacked alfisols and ultisols, seasonal rainfall, subhumid to humid conditions, MAP¼900–1200 mm4; Antarctic Circumpolar Current established 23.95 Ma5 Discontinuity 6 Deep fluvial erosion, vertical relief 2.46–2.96 myr 105 m2 Vera Mbr Eolian. Thick massively bedded 35.25–33.23 Ma tephric loessites3; with scarce weakly developed calcic entisols, aridisols, andisols, semiarid conditions, increased rate of eolian sediment supply, MAP¼200–600 mm4; continuous deep–intermediate flow through Drake Passage6; appearance of polar front; major continental-scale Antarctic ice sheet growth at Oi-1 (about 33.6–33.5 Ma); 70 m drop in sea-level7;2–4 C SST cooling5; increased marine productivity8 Discontinuity 5 Fluvial erosion, vertical relief 18 m2 Late Eocene warming event 1.42–2.58 myr Lower Puesto Fluvial, lenticular clast-supported Almendra Mbr intra-formational conglomerates and 38.03–36.67 Ma cross-bedded tufoarenite channel bodies3; moderately developed alfisols, subhumid conditions, rainstorms, MAP¼700–1000 mm4 8.4 Paleotemperature and paleoprecipitation 247

Table 8.1 (cont.)

Unit/age range (Ma) or duration (myr)1,2 Fluvial (wet climate) Eolian (dry climate)

Discontinuity 4 Fluvial erosion, vertical relief 8 m2 Rosado Mbr Eolian. Thick massively bedded 38.16–37.96 Ma tuffite3; aridisol, xeric conditions, MAP<400mm4;intermediateto shallow water through-flow at Drake Passage6; Antarctic glacial advance9 Discontinuity 3 Fluvial erosion, vertical relief 10 m2 0.44–1.03 myr Gran Barranca Fluvial, bentonites or weathered Loessic sedimentation, absence of Mbr smectite, ephemeral small lakes, fluvial reworking3; semiarid 42.11–38.16 Ma crocodilians3; subhumid to humid conditions4; brief glacial (41.5–40.6 conditions, andisols, vertisols, Ma)9;influx of shallow Pacific MAP¼400–1000 mm4 seawater into Atlantic Sector of Southern Ocean (41.3–39.6 Ma)10; immediately follow the MECO (42.2 – 41.4 Ma)11 45–42 Ma Shallow flow through Drake Cañadon Vaca or Passage begins6,9; temporary ice the Kolhuel- reaches sea-level in Antarctica9; Kaike Fm drop in sea-level7

1 Sarmiento Formation members maximum intervals (Ma) and discontinuity minimum and maximum durations (myr) from Dunn et al., 2013. 2 Bellosi, 2010a. 3 Bellosi, 2010b. 4 Bellosi and González, 2010. 5 Pfuhl and McCave, 2005. 6 Livermore et al., 2007. 7 Pekar et al., 2002, 2005. 8 Salamy and Zachos, 1999; Latimer and Filippelli, 2002. 9 Scher and Martin, 2004, 2006. 10 Tripati et al., 2005. 11 Bohaty and Zachos, 2003; Bohaty et al., 2009. not abrupt in Patagonia, and the abruptness is an ice volume effect. The smoothness of this transition might seem to imply that atmospheric pCO2 was driving the middle-late Eocene cooling trend in SSTs and the rapidly steepening latitudinal temperature gradient between 35 S and 50 S latitude. There was more abrupt and substantial cooling between 34 Ma and 33 Ma. More than >5 C cooling from the late Eocene to early and mid-Oligocene at DSDP Site 511 (where there is also an EOT record), and as much as 8 C cooling at higher latitudes at DSDP Site 277 and ODP Site1090. At DSDP Site 511, SSTs reached their lowest value at the same time as the benthic δ18O excursion at about 33.5 Ma. Importantly, late Eocene high-latitude SSTs were about 20 C. DSDP Site 277 on Campbell Plateau, 248 The middle Cenozoic of Patagonia

Table 8.2 Estimates of mean annual temperature (MAT), coldest month mean temperature (CMMT), and warmest month mean temperature (WMMT), based on leaf morphology in four fossil ﬂoras from southern South America (Hinojosa, 2005)

Flora Approx. age (Ma) MAT (C) CMMT (C) WMMT (C)

Ñirihuau inferior 46 17.9 11.3 24.9 Ñirihuau medio 34 15.3 7.4 22.8 Navidad-Goterones 27 16 8.5 21.9 Los Litres 19 17 9.9 22.4

south of New Zealand in the southern South Paciﬁc Ocean, was extraordinarily warm, but the record from DSDP Site 511 in the South Atlantic Ocean indicates that the early K’ Oligocene U 37 SST was only about 3–6 C warmer when compared with the same location today. That is to say, that SSTs at the latitude of the Malvinas Plateau during Oi-1 were 3–6 C warmer than today.

8.4.2 Atmospheric paleotemperatures

Hinojosa (2005) estimates MAT and the annual amplitude of MMTs for the warmest and coldest months (WMMT, CMMT) for a sequence of four Patagonian paleoﬂoras (Table 8.2). Atmospheric MATs were relatively constant over Patagonia through the interval of time preserved in the Sarmiento Formation, and this is particularly true for WMMT. The coldest MAT is associated with the EOT. Most variation in this interval is observed in the CMMT. Two temperature-sensitive organisms, palms (Strömberg et al., 2013) and alligators (Simpson, 1933), were present in Patagonia during the middle Cenozoic (Figure 8.3). Palms persisted throughout the interval represented by the Sarmiento Formation at Gran Barranca, far beyond the last occurrence of alligators in the middle of the Gran Barranca Member. These two organisms provide useful additional constraints on atmospheric paleotemperatures.

8.4.2.1 The southern limit of Alligatoridae The crocodilian Eocaiman was collected from Simpson’s Y Guide Level or Tuff at Profile A (Simpson FieldBook specimen 55), the only specimen of crocodilian ever collected from the Sarmiento Formation at Gran Barranca (Simpson, 1933). This record of Eocaiman cavernensis (Simpson, 1933) at Simpson’s Y at 39.1 Ma (Chron C18n.2n) at Gran Barranca is the last record of Alligatoridae in Patagonia. For crocodilians to have been present in Patagonia at this time, atmospheric temperatures must have been at least warm temperate with only moderate seasonality and a hydrology supporting permanent streams and complex fluvial systems (Gasparini, 1981). The most southern species of living alligatorid is Caiman jacare in the esteros del Iberá at about 30 S latitude. There are two species of Caiman in the fluvial system of 8.4 Paleotemperature and paleoprecipitation 249

Modern mean annual sea-surface temperatures for the southern hemisphere

10 Lat (°S)= -57.052 + 1.055 SST + 0.014 (SST)2 R2=0.847

30 Limit of Alligatoridae (Argentina) Limit of palms (Chile)

40 Latitude (°S) Limit of palms (New Zealand) Latitude of Gran 50 Barranca

70 -5 0 5 10 15 20 25 30 Annual mean sea-surface temperature (°C)

Figure 8.3 The latitudinal limits of Alligatoridae and palms in southern South America and New Zealand today in relation to annual mean sea-surface temperature. Today, Alligatoridae are not found south of about 32 S latitude, corresponding to a sea-surface temperature of about 18.5 C. Palms do not occur south of about 36 S latitude in South America and 44 S latitude in New Zealand. These southern limits of the distribution of palms corresponds to a mean annual sea- surface temperature along the coast of between 10.5 C (in New Zealand) and 16.5 C (in Chile). the Paraná–Paraguay–Rio de la Plata, Caiman latirostris in Chaco and Misiones provinces and Caiman jacare that formerly reached approximately 32 S prior to signiﬁcant human disturbance. Thirty degrees S latitude today corresponds to a global mean annual SST in adjacent coastal waters of between 18 C and 19 C. At the latitude of the esteros del Iberá, Caiman hibernates in winter as atmospheric temperatures reach as low as –3.0 C. Eusuchian crocodilians in South America are also limited in their distribution by the suitability of nest sites, and their survival in seasonal environments at this latitude, where atmospheric temperatures can freeze in winter, requires large low-energy ﬂuvial systems supported by mean annual precipitation (MAP) in the range of 1200–2300 mm in warmer headwaters. Shortly after their last occurrence at Simpson’s Y at 39.1 Ma, there was a brief but pronounced episode of dry climate and wind-dominated sedimentation. The relationship between water temperature and crocodilian distribution is made complex by the 22 C difference between critical minimum body temperature (the extreme limit of individual survival) and the environmental temperature activity range 250 The middle Cenozoic of Patagonia

for thriving viable populations capable of successful reproduction (MATs range optimally between 25 C and 35 C) (Markwick, 1998a, b). Markwick (1998a, b) documents a mid-Eocene peak in crown-group crocodilian diversity globally and an abrupt decline in diversity in the late Eocene. This decline is calibrated to have occurred sometime between 38 Ma and 36 Ma, with a slight additional decrease in diversity in the early Oligocene. Markwick’s data show a retraction in paleolatitude range from high latitudes in the northern hemisphere in the late Eocene. This appears now to be what happened in Patagonia and suggests that the local extirpation of crocodilians in Patagonia sometime after 39.1 Ma might have been in response to global change, rather than or in addition to regional climate drying.

8.4.2.2 The southern limit of palms Globally, the extreme limits of palm distribution today are 44NinEurope(Chamaerops humilis) and 44.3SinNewZealand(Rhopalostylis sapida). In South America, palms occur as far south as the Argentine pampas (Trithrinax) and Central Chile (Jubaea). Trithrinax in south subtropical South America is among the most cold- and drought- resistant American palm and is considered one of the least specialized genera (Henderson et al., 1997). In Argentina, Trithrinax occurs as far south as Córdoba, Entre Rios, Salta, San Luis, Santa Fe, and Tucuman provinces, and also in western Uruguay. Jubaea chilensis in Chile reaches as far south as 36 S (Aconcagua, O’Higgins, Valparaiso), but is most abundant between 32 Sand35S (Henderson et al., 1997). Forty-four degrees S latitude today corresponds to a global annual mean SST in surrounding waters of Patagonia of about 10 C (with a range between 8 Cand13C). The southern limit of palms in South America at about 36 S corresponds to an annual mean SST of about 16 C (with a range between 13 Cand22C). In New Zealand, palms occur at the extreme limit of palm distribution globally. At least part of the explanation for the presence of palms this far south in New Zealand has to do with the fact that the climate there is frost-free and sea-level climates are moderatedbymaritimeinﬂuences. The palm Rhopalostylis sapida occurs mainly or exclusively along the coast at the southern limit of its distribution. The southernmost occurrence of Nikau (Rhopalostylis sapida) palm is at 44.18 Slatitudeinthe Chatham Islands (800 km to the east of the South Island of New Zealand). On the west coast of the South Island it reaches to latitude of 42.28 S, and on the leeward east coast to 43.46 S. Rhopalostylis is frost tender, and like many plants in New Zealand, the southern limit of its distribution is described best by the CMMT (Table 8.3). By these examples from the southern hemisphere, palms could have survived along Patagonian coastlines under oceanic climates down to MAT of 11–12 C, with a CMMT of about 8 C, and a seasonal temperature amplitude of about 8 C. As palms are fairly common in phytolith assemblages throughout the Sarmiento Formation at Gran Barranca, it is unlikely that climate conditions this severe were ever established over Patagonia at any time during the middle Cenozoic. 8.4 Paleotemperature and paleoprecipitation 251

Table 8.3 Climates at the southernmost distrubution of Rhopalostylis palm on the east and west coasts of the South Island of New Zealand and Chatham Island

West coast East coast South Island East Coast South Island Chatham Island (Greymouth) (Banks Peninsula) 44.18 S 42.28 S 43.46 S

MAT (C) 11.1 12.1 12.2 ColdestMonthMT (C) 7.6 7.9 7.7 AmpMMT (C) 7.2 8.1 9.2 MAP (mm) 913 2488 993

8.4.3 Paleoprecipitation

At least five approaches have been used to estimate precipitation in Patagonia during the time of deposition of the Sarmiento Formation: (1) characteristics of the sediments that suggest semiquantitative estimates of a range of MAPs consistent with modern depositional environments (Bellosi and Gonzalez, 2010), (2) quantitative methods of rainfall estimation from the weathering of paleosol oxides following Sheldon et al. (2002), (3) a rough index of relative dryness based on the prevalence of arid-adapted plant taxa in pollen and leaf floras (Barreda and Palazzesi, 2007), (4) quantitative estimates of MAP derived from leaf shape in paleomacrofloras using modern analog floras (Hinojosa, 2005), and (5) quantitative estimates of MAP from stable carbon isotopes in mammalian tooth enamel (following Kohn, 2010).

8.4.3.1 Sedimentology The macro- and microscopic attributes of paleosols in the Sarmiento Formation (mineral alteration and clay composition by chemical weathering) suggest that MAP was never more than about 1100 mm and never drier than about 300 mm (Bellosi 2010b; Bellosi and Gonzalez, 2010). This range is consistent with modern Argentine environments where arid climates have <250 mm, semiarid between 250 mm and 500 mm, dry pampas in the interior with <700 mm, humid pampas along the coast with 900 mm; the chaco that varies from semiarid to semihumid from west to east or between 600 mm and 1300 mm MAP, where vegetation is a mosaic of lakes, swamps, reed-beds, and gallery forests. Thus, Patagonian environments varied between these extremes during the middle Eocene–early Miocene. The wettest and warmest conditions during Sarmiento times are found in the Lower Puesto Almendra Member (Mustersan) when MAP was 1044 mm (with a range of error around 150 mm) and MAT >13 C (Bellosi and Gonzalez, 2010). By comparison, the humid pampas today gets between 700 mm and 1200 mm MAP; at the high end of this range conditions are considered humid, and in other places at the lower end of this range they are considered subhumid. These conditions are comparable with the precipitation on the North Island of New Zealand today where MAP varies between 1000 mm and 1500 mm on an island that was forested before the arrival of Polynesians and the conversion to pasture by Europeans. 252 The middle Cenozoic of Patagonia

Along the spectrum between 300 mm and 1100 mm MAP, the driest intervals of the Sarmiento Formation correspond to the Rosado Member (MAP <400 mm), the Vera Member (MAP¼200–600 mm), and the upper Colhue-Huapi Member (MAP¼200–400 mm). The only truly arid conditions, implying moisture deﬁcits and insufﬁcient rainfall to support trees or woody plants, occurred during the Vera and again in the upper Colhue-Huapi Members. Conditions of semiarid climate with an MAP of between 250 mm and 500 mm were almost certainly not found in Patagonia during the middle Eocene–early Miocene (Zucol et al., 2010;Strömberg et al., 2013).

8.4.3.2 Paleosol oxides Estimates of MAP have been provided by Bellosi (personal communication, November 21, 2013) for select paleosol levels of the Sarmiento Formation, using a method based on the weathering geochemistry of oxides of aluminum, calcium, sodium, and magnesium in the B horizon (Table 8.4), following Sheldon et al. (2002). The age of the samples can be fairly precisely determined from the age model of Dunn et al. (2013). Sheldon’s method was developed for conditions in the mid-continent of North America. When applied to the very different paleosols and soil parent material of the Eocene and Oligocene of Patagonia, this method yields relatively unvarying estimates of MAP in the narrow range between 800 mm and 1000 mm. In general, these values indicate humid to subhumid conditions, even during the two intervals of relatively dry climate when eolian sediment deposition prevailed in central Patagonia.

8.4.3.3 Arid-adapted plant taxa There is paleobotanical evidence from the percentage of arid-adapted taxa in Patagonian paleoﬂoras and pollen assemblages suggesting a change to drier environments beginning in the late Oligocene. This drying trend became especially prevalent when arid- adapted taxa came to comprise >80% of plant taxa in the middle to late Miocene, after deposition of the Sarmiento Formation (Barreda and Palazzesi, 2007). By their interpretation of the available record, forests and woodlands persisted across Patagonia and vegetation did not become open until about the middle Miocene with the expansion of xerophytic-adapted shrubby and herbaceous taxa.

8.4.3.4 Leaf morphology Hinojosa (2005) assigns approximate ages to a sequence of seven Patagonian paleofloras from latitudes between 33 S and 52 S and estimates mean annual precipitation (MAP) trends from their leaf morphology (Table 8.5). The analysis used linear and multivariate methods and a modern reference dataset of 161 sites comprising the CLAMP3 dataset supplemented with 17 floras from Bolivia and Chile (excluding the coldest and driest continental sites outside the range of modern South American climates). The age of the paleofloras is estimated for each site. One might question some of these ages, especially the floras from the Navidad Formation in Chile, the ages 8.4 Paleotemperature and paleoprecipitation 253

Table 8.4 Estimates of MAP for the Sarmiento Formation at Gran Barranca (courtesy of Eduardo Bellosi), as calculated from the geochemistry of B horizon oxides of Al, Ca, Na, and Mg (following Sheldon et al., 2002)

MAP (mm) Mean of estimates Member/unit for stratigraphic unit Stratigraphic level 1Age MAP (mm)

Gran Barranca 798 Simpson’s Y (95–06) 39.86 798 Sample CC3 Lower Puesto 980 Unit 1 (95–08.5) Sample 38.03 915 Almendra Unit CC5 1 or GBV-3 Rosado Member Unit 1 (95–08.5) Sample 1044 CC6 Lower Puesto 934 Unit 2 “Mustersan” 37.48 1017 Almendra Unit 2 (95–10.2) Sample CC19 Unit 2 “Mustersan” 850 (95–10.2) Sample CC20 Vera Member 853 La Cancha Profile 33.58 850 K Aridisol–Andisol Sample DD2 La Cancha Profile 850 M Andisol (Mn) Sample CC10 La Cancha Profile 858 M Andisol (Mn) Sample CC11 Upper Puesto 904 Unit 5 (95–14.5) Alfisol 22.94 915 Almendra Sample CC25 Unit 5 (95–14.5) Alfisol 893 Sample CC26 Unit 5 (95–16.6) Alfisol 882 Sample CC35 Unit 5 (95–16.5) Alfisol 22.71 906 Sample CC36 Colhue-Huapi 870 (95–19) Alfisol (Alf) 20.89 818 Member Sample CC44 (Lower) (95–19) Alfisol (Alf) 905 Sample CC45 (95–19) Alfisol (Alf) 888 Sample CC46

1 Dunn et al., 2013. of which are intensely debated (Finger et al., 2013). Estimates of MAP based on leaf morphology through the middle Cenozoic of southern South America range from 517mm to 1115 mm (Table 8.5), similar to the 300–1100 mm range estimated by Bellosi and Gonzalez (2010) for the Sarmiento Formation. 254 The middle Cenozoic of Patagonia

Table 8.5 Estimates of atmospheric temperature (MAT, CMMT, and WMMT) and rainfall (MAP) from leaf macroﬂoras in Patagonia from the middle Eocene to middle Miocene (Hinojosa, 2005)

Approx. MAP MAT CMMT WMMT Flora age (Ma) (mm) (C) (C) (C)

Rio Turbio (51.5 S) 52 1028 17.5 10.7 24.6 Ñirihuau inferior (41 S) 46 570 17.9 11.3 24.9 Ñirihuau medio (41 S) 34 876 15.3 7.4 22.8 Cerro Las Aguilas (33.2 S) 30 756 Navidad-Goterones (34 S) 27 1115 16 8.5 21.9 Los Litres 19 929 17 9.9 22.4 Navidad–Boca Pupuya (34 S) 17 517 21.40 15.8 24.8

Table 8.6 Estimates of MAP using stable carbon isotope ratios in mammalian enamel apatite

Unit (age range) MAP (mm) Error (mm)

Gran Barranca Mbr (42.1–38.2 Ma) 580 þ/180 Rosado Mbr (38.2–38.0 Ma) 420 þ/110 Vera Mbr (35.3–33.2 Ma) 400 þ/160 La Cantera 520 þ/160 Upper Puesto Almendra Mbr (30.8–21.1 Ma) 700 þ/180 Lower Colhue-Huapi Mbr (21.1–19.0 Ma) 800 þ/160

Note: these values do not take calibration errors into account; thus there may be systematic offsets. It is the evidence of change that is most relevant.

8.4.3.5 Stable carbon isotopes Kohn et al. (2011) estimated MAP for six fossil mammal-bearing levels of the Sarmiento Formation using the general relationship between δ13C and MAP (Kohn, 2010). These estimates are derived from tooth enamel collected at a single stratigraphic level or levels referred to the same SALMA (South American land mammal age) (Table 8.6). The general trends are consistent with the observed alternation of wet and dry climates; that is, the Gran Barranca, Upper Puesto Almendra, and Lower Colhue-Huapi members were wetter. However, the amount of annual rainfall during these wet climate intervals is low (580–700 mm MAP), except for the Lower Colhue-Huapi Member (800 mm MAP). Drier conditions are found in the Rosado and Vera members (420 mm and 400 mm MAP, respectively) and these values are within the range of MAP for semiarid climates consistent with eolian sediment deposition (Bellosi, 2010b; Bellosi and Gonzalez, 2010). However, the total range of values of estimated MAP for the Sarmiento Formation (520–800 mm) by Kohn et al. (2011) are generally less than the range of estimates from sedimentology and paleosol geochemistry (Bellosi, 2010b), and leaf morphology (Hinojosa 2005). 8.5 Volcanic activity 255

Table 8.7 Estimates of mean annual precipitation (MAP in mm) for the middle Cenozoic of Patagonia

Unit of the Sarmiento Fm or Approx. Leaf paleoﬂora age (Ma) Sediments Oxides ﬂora δ13C

Rio Turbio 52 1028 Ñirihuau inferior 46 570 Gran Barranca Member 42.1–38.2 400–1000 798 580 Rosado Member 38.2–38.0 <400 420 Lower Puesto Almendra Member 38.0–36.7 700–1000 934 Vera Member 35.3–33.2 200–600 853 876 400 Upper Puesto Almendra Member 30.8–21.1 900–1200 904 756 520 Navidad-Goterones 27 1115 700 Lower Colhue-Huapi Member 21.1–19.0 700–1000 870 929 800 Upper Colhue-Huapi Member 19.0–18.6 200–400 Navidad-Boca Pupuya 17 517

8.4.4 Discussion

When estimates of MAP from such diverse sources of evidence yield similar values, or their ranges overlap, there is probably good reason to believe them (Table 8.7). Annual rainfall in Patagonia was probably never above 1200 mm at any time between the middle Eocene and middle Miocene. Annual precipitation ﬂuctuated throughout the middle Eocene–Oligocene corresponding with the alternation between wet and dry climates, while mean annual atmospheric temperatures remained fairly constant, and high-latitude SSTs in the South Atlantic, Campbell Plateau off southern New Zealand, describe a smooth overall descent of nearly 10 degrees, punctuated by a more rapid descent at the EOT.

8.5 Volcanic activity

Both the generation of fresh volcanic ash and of the availability of volcanic ash accumulations to surface processes probably contributed to tooth shape evolution in Patagonia. Eruption activity in Patagonia today (e.g., Hudson, Chaitén, and Puyehue- Cordón Caulle) tends to have ephemeral effects on tooth wear as the ash clouds are widely distributed and their generally shallow surface deposits are rapidly blown away by the prevailing winds. However, deﬂation off thicker accumulations including older pyroclastic sediments have longer-term consequences. In this sense, even today, the Sarmiento Formation in Patagonia serves as a source of ﬁne-grained glass-rich dust. When mobilized by wind, these surfaces give rise to non-eruptive tephric dust plumes. Their frequency of mobilization is as regular as the seasonal variation in soil moisture and wind intensity. Such accumulations can remain potential sources of atmospheric dust millions of years after their origin. This suggests that erodible or actively eroding unconsolidated pyroclastic sediments, regardless of whether these are recent ash falls, volcanic ash soils (andisols) 256 The middle Cenozoic of Patagonia

or their relic ash parent materials, or fine-grained Cenozoic sediments, all potentially contribute to the soil load on plant surfaces and ingested soil. The crucial variables driving the contribution of all these sources of ash to surface flux (environmental abrasiveness) are their texture and consolidation, aridity, plant cover, and the potential of wind to detach, entrain, and transport. During Sarmiento times, there were pre-existing pyroclastic sediments on the Pata- gonian land surface, including the extensive Cretaceous units of the Chubut Group (especially the Cerro Barcino and Bajo Barreal Formations), and the Las Flores and Kolhue-Kaike Formations of the Paleogene–Rio–Chico Group (Manassero et al., 2000; Raigemborn et al., 2009; Umazano et al., 2009). However, not all of these units are unconsolidated. In fact, these are all uniformly clay rich, and the detrital clay that originated as volcanic ash was altered to varying extents by chemical or mechanical weathering. In particular, Rio–Chico Group sediments were consolidated by clay content and forest-cover (Raigemborn et al., 2009), and probably never subjected to significant erosion either around the time of deposition or subsequently. Whether these older units ever formed part of the mineral particle flux during Sarmiento time must await detrital zircon analyses of Sarmiento Formation sediments. By contrast with these pre-existing pyroclastic units, the Sarmiento Formation is notable for its relatively low clay content, the absence of clay altogether, or its weakly weathered condition. These are hallmark features of the Sarmiento Formation that explain its almost uniform pale coloration. The temporal coincidence between the age of the base of the Sarmiento Formation and the initiation of the opening of Drake Passage, and the onset of the evolution of hypsodonty is not mere coincidence. The most conspicuous effect of the process of development of Drake Passage on Patagonian terrestrial environments are the winnowing of clay-sized particles out of the pyroclastic products of Andean volcanism and the absence of weathering and detrital clay. These features of the sedimentology mark the intensification of prevailing westerly atmospheric flow across Patagonia. Although the area of Patagonia affected by the mobilization of pyroclastic material of the Sarmiento Formation is difficult to constrain geographically, tracing the geographic source or sources of the pyroclastic sediments of the Sarmiento Formation tells us something about the timing and place of origin, and the direction of transport. Coincident dates of a rather imprecise nature, rather than direct geochemical tracing, are the only currently available way of identifying potential sources of Sarmiento Formation pyroclastic material. Originally thought to have originated from sources in northwestern Patagonia (Mazzoni, 1985), the suspected source areas of these pyroclastics now appear to have varied in time and geography (Aragón et al., 2011). Potential source volcanics include: (1) shield volcanoes of the Pilcaniyeu belt north of Lake Colhue-Huapi during deposition of the Gran Barranca Member (Ardolino et al., 1999), (2) explosive activity in the El Maitán Belt or atop Somún Curá during deposition of the Vera and UPA members, (3) local intraplate sources associated with polygenic basic to alkaline magmatism in the immediate vicinity of Gran Barranca contemporaneous with deposition of the UPA Member (Paredes et al., 2008), and (4) arc volcanism along the Andean axis that is partially contemporaneous with the Colhue-Huapi Member in the early Miocene (Aragon et al., 2011). 8.5 Volcanic activity 257

In general, the geographic sources of Sarmiento Formation ash were eruptive centers located to the north, northwest, and west. They were transported to the south and southeast during Sarmiento time by both eolian and ﬂuvial transport, and although we refer to Sarmiento Formation pyroclastics as distal ash deposits, the distances transported were not great.

8.5.1 Andisol erodibility

Andisols are soils derived from tephra or pyroclastic material and have unique properties inherited from or associated with this parent material. Not all volcanic ash soils are andisols, as there are tephra-derived spodosols, inceptisols, mollisols, and oxisols, and there are andisols derived from mixed tephra and loess. Yellow-brown loams and yellow-brown pumice soils are andisols in New Zealand. Their geographic distribution closely parallels the distribution of active volcanism along the Andesite Line and the Pacific “Ring of Fire,” including Washington and Oregon states in the United States, Nicaragua in Central America, Colombia, Ecuador, Peru, Bolivia, Chile, and Argentina. Geologically young, this ash-rich volcanism has characteristically high explosion indices typical of their andesitic source. The distribution of andisols also extends along the Apline–Himalayan volcanic belt that extends from the Canary and Madeira islands through the Mediterranean, including Italy, Sicily, and Sardinia. The active volcanoes of the Red Sea and great Rift Valleys of Kenya, Tanzania, and Ethiopia are less violent and have lower pyroclastic production. For this reason, a map of the distribution of andisols fairly accurately depicts the distribution of active volcanism, but it does not map accurately the geographic distribution of volcanic ash and the reworked products derived from accumulations of pyroclastic material. Distributed by water and wind, the contribution of pyroclastics to soil parent material extends to an area much greater than the mapped distribution of andisols. Soils developed on fresh tephra deposits have low bulk density, high specific surface area, strong aggregation of particles, and are generally associated with low erodibility and high structural stability, and are sometimes considered erosion-resistant (Shoji et al., 1993). However, under different conditions in dry and windy climates, soil drying induces severe erosion (Warkentin and Maeda, 1980), soil formation is slow, vegetation cover reduced, and protecting dura-crusts do not form in the brief rainy seasons. Furthermore, when the tephric parent material has been winnowed by wind and the finest fraction removed and the concentration of unweathered glass increased, the properties of cohesion, strong aggregation, and stability decrease. Soils that develop on parent material that is derived from the accumulation of weathered, winnowed, and eroded pyroclastic sediments, transported from volcanic source areas and everywhere in between, while not technically andisols, have distinct properties of higher erodibility.

8.5.2 Erosion of the Sarmiento Formation

Volcanic glass is the most abundant constituent of the Sarmiento Formation at Gran Barranca, and is usually fresh and angular; the primary evidence for transport in suspension by wind. Despite the fact that their erodibility has never been assessed, 258 The middle Cenozoic of Patagonia

the Sarmiento Formation provides indirect records of erosion and surface sediment flux in central Patagonia in at least five ways: (1) dominant depositional environment (eolian or fluvial), (2) erosional unconformities (indicating change in mode from deposition to erosion and local erosional relief), (3) change in linear sedimentation rates, (4) change in rates of pyroclastic sediment supply, and (5) the temporal distribution of tephric loessites (that indicate active eolian processes). For example, there are no erosional unconformities or temporal hiatuses signifying breaks in sediment accumulation during the interval of accelerated hypsodonty in the Rosado Member between 39.1 Ma and 38.2 Ma, and no erosional unconformities during deposition of the Vera Member in the course of the second interval of dry climate and sustained eolian-dominated deposition during at least part of the second interval of accelerated hypsodonty. Eolian processes dominate throughout the Rosado and Vera Members, and also during the Upper Colhue-Huapi Member. Sedimentation rates increased from low in the Gran Barranca Member to relatively high during the one-million-year interval of increasing faunal hypsodonty represented by the Rosado Member (Table 8.8). Sedimentation rates were higher still during the interval represented by the Vera Member, especially during Oi-1 just after the La Cancha level. After an interval of low sedimentation rates during the fluvial Upper Puesto Almendra and Lower Colhue-Huapi members, linear sedimentation rates were high through the Upper Colhue-Huapi Member when eolian processes dominate deposition.

8.5.3 Tephric loessites

Until only very recently, most evidence for dry climates in the Sarmiento Formation has been features or types of paleosols (Bellosi, 2010b) or abundant fine-grained loessite sediments deposited through eolian processes. The model of loess sedimentation described by Bellosi (2010b) is the classic model of the accumulation of uniformly fine-grained sediments by wind under subhumid to dry moisture conditions and cool to cold temperatures analogous to “glacial” conditions. The general association of loess (or fine-grained loessites) with dry climates and denuded land surfaces of sparse or low vegetation (such as deserts and dry grasslands) during arid climate phases is well established (Pye 1995;Kemp2001). Most studies of aerosol dust, its transport, and its significance for loess deposition concentrate on the dry lands of continental interiors (the loess plateau of northern China, the Sahara and Sahel, the Palouse and the arid western interior of North America, Central Europe, Australia, Tibet, the Sinai, and elsewhere across the Middle East) or arid islands (Crete in the eastern Mediterranean, the Canary Islands), and with glacial-interglacial cycles of the Quaternary. In these contexts, the term “loess” carries a connotation about dry climate and open vegetation. By the classic definition, loesses are continental fine- grained sediments deposited by eolian processes during dry phases of climate cycles. So pervasive is the literature that associates loess with arid phases of the Quaternary that the association is a widely recognized generalization and many assume that where you find loess, you can infer dry climates. 8.5 Volcanic activity 259

Table 8.8 Age, mammalian diversity, proportion of elodont taxa, dominant mode of deposition, rate of pyroclastic sediment supply, and linear sedimentation rates for the Sarmiento Formation of Patagonia

Proportion Number of (and Dominant Rate of Linear Rock units/ Age mammalian number) of mode of supply sedimentation faunas (Ma)1 taxa2 taxa elodont3 deposition (N/myr)4 rate (m/myr)5

Gran Barranca 42.1–38.2 29 0.14 (4) Fluvial 2.5 12.35 Mbr/Barrancan SALMA Rosado Mbr/El 38.2 22 0.32 (7) Eolian 3.5 - Nuevo Rosado Mbr/ 38.2–38.0 21 0.24 (5) Eolian 3.5 24.67 Mustersan Lower Puesto - - Fluvial - - Almendra Member Vera Mbr/La 35.3–33.2 41 0.15 (6) Eolian 3.5 80.6–85.9 Cancha Upper Puesto 30.8 41 0.20 (8) Fluvial 9.5 - Almendra Mbr/ La Cantera Deseadan 26.3–24.1 53 0.30 (16) Fluvial 17 - SALMA (La Flecha and Cabeza Blanca) Lower Colhue- 21.1–19.0 77 0.16 (12) Fluvial 12.5 18.63–16.38 Huapi Mbr/ Colhuehuapian Upper Colhue- 19.0–18.6 23 0.48 (11) Eolian 14 82.23 Huapi Mbr/ “Pinturan”

SALMA, South American land mammal age. 1 Age of rock units and faunas: Ar/Ar from Re et al. (2010), U-Pb TIMMS from Dunn et al. (2013). Magnetic polarity-based durations for rock units uses the ATNTS of Gradstein et al. (2012). 2 Number of mammalian taxa: Madden et al. (2010) and chapters therein. 3 Proportion of elodont taxa: N¼total number of taxa/(Ne¼number of taxa with complete elodonty). Complete elodonty in all Xenarthrans, Patagoniidae, Argyrolagidae, Hegetotheriidae, Interatheriinae, post-Santacrucian advanced Toxodontidae, Caviidae, Chinchillidae. 4 Rate of supply of volcanic minerals: (N/myr) is the number of K-Ar, Ar/Ar, and U/Pb dates in Patagonia during the 1 myr interval immediately prior to the age of the fauna. (Ardolino et al., 1999; Ré et al., 2010; Dunn et al., 2013.) 5 Linear sedimentation rate (m/myr): total thickness of fossil-bearing unit/estimated temporal duration from all available geochronology. (Bellosi, 2010a; Dunn et al., 2013.)

However, there are numerous examples of “non-classical” types of loess (see, for example, Iriondo and Kröhling, 2007). Source areas of eolian dust include glacial/ periglacial environments, tropical deserts, pyroclastic eruptions and accumulations, and many kinds of remobilized ﬁne-grained sediments (or dust) off tidal ﬂats, alluvial fans, 260 The middle Cenozoic of Patagonia

dry lake beds, deflation pans, etc., and examples of such exposures can be found in all types of climate and under all types of vegetation. In addition, the diversity of environments where eolian sediments accumulate is so great that it should not surprise anyone to learn that eolian sediments can also accumulate in shrubland, woodland, and even forest environments, although the association between erosion and transport of fine- grained windborne sediments in woody environments is less well known. Loess or eolian substrates can also accumulate in super-humid temperate climates (Eger et al., 2012). They are known to accumulate in subtropical climates provided suitable local sources of sediment are available (Hao et al., 2010). In addition, when suitable source areas are active, they accumulate in subtropical latitudes, such as in southwest China and into northern Vietnam (Nichol and Nichol, 2013). Here, extensive and thick loess deposits have characteristic large particle sizes (coarse silt and fine sand) that suggest a local origin thought to be deflation off the exposed nearby East Asian continental shelf during low sea-level stands. These loess deposits are not interbedded with paleosols, but accumulated continuously at a time when pollen evidence indicates open forest–grassland vegetation. The North Island of New Zealand is covered by thick fine-grained pyroclastic deposits. These deposits include alternations of interbedded air fall tuffs and tephric loess (Pillans et al., 1992). These deposits are typically carbonate-free (Berger et al., 1992). Much of its mineralogy is volcanic, and the terms “tephric loess” and “vitric loess” were introduced to describe these distinctive windblown pyroclastic deposits (Kennedy, 1980). Under the classic model, these loessites must have been deposited during dry phases of the Quaternary when vegetation was open grassland. However, the most recent reconstructions of the vegetation cover of New Zealand at the Last Glacial Maximum (LGM) from pollen records (McGlone et al., 2010) document extensive forest on the North Island north of Auckland, and Nothofagus-dominated forest enclaves in protected coastal and exposed shelf locations SW of Auckland. Beyond these enclaves, vegetation cover comprised mostly woody shrubland, not grassland. Although grassland- dominant communities were more prominent in eastern areas and presumably higher elevations, most of the North Island was covered by extensive shrublands. Thus, woody vegetation has long served to trap windblown sediment on the North Island, even during the LGM. In particular, tephric loess accumulated at high rates under forests during the Holocene in the volcanically active Rotorua area of the northern North Island of New Zealand (Lanigan, 2012). These deposits were ultimately sourced from Plinian-style rhyolitic eruptions. Loess deposition occurred at a time when phytolith reconstructions using forest-indicator systematics indicate woodland environments.

8.6 Vegetation in Patagonia

8.6.1 Vegetation and surface processes

The ground cover afforded by the lowest stratum of vegetation inﬂuences erosion rates and the height of the canopy inﬂuences dust deposition and accession to soil. For example, there is a geographic coincidence between very low Leaf Area Index (LAI) 8.6 Vegetation in Patagonia 261

and dust source regions in both North and South America. The reason for this coincidence relates to the fact that dust emission from fine-grained sediments in topographic depressions on glacial outwash plains, river floodplains, alluvial fans, basalt plateau surfaces, and evaporation pans is strongly controlled by the presence and density of ground and canopy plant cover. Increasing the area of potential dust sources by reducing vegetation cover is known to result in a 20-fold increase in atmospheric dust loads at high latitudes (Mahowald et al., 1999). Conversely, carbon dioxide fertilization of vegetation during periods of high pCO2 (modeled as double modern-pCO2 climate) reduces atmospheric dust loads (Mahowald et al., 2006)by increasing the density of vegetation. LAI is the amount of functional (green) leaf area (m2) in the vegetation canopy per unit ground area (m2) and is measured, analyzed, and modeled across a range of spatial scales, from individual tree crowns, vegetation stands, to regions and even continents. It is a descriptor of vegetation condition in a wide variety of physiological, climatological, and biogeochemical studies (Asner et al., 2003). LAI is measured optically by the area of “shadow” cast by the leaves of the canopy with a light source (the sun) at infinite distance and oriented perpendicular to the land surface. Under vegetation, a tripod-stable camera with fish-eye lens is pointed directly upward and a photograph of the foliar canopy is taken at noon on a cloudless day. LAI can also be measured destructively by collecting and weighing total leaf litterfall and converting litterfall to leaf area using the specific leaf area (leaf area/leaf mass) of foliar subsamples. Specific leaf area varies between sun and shade leaves, with leaf turnover and seasonal phenology. Seasonality thus presents problems for determining annual average values of LAI. Now, with field research in general decline while the geographic scope of study expands to encompass the entire globe, LAI is more often estimated using remote sensing. Satellite data are used to quantify LAI, canopy cover, and the fraction of absorbed photosynthetically active radiation (fAPAR). LAI is also derived remotely from satellite-based normalized difference vegetation index (NDVI) data. The NASA SeaWIFS sensor and LAI algorithm are used with MODIS data to produce global maps of quarterly mean LAI at 8 km spatial resolution (Myneni et al., 1997). This data is averaged to produce a digital map of mean annual LAI. LAI and fAPAR products have been produced by MODIS since February 2000 (Justice et al., 2000) and undergo constant refinement (Yang et al., 2006; Shao et al., 2009; De Kauwe et al., 2011). Albani et al. (2012) used the well-documented model of Mahowald et al. (2006)to look at dust source areas and transport pathways around the Southern Ocean, and combined information from ice cores and model simulations to explain observed changes in dust deposition fluxes and dust particle size distributions between the LGM and present. This dust originates from the surface of southern South America. In their simulations, dust source areas changed in response to carbon dioxide, temperature, precipitation, and insolation changes, all known to influence LAI. If it were possible to reconstruct LAI for times in the past, it would also be possible to summarize the vegetation response (and in turn, its significance for erosion and sedimentation) with any or all of these climate variables. In this modeling exercise, enhanced coupling was 262 The middle Cenozoic of Patagonia

observed between Antarctic climate and conditions at the southern hemisphere mid- latitudes during glacial periods relative to interglacial periods. The most important sources of mineral dust for long-range transport were arid/semiarid regions with low vegetation cover within landscapes prone to the accumulation of ﬁne-grained sediment and strong winds.

8.6.2 Forest or grassland?

From the best available phytolith and pollen records, grasslands do not appear in Patagonia until very late in the Cenozoic (Barreda and Palazezzi, 2012; Strömberg et al., 2013). Phytoliths of arboreal life forms (palms and woody plants) occur abundantly at all stratigraphic levels of the Sarmiento Formation. The high abundances of palms and woody dicots and the low abundance of phytoliths diagnostic of open-habitat grasses indicates that there were no extensive grasslands or grass-dominated ecosystems in Patagonia between the middle Eocene and early Miocene, when mammals were precociously evolving high crowns. Thus, tooth shape evolution appears to have occurred in woodland or forest environments. The available record from Patagonian paleofloras does not contradict this. The most well-preserved floras of immediate relevance for a phytolith-based reconstruction of vegetation are those of Hünicken (1966) at Rio Turbio, and Aragón and Romero (1984) in the Ñirihuau Formation. In general, Patagonian paleofloras and pollen assemblages between 40 Ma and 30 Ma have little grass and are dominated by Nothofagus (Romero, 1986a; Barreda and Palazessi, 2007). These studies confirm that the progressive aridification leading to steppe-like environments occurred much later, in the late Cenozoic (Romero, 1986b; Case, 1988). Without a doubt, the presence of grasslands in Patagonia has been proposed during the interval of precocious hypsodonty, based on interpretations of both direct and indirect evidence from the Sarmiento Formation at Gran Barranca (Pascual and Ortiz- Jaureguizar, 1990; Bellosi and Gonzalez, 2010; Zucol et al., 2010). For these researchers and others, the existence of grassland vegetation and grass-dominated ecosystems relies on the direct evidence of grass phytoliths and indirect evidence of commensal insect trace fossils, grassland soils, and grass-dependent animals. Construing an early or precocious history of grass-dominated ecosystems in Patagonia has involved evidence from: (1) grass phytoliths (Mazzoni, 1979; Zucol et al., 2010), (2) aridland paleosols and trace fossil associations (Bellosi and Gonzalez, 2010; Bellosi et al., 2010), (3) the acquisition by mammalian herbivores of a stereotyped grazing morphology including high-crowned teeth (Pascual and Ortiz-Jaureguizar, 1990), (4) herbivore communities with high proportions of hypsodont taxa (Pascual and Ortiz-Jaureguizar, 1990), and (5) high seasonality and aridity (Bellosi, 2010a, b). South American grasslands are diverse today (Burkart, 1975). The modern distribution of grassland and savanna biomes in South America is generally correlated with climate conditions that vary with latitude. In the aseasonal equatorial tropics of the Andes, grasslands require high altitudes and low temperatures. Within the broader lowland zone of tropical latitudes, savannas require seasonally dry climates with significant periods of 8.6 Vegetation in Patagonia 263

water stress. At subtropical latitudes, extensive cerrado savannas occur where there is intense seasonal drought. At temperate latitudes, diminished zonal precipitation is reflected in extensive grasslands. At high temperate latitudes, semidesert shrub steppe occurs where orographic barriers reduce rainfall to levels below 500 mm MAP. Thus, variation in temperature, moisture, and seasonality shape the modern distribution of South American grasslands. One proposed scenario for the first appearance of grass- dominated habitats posits drought-stressed patches within a forested landscape under generally dry climate conditions following Eocene climate deterioration (Bredenkamp et al., 2002). Under this scenario, aridity is the major evolutionary force underlying the shift in plants to the herbaceous habit and annual growth. In the grassland versus forest debate, there seem to be four issues in contention: (1) details of phytolith analysis, (2) sedimentology and paleosols, (3) the significance of dung-beetle brood balls, and (4) the appropriate choice of a modern analog environment. Only one of these issues (phytolith analysis) relates to the direct evidence for grasslands (Zucol et al., 2010; Strömberg et al., 2013).

8.6.3 Grass phytoliths

Of the four available phytolith analyses of the Sarmiento Formation, only one (Maz- zoni, 1979) might be construed to provide evidence in support of the presence of open grasslands in the Eocene of Patagonia. To better understand how Sánchez et al. (2010b), Zucol et al. (2010), and Strömberg et al. (2013) came to a diametrically opposed conclusion requires comparing the morphological classification of phytolith shape and the assignment of phytolith morphotypes to particular plant groups. In his classic paper, the first analysis of Sarmiento Formation phytoliths, Mazzoni (1979) analyzed 21 sediment samples (none from either the Rosado or Vera Members), and distinguished 10 different phytolith morphotypes. Mazzoni (1979) sorted phytoliths into Bertoldi de Pomar’s broad morphological shape classes. Bertoldi de Pomar’s classification (1971, 1975) was highly original but based largely on published descriptions of phytoliths in the literature of the time, which was limited in phylogenetic scope and basically restricted to grasses. Thus, it is not altogether surprising that Mazzoni’s 1979 classification revealed the presence of grasses. Only after Piperno and Pearsall (1998), did phytolitharians begin to appreciate that the odd shapes formerly ignored or uncritically grouped into broadly defined classes were potentially more meaningful for the reconstruction of past vegetation. As dicot forest trees produce relatively few phytoliths, when their distinctive phytoliths are present, they indicate something important about the architectural complexity of the vegetation. By contrast with Mazzoni (1979), Zucol et al. (2010) distinguished over 100 morphotypes, grouped into six broad classes of plants (forest, shrub, palm, and three classes of herbs), far more morphotypes than reported by Mazzoni (1979). The diversity of morphotypes alone suggests the presence of architecturally more complex vegetation, and interpretations given to this diversity are consistent with this (Zucol et al., 2010). Strömberg et al. (2013) found that grasses comprise only about 6% of phytolith assemblages in the Eocene samples from Gran Barranca. This differs dramatically from 264 The middle Cenozoic of Patagonia

what Mazzoni’s 1979 data revealed, and among other things, reflects differences in the classification of prismatolite and brachiolite morphotypes, both of which are abundant in Mazzoni’s samples. Any way you look at it, palm phytoliths are abundant in the Gran Barranca Member and at nearly all stratigraphic levels of the Sarmiento Formation. Does this fact alone indicate forests? While palms may be generally subordinate in closed tropical forest (restricted mostly to the lower and middle stories), and occur in association with a wide range of more or less open vegetation, their absolute and relative abundance in soil phytolith assemblages can only be understood to imply architecturally complex vegetation. Their association with other phytolith types, whether forest indicators or open- habitat indicators, places the presence of palms in broader context. Like grasses, palms produce many phytoliths, possibly more than most (if not all) dicot shrubs and trees. Even if “subordinate” in a forest, palm phytoliths make up nearly 60% of phytoliths found in a tropical evergreen forest (Dickau et al., 2013). Beyond the generally high proportions of palm and dicot phytoliths, long cell, bulliform, trichome (aculeolita), and hair base phytoliths are abundant in many samples from the Sarmiento Formation at Gran Barranca. Although abundant, these are considered non-diagnostic by Strömberg et al. (2013), while other researchers commonly assign them to Poaceae (Mazzoni, 1979; Piperno, 2006; Zucol et al., 2010). Polyhedral, fan-shaped, or saddle “chloridoid” phytoliths present a particular problem. Stromberg et al. (2013) report very few. Herbaceous forest-floor bamboos also make saddles, and distinguishing between the phytoliths of forest-floor bamboos and open-habitat chloridoid grasses requires careful scrutiny of each phytolith.

8.6.4 Paleosols and trace fossil associations

Many of the paleosols in the Sarmiento Formation are weakly developed. Soils are weakly developed in areas where tephra and loess are actively deposited and contribute to aggrading soil parent material. Upbuilding pedogenesis can occur by airfall tephras (typically forming andisols) and from windblown dust (typically forming alfisols). In upbuilding, soil formation occurs simultaneously with additions of thin incremental tephra layers or slow dust accumulation (Lowe et al., 2008) and the rate of upbuilding determines the rate of pedogenesis. Many andisol and alfisol profiles form by upbuilding pedogenesis as younger tephra materials are deposited on top of older ones. This is especially so in loess terrains, where upbuilding pedogenesis is associated with high rates of loess accumulation. Most of the paleosols in the Sarmiento Formation at Gran Barranca are bioturbated (Genise et al., 2004) and show an argillic horizon, Fe, Mn, and carbonate nodules, a moderate to well-developed b-fabric, argilans, and ferromangans (Bellosi and González, 2010). One of the most important features of Sarmiento Formation paleosols that implies “arid or semiarid” conditions are calcic horizons that generally form in soils where mean annual precipitation is <600 mm, in association with xeric, herbaceous, shrubby, or open-arboreal communities. For carbonate nodules to form, the climate must be dry. However, there are few, if any, carbonate nodules in the Sarmiento 8.6 Vegetation in Patagonia 265

Formation at Gran Barranca, and only about 10% of all sediment samples have been found to react to HCl (these were El Nuevo, El Rosado, La Cancha, various levels in the Vera, and a few in the upper Colhue-Huapi Member), the relatively dry intervals when eolian processes dominated. Bellosi et al. (2010) document the prevalence of dung-beetle brood balls, the “Copri- nisphaera ichnofacies” (an insect trace fossil association in paleosols), the essential features of which were established by Genise et al. (2000) and characterize herbaceous communities in both dry and humid climates. Coprinisphaera were collected in the Sarmiento Formation at Gran Barranca and studied by Sánchez et al. (2010a, b) from 15 stratigraphic levels, and analysis of this collection led to the following conclusions. The lowest two levels in the upper middle Eocene Gran Barranca Member: dung-beetle brood balls occur but in low diversity and abundance. The drier conditions in the Rosado Member led to the total absence of dung beetle traces. Following a burst of diversity about 2 myr later in the Lower Puesto Almendra Member, the absence of dung beetle traces in the Vera Member continued through the EOT and into the early Oligocene. Dung-beetle brood balls appear again in the fluvial Upper Puesto Almendra and lower Colhue-Huapi Members. Where abundant and diverse, dung-beetle brood balls occur in association with fluvial depositional environments. Where arid, they do not occur. You can find many explicit statements of caution warning against overinterpreting paleoenvironments from the Coprinisphaera trace fossil association (Genise et al., 2000). Halffter (1991) explained the diversity of dung beetles in forests of South America today to the adoption of diverse coprophagous, necrophagous, and sapropha- gous diets (carrion and rotten fruit). If dung beetles depended solely on large grazing herbivore dung to survive in the tropical rainforest, and there were no such herbivores, they would not occur there. However, they do thrive in tropical rainforests, and in great abundance and diversity (Favila and Halffter, 1997), and they exploit dung from birds, reptiles, and mammals; that is, not dung from large grazing herbivores but from large browsers, folivorous and omnivorous rodents, and monkeys (Anduaga and Halffter, 1991; Estrada and Halffter, 1993). Therefore, dung beetles do not depend exclusively on large accumulations of herbivore dung in open savanna or grassland environments, and cannot be used as an indicator of either abundant large herbivore dung or open- grassland environments. In fact, dung beetles of the Scarabaeinae have been proposed as indicators of high biodiversity in tropical rain and deciduous forest (Favila and Halffter, 1997). Two things seem important about dung-beetle brood balls: their construction requires exposed soil or bare ground, and brood balls with a thick external layer of cemented fine-grained soil are especially well suited for resisting seasonal drought.

8.6.5 Shrublands

Shrublands are woody plant-dominated vegetation with a low canopy (<8 m high) and comprise much-branched and many-stemmed woody plant life forms. Botanists distinguish tall (2–8 m high), small (1–2 m high), and/or even low shrubs (<1 m high), and 266 The middle Cenozoic of Patagonia

among shrublands, closed scrub has dense foliage (70%–100%) and open scrub has more open foliage (10%–70%), while tall shrublands have sparse foliage (10%–30%) and open shrublands have very sparse foliage cover (<10%). In temperate Argentina, shrubland vegetation includes the espinal, the extensive monte, portions of the humid pampas of Buenos Aires province, and grasslands of the more humid western Patagonia, the more extensive shrubland steppes of drier central, eastern, and southern Patagonia, and larger portions of the semiarid pampas of La Pampa and San Luis provinces. Shrublands in tropical and subtropical latitudes include montane shrublands bordering the paramo, where without continued disturbance, these thickets might become high montane dwarf forests. Neotropical savannas when woody plants are present can also be called shrublands; for example, low to tall shrub savanna in the llanos, and areas of seasonally dry forests, and areas of forest–shrubland–savanna, where with continual disturbance, they support shrub thickets. The xeric shrublands of the caatingas of NE Brazil are another example, as is the cerradao of Brazil, a dense arboreal vegetation that varies between either a matorral (scrub) or monte seco (dry low forest). All these diverse shrublands are characteristic vegetation where rainfall or rainfall seasonality is limiting. In their review of atmospheric dust, Tsoar and Pye (1987) noted that thick loess accumulations are not associated with deserts or other dry climate source areas, because in the absence of dust traps, deserts and drylands do not accumulate dust. Signiﬁcant thicknesses of loess only accumulate when dust is trapped by topographic obstacles. Such obstacles include vegetation. Comparing dust trapping in three different vegetation types in semiarid climate (open grasslands, shrublands, and forest), shrublands were found to be more efﬁcient traps of windborne dust than either forests or grasslands (Breashears et al., 2003). Woody vegetation (shrublands and forests) have been found to capture considerable amounts of aerosols relative to adjacent grasslands (Gallagher et al., 2002; Breshears et al., 2003, 2009; Branford et al., 2004; Mills et al., 2012). The thickness and rate of deposition of loess deposits under woody vegetation typically decreases exponentially away from the woodland edge and the enhanced accumulation of thick loess deposits at the woodland boundary is noteworthy. This pattern suggests that shrublands associated with the migrating forest boundary may be an important feature of Holocene loess accumulations (Baker et al., 2002) and has given rise to the idea that, as the forest retreats during dry climate phases (or advances with wetter climates), the focus of loess accumulation also migrates.

8.7 Wind, marine productivity, and hypsodonty

Most eolian dust deposited today as sediment in the marine record is seasonal, produced by spring wind storms, and most dust is produced in the northern hemisphere, where large land areas experience arid and hyper-arid conditions and great seasonal temperature amplitude. On continental surfaces, dust storms are known to reﬂect rainfall, and occur most frequently in arid climates (between 100 mm and 200 mm MAP) and least 8.7 Wind, marine productivity, and hypsodonty 267

frequently in “humid” climates (MAP >500 mm) (Pye, 1987). However, even in arid and hyper-arid regions, dust storm frequency decreases with landscape stability. In the oldest aridland surfaces (core Sahara, Australia, and southern Africa), surface winds contribute little dust into atmospheric aerosols because the land has already been deflated and stripped of fine-grained surface sediments. Southern South America is the geographic source of most of the mineral dust in Vostok and Epica Dome C cores (Delmonte et al., 2004). More precisely, it is dust deflated off the Southern Andean Volcanic Zone and glaciated batholith complex subject to high mechanical weathering and strong westerly winds. The temporal cycles of atmospheric dust abundance in the Vostok core matches the organic carbon accumulation rate in the adjacent oceans. Maps of global ocean chlorophyll concentrations from SeaWiFS show a plume of surface productivity that extended east from the least vegetated parts of Patagonia [http://earthobservatory.nasa.gov/IOTD/view.php?id=4097], a plume of surface marine productivity fertilized by aerosol dust. [There is another plume of high chlorophyll concentration extending northeast off the tip of the Antarctic Peninsula, an upwelling plume associated with the flow through Drake Passage.] ODP Core 1094 in the sub-Antarctic sector of the SE South Atlantic Ocean preserves a record of terrigenous dust (mostly volcanic ash, but also quartz and lithic fragments) that matches the temporal fluctuations in dust concentration in Vostok ice (Kanfoush et al., 2002). An analysis of a longer four-million-year record of dust and iron fertilization in nearby ODP Core 1090 reveals a general association between cooling, the strength of the ice ages, increased dust loads and carbon sequestration, and atmospheric pCO2 reduction (Martínez-Garcia et al., 2011). Coincident increases in opal mass accumulation rates and the development of extensive diatom mats have also been documented (Cortese and Gersonde, 2008). Were the pyroclastic products of Patagonian volcanism a significant source of atmospheric dust over the South Atlantic and Southern Ocean during the middle and late Eocene and at the EOT? The Sarmiento Formation is the thickest and most widespread (some 200 000 km2) and characteristic unit of Paleogene sedimentary rocks in central Patagonia (Mazzoni, 1985). Sarmiento Formation sediments are mixed pyroclastic and epiclastic claystones, mudstones, and siltstones with chemical composition of typical calc-alkaline dacitic tephras (Mazzoni, 1985). The ultimate source of Sarmiento Formation sediments was explosive Plinian volcanism along the western margin of Patagonia. The fine-grained volcanic ash was, and is, highly susceptible to erosion, and evidence for erosion ranges in form from conspicuous irregular or undulating surfaces or erosional unconformities to much more subtle parallel discontinuities in sediment accumulation. Diatoms require silica and silica in the oceans is derived primarily from the weathering of continental rocks (Coale et al., 2004), delivered in solid form by wind and rivers. During the Pleistocene, dust supply to the Southern Ocean increased during ice ages and the productivity it fertilized contributed to the observed drawdown of atmospheric carbon dioxide (Martínez-Garcia et al., 2011). Marine productivity also increased in the Southern Ocean during the middle Ceno- zoic. These increases are indicated by decreased carbonate sedimentation coincident with peak dissolution, increased opal sedimentation, and high benthic foramineral 268 The middle Cenozoic of Patagonia

accumulation rates. The increase in productivity has been associated with the initial development of the Antarctic Circumpolar Current with its increased wind strength and intensified upwelling (Schumacher and Lazarus, 2004). There is abundant evidence from benthic foraminiferal, radiolarian, and diatom opal accumulation rates for an increase in ocean productivity during the EOT (Diester-Haas and Zahn, 2001). A high amount of explosive volcanism is associated with this increase in productivity in the South Tasman Sea (Kennett and Von der Borch, 1986), as are increases in terrigenous matter (Diester- Haas and Zahn, 2001). Changes in net productivity in surface waters of the Southern Ocean near the Eocene–Oligocene boundary are also indicated by the positive carbon isotope shift (about 0.75 ppm) or transient carbon isotope excursion (Salamy and Zachos, 1999). These are thought to result from a climate-induced intensification of wind stress and increased terrigenous sediment inputs. As has been shown, dust storm frequency has a direct relationship to tooth wear at ecological timescales and tooth shape at evolutionary timescales. High dust storm frequency is geographically coincident with areas of high hypsodonty globally, dust storm frequency is associated with high tooth wear in southeast Australia, and the temporal variation in aerosol dust transport (and dust accumulation on the sea-floor) relates directly to changing rates of tooth shape evolution in the Plio-Pleistocene of East Africa. A possible association between changes in the rate of evolution of high-crowned teeth in Patagonia and the influence of dust in sea-floor sediments of the South Atlantic or beyond has never been examined. Wind strength varies inversely with the pole-to-equator temperature gradient; that is, a low or weak gradient reduces zonal average wind strengths, and a steepened or strengthened equator-to-pole gradient implies increased average wind strengths. Strength of the westerlies is termed “the zonal index,” a high zonal index (with strengthened equator-to-pole temperature gradient) implies increased wind intensity and poleward shifts of intensity maxima (Campagnucci, 2011). The presence and abundance of eolian loessites in the Sarmiento Formation, and the temporal coincidence between wind-dominated surface processes during dry climate intervals leads me to suspect that dust mobilization was part of the story of precocious hypsodonty. First, however, is there temporal coincidence between dry climate intervals and eolian sedimentation in Patagonia with episodes of high ocean productivity? Temporal relationships between marine productivity downwind and changing rates of taxonomic increase of high-crowned herbivores in the presumed dust source area of central Patagonia are presented in Figure 8.4. An interval of high “export production” occurred between 44 Ma and 42 Ma at ODP Site 1090 (Latimer and Filippelli, 2002) and between 44 Ma and 41.6 Ma at ODP Site 689 (Diester-Haass and Zahn, 1996). These intervals occurred just prior to the onset of deposition of the Gran Barranca Member of the Sarmiento Formation. Major deterioration in global climate followed, and long-term cooling continued between 42 Ma and 36 Ma. Variation in the temperate-warm water calcareous nannofossil assemblage index (or Twwt Index) has been related to instability in the Southern Ocean SST conditions and has been used to identify warming and cooling events within this long interval (Vila et al., 2008). 269 20

Smear slide composition (%) ), arranged in 2004 0 0 0 50 50 50 100 100 100 25 25 30 30 diatoms diatoms Hiatus radiolarians Time (Ma) 35 35 nanoplankton forams 8.7 Wind, marine productivity, and hypsodonty diatoms nanoplankton Hiatus forams 40 40 Archaeohyracidae Oldfieldthomasiidae Notostylopidae Toxodontidae Interatheriidae Notohippidae

Site 511 Site 689 Site 748 45 wind wind

Middle Eocene through Oligocene chronology of marine productivity in the Southern 0

75 50 25 100

1.0 2.0 3.0 4.0

Hypsodonty (%) Hypsodonty

Hypsodonty Index (HI) Index Hypsodonty Notoungulate progressively greater distances downwind fromElsevier). the dust source area (with permission from Ocean downwind of Patagonia andthe the middle evolution Eocene of and tooth Oligocene.concentrations crown Plots of height of marine in DSDP/ODP diatoms fossil Site (from ungulates 511, Schumacher from 689, and and Lazarus, 748 smear slide Figure 8.4 270 The middle Cenozoic of Patagonia

There occurs a brief pre-MECO interval at 41.5 Ma that ended at about 40.5 Ma, attributed to a cooling phase or a combination of cooling and minor glaciation in Antarctica (Bohaty et al., 2009). MECO itself is a relatively short duration and transient

warming event (linked to a transient increase in atmospheric pCO2) that peaked at about 40 Ma (Bohaty et al., 2009) and ended with a cooling episode at ODP Site 748 at about 39 Ma. In general, the δ18O record between about 39 Ma and 37 Ma indicates resumed gradual cooling, while the Twwt Index shows several small but prominent cycles within this interval. One of these is a brief instability or cooling coincident with the Rosado Member at Gran Barranca (Vila et al., 2008), but there is no evidence for increased marine productivity during this time. During the time of deposition of the eolian-dominated Vera Member, a second and much more significant interval of increased productivity occurred. This increase in ocean productivity is evident between 34.5 Ma and 32.8 Ma at Site 1090 (Latimer and Filippelli, 2002) and from the Maud Rise (Diester-Haass and Zahn, 1996). Salamy and Zachos (1999) observed a sharp peak in productivity after the Eocene–Oligocene boundary. Fe and P concentrations plotted against age (Latimer and Filippelli, 2002; Figure 8) suggest that eolian Fe-fertilization increased productivity in the earliest Oligocene. Mallinson et al. (2003) present a study of clay mineralogy from marine sediments at ODP Site 1128 in the Great Australian Bight, where they find evidence for a major increase in Antarctic glaciation between 33.6 Ma and 33.48 Ma, correlated temporally with the positive oxygen isotope shift, and clay mineralogy dominated by crystalline smectite suggesting a terrestrial source of explosive volcanism. This study presents evidence for a chronologic link among explosive volcanism, climate drying, and an intensification of wind velocities at 33.4 Ma. There is an increase in productivity in the equatorial Atlantic Ocean between 19 Ma and 18.2 Ma at about the time of the upper Colhue-Huapi Member, but is not yet evident in the SE Atlantic Ocean nor anywhere else in the Southern Ocean downwind of Patagonia (Diester-Haass, et al., 2009).

8.8 Discussion

8.8.1 Grazing morphology in fossil mammals

Stereotyped grazing morphology includes high-crowned teeth, a transversely expanded premaxilla with straight incisor cropping battery, and limbs modiﬁed for cursoriality and to bear body weight on the ungual phalanges. Most of the mammalian fossil record in the Sarmiento Formation at Gran Barranca is teeth; skulls and skeletons are rare. For some species, however, cranial and postcranial material is known from deposits elsewhere in Patagonia (Simpson, 1948, 1967). Only the skulls of Thomashuxleya, Notopithecus, Notostylops, Trigonostylops, Pleurostylodon, and Acropithecus are known from Vacan- or Barrancan-age deposits of the Sarmiento Formation. Only one of these genera is involved in “precocious” hypsodonty, Notopithecus (Interatheriidae). The skull and masticatory morphology of 8.8 Discussion 271

Notopithecus and other Interatheriidae are conservative and did not change through the evolutionary transition from low to ever-growing teeth (Scarano, 2009). The skulls of Notostylops murinus (Notostylopidae) and Acropithecus rigidus (Archaeopithecidae) have anterior dentitions with narrowing rostrum anterior to the cheek teeth, enlarged central incisors with pointed rather than spatulate crowns, diminuitive lateral incisors, and diastemata between anterior and cheek teeth, suggesting a selective browsing rather than grazing habitus. In Notostylops murinus, the mandibular symphysis supports elongate narrow and procumbant central incisors that, in occlusion against the upper central incisors, would have permitted selective browsing. This same morphology is found in the mandible of Homalostylops parvus, the smaller genus of notostyopid from the Casamayoran. In summary, there is little morphological evidence for the grazing habitus in middle to late Eocene notoungulates of Patagonia. For late Eocene Mustersan taxa in the Rosado Member at Gran Barranca, only the skulls of Astraponotus (Astrapotheriidae) and Puelia (Notohippidae?) are known. Puelia is interesting because it is close to the base of the notohippid clade that is an important part of the story of “precocious” increases in molar crown height (Cerdeño and Vera, 2010). No cranial or postcranial material has been collected in the early Oligocene Tinguirirican level of La Cancha in the Vera Member at Gran Barranca. While notohippid and archarohyracid teeth are abundant and high-crowned to ever- growing, nothing can be said about other morphological features of the grazing complex in these clades in Patagonia. For taxa occurring in the Deseadan levels of the Upper Puesto Almendra Member at Gran Barranca, the skulls and/or palates and/or anterior dentitions are known for the large Pyrotherium, Asmodeus,andParastrapotherium, albeit from other localities. None displays rostral or anterior dentitions associated with the grazing habitus. Among medium- sized Notoungulata, neither Leontinia, Scarrittia,orAncylocoelus (Leontiniidae) has broad muzzles. The partial skull of Proadinotherium leptognathum (Toxodontidae) is known, and its anterior dentition and rostrum are broad and suggest a grazing habitus (MacFadden, 2005). Diverse Notohippidae are known from Deseadan-age deposits in Patagonia, including the skull of Rhynchippus equinus. All Deseadan-age Notohippidae are generally considered to have been grazers, given their broad muzzles, transversely arrayed anterior dentition, high-crowned teeth at all tooth positions, and subcursorial postcranial specializations (Shockey, 1997a, b; Shockey and Flynn, 2007; Shockey and Anaya, 2008). The best-preserved cranial material from Gran Barranca comes from Colhuehuapian levels, and includes skulls of Proadinotherium muensteri (Toxodontidae), Argyrohippus (Notohippidae), Colpodon (Leontiniidae), and Cochilius (Interatheriidae). The ﬁrst three of these taxa show morphological features associated with grazing, including high- crowned cementum-covered cheek teeth separated by a wide diastema from a transversely arrayed anterior dentition (Argyrohippus), and the same morphology in Proadinotherium (less thick external cementum); and in Colpodon (Leontiniidae) which has only relatively high-crowned teeth. Cochilius had evolved ever-growing cheek teeth, but neither its skull nor anterior dentition nor rostrum changed appreciably during this evolutionary transformation (Scarano, 2009). 272 The middle Cenozoic of Patagonia

Classically, adaptations for cursoriality or rapid digitigrade locomotion in open habitat include the evolutionary elongation of the distal limb elements to increase running stride, reduction in the number of digits, and the development of hard, narrow hooves. Unfortunately, postcranial remains, when present at Gran Barranca, are almost always found as isolated elements difﬁcult to allocate. Scant but informative postcranial remains are known from elsewhere in Patagonia for Casamayoran taxa Thomashuxleya, Anisotemnus, and Pleurostylodon (Simpson, 1967; Shockey and Flynn, 2008).For Mustersan taxa, the situation would be worse were it not for postcranial elements of Astraponotus (Astrapotheriidae), Periphragnis, and Rhyphodon (Isotemnidae) having been recovered from Gran Hondonada (Cladera et al., 2004), but these have yet to be described. Most of these archaic native unguligrade herbivores were medium-sized and only a few (principally among Interatheriidae and Archaeopithecidae) had body masses of <55 kg (Scarano et al., 2011). At the other extreme, there are few large unguligrade mammals in middle to late Eocene faunas of Patagonia, but this changes in the late Oligocene–early Miocene. In mammal faunas of the Deseadan and Colhuehuapian, while relatively few taxa had body masses greater than 1000 kg, both Pyrotheriidae and Astrapotheriidae had tusks (elongate, robust, salient anterior teeth) and display tooth wear consistent with harvesting foliage. Sexual dimorphism has not been documented in South American native ungulates between the Vacan and Colhuehuapian. At the community level, a decline in the abundance and diversity of browsing mammals relative to grazers is often associated with grass-dominated habitats (Pascual and Ortiz-Jaureguizar, 1990). The record from Gran Barranca documents a gradual but step-wise shift in the proportions of tooth shape classes toward increasing prevalence of hypsodont taxa into the Miocene, suggesting that grasses or grasslands might have become more prominent through the Miocene. The only other faunal evidence that sheds light on the architectural complexity of Eocene and Oligocene environments in central Patagonia comes from the overall diversity and assortment of dental adaptations among the fossil mammals. Among the oldest faunas of the Sarmiento Formation at Gran Barranca, there are 29 taxa of mammalsintheGranBarrancaMember,22atElNuevo(GBV-60)and21atEl Rosado (GBV-3) in the Rosado Member, 41 at La Cancha in the Vera Member, and 41 taxa at La Cantera in the Upper Puesto Almendra. This pattern of variation in total richness bears no obvious relationship to increases or decreases in humidity, the alternation of intervals of wet and dry climates, or ﬂuvial and eolian depositional environments. Cingulata and “meridiungulates” are common taxa in all these faunas and occur in relatively constant and unvarying proportions. There are always from four to seven taxa of fully elodont Cingulata and 15 to 20 taxa of “meridiungulates” in these faunas. Were armadillos important engines of denudation and erosion? While the proportion of high- crowned taxa among notoungulates increases through time, there persist “meridiungulates” with low bunoid and brachydont crowns among notoungulates, litopterns, and “condylarthrans.” These are perhaps less conspicuous as fossils, but their presence is real. Taken together with the diversity of crown types among marsupials and rodents, 8.8 Discussion 273

A B 0.7 0.7 0.6 0.6 0.5 0.5 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 0 0

0 1000 3000 5000 7000 0510 15 20 25 30 Mean annual precipitation (mm) Mean annual temperature (ЊC) R2=0.232; p<0.0001 R2=0.555; p<0.0001 CD 0.7 0.7 0.6 0.6 0.5 0.5 0.4 0.4 0.3 0.3 0.2 0.2 0.1 0.1 0 0

Percentage of sigmodontine species hypsodont Percentage 0 2 4 6 8 10 12 14 16 18 –15 –10 –5 0 5 10 15 20 25 30 Seasonal temperature amplitude (ЊC) Mean temperature of coldest month (ЊC) R2=0.256; p<0.0001 R2=0.471; p<0.0001

Figure 8.5 Bivariate plots of the proportion of species of Sigmodontinae (Rodentia, Muridae) with high molar crowns in modern mammalian faunas from South America in relation to (A) mean annual precipitation, (B) mean annual temperature, (C) mean monthly temperature seasonality and (D) mean coldest month mean temperature.

the total range of body size and tooth crown shape diversity can be reconciled only by invoking architecturally complex vegetation.

8.8.2 Temperature, precipitation, and hypsodonty

In a sample of 80 modern faunas in South America today (see Chapter 2), sigmodontine rodents display relatively high molar crowns in faunas where temperature and rainfall have the following characteristics (Figure 8.5). Precipitation exerts a noteworthy inﬂuence on sigmodontine hypsodonty. With only two exceptions, when MAP is >2000 mm, all sigmododontine species are low-crowned in modern mammalian faunas. In semiarid climates (with MAP <750 mm), 25% or more of sigmodontine species are high-crowned. High prevalences (50% or more) of high-crowned species are associated only with MAPs <1500 mm. The estimated MAPs for the Sarmiento Formation at Gran Barranca are consistent with the presence of high- crowned herbivores. In faunas that occur where MAT is <15 C(Figure 8.5B), there are always hypsodont species, and with only one exception, the highest levels of sigmodontine hypsodonty (>50% of species) occur only when MAT is <17 C. Hypsodont sigmodontines are found in modern faunas at MATs of 22 C. Crocodilian and palm thresholds indicate that MATs in central Patagonia during the middle Cenozoic ranged from above 18–19 Cin 274 The middle Cenozoic of Patagonia

the lower Gran Barranca Member and did not dip below about 11–12 C. Within this range today, the prevalence of high-crowned sigmodontines ranges between 0% and 66%. With only three exceptions, high levels of prevalence (>50%) are found only where the seasonal amplitude of MMTs is 10 C or more (Figure 8.5C). That is, where seasonal amplitude of MMTs is low (as in the tropics), all sigmodontines have low molar crowns, and with relatively high seasonality (for oceanic peninsular Patagonia), high tooth crowns become prevalent. When the CMMT is <5 C, high-crowned species comprise 15% or more, and the highest levels of sigmodontine hypsodonty are associated with climates with CMMTs between 0 C and 10 C(Figure 8.5D). What is the meaning of these thresholds of temperature (MAT <15 C, CMMT <5 C, and seasonality >10 C) and precipitation (MAP <1500 mm)? High rates of tooth wear are found in seasonal climates with prolonged dusty dry seasons and/or rainstorm- induced soil erosion in the wet season. This suggests that any climate change bringing increased seasonality, especially peak rainfall in the winter season of slow plant growth, or more severe seasonal aridity and high winds might accelerate evolutionary rates of hypsodonty. How?

8.8.3 Sediment supply, sedimentation rates, and hypsodonty

When dated zircons from the same tuff have non-overlapping error margins, we infer that these may represent detrital components of older eruption events. Their presence in tuffs or tuffaceous horizons represents reworking, whether within the magma chamber, vent, or during subsequent transport. When these dates are plotted, three periods of more frequent eruption activity become apparent (Figure 8.6). The oldest of these periods of apparently higher eruption frequency corresponds with the time interval (approximately 41.5 Ma to 36.8 Ma) preserved by the Gran Barranca and Rosado members. Within this interval occurs Hypsodonty Event #1 (Figure 8.6), the relatively brief one-million-year episode of accelerating evolution of increasing mean hypsodonty index (HI) in three clades (Archaeohyracidae, Interatheriidae, and Notostylopidae) and increasing proportion of high-crowned taxa among notoungulates. Volcanic eruption activity reached a peak during the roughly two-million-year interval between 39.1 Ma and 37.0 Ma, during which the evolution of crown height is most conspicuous. A second interval of apparently more frequent eruption activity between 31.5 Ma and 30 Ma partially overlaps Hypsodonty Event #2 (Figure 8.6), when clades Archaeohyr- acidae, Notohippidae, and Interatheriidae increased in mean hypsodonty, and there was a slight acceleration in the trend of generally increasing faunal hypsodonty among notoungulates. A third episode of apparently more frequent eruption activity occurs between 23.4 Ma and 22.1 Ma, between the Deseadan and Colhuehuapian, during which time the clades Notohippidae, Toxodontidae, and Interatheriidae increased in mean hypsodonty but the overall proportion of notoungulate taxa did not increase. This interval corresponds in time to the Upper Puesto Almendra Member following the eruption of basalts. egtin height rws hog h ideCnzi fPatagonia. of Cenozoic middle the through crowns, iue8.6 Figure Stratigraphy Magnetic age (Ma) Linear sedimentation Volcanic Eruption event Archaeohyracidae Toxodontidae at Gran Barrana polarity rates eruption APTS06GTS04 events Inferred eruption event Oldfieldthomasiidae Interatheriidae 17

Mbrs. 5Dn basalt flow 5Dr.1 Notostylopidae Notohippidae ﬁ ycrn mn iersdmnainrts ocncatvt,icesn encrown mean increasing activity, volcanic rates, sedimentation linear among Synchrony 18 ecae fNtuglt,adtepooto fntugltswt ihmolar high with notoungulates of proportion the and Notoungulata, of clades ve

5E Intervals of high 1 01-24.5 Tuff Upper eruption frequency MMZ24.5 Tuff 19 6 20

6An 21 ? 6AA Colhue-Huapi 6AAr Lower ? ? 22 6B Big Mammal Tuff ? 3 3 23 Ds10 6C

Unit 5 24 Ds 9 7

7A 25 Pendorcho bed

Unit 4 Ds8 26

Almendra Carbon Tuff

Upper Puesto Ds 8 Ds 7 basalt 27 Unit 3 Cantera Tuff flows Ds6 (Section A2) 28

Ds7 29

Ds6 30 La Cancha Tuff 2 31 2 32 Vera (Profile K) Vera 33 13 12 11 10 9 8 13r.14 34

Ds5

Kay Tuff 13r.1? 35 Ds5 15 Unit 2 Ds4 Bed 10Tuff 36 Unit 1 Almendra

37 Discussion 8.8 Lower Puesto Ds3 Rosado EI Rosado Tuff (Profile J) 17 16 Ds 2 38 1 39 1 50

Ds1 Simpson’s Y Tuff 18 40 41 19 Gran Barranca 42

0 100 25 50 75 1.0 2.0 3.0 050 100 150 0 275 m/myr Hypsodonty Index (HI) Notoungulate hypsodonty (%) 276 The middle Cenozoic of Patagonia

These periods of higher eruption frequencies are more apparent than real. Clusters of similar age are likely just artifacts of the unintentional discovery of older zircons in reworked tuffs. When primary airfall tuffs from actual eruption events are dated, no reworked zircons are found (see Figure 8.6), and hence no “history” of prior eruption can be crafted. In addition, the depositional hiatuses contribute to artificial clustering. Undoubtedly, dating older zircons in reworked tuffs provides a glimpse into the temporal hiatuses that are otherwise opaque. There may be no legitimate way to approach a reconstruction of changing rates of volcanic eruption, even with a compilation of all the discrete zircon ages sampled at regular intervals throughout the Sar- miento Formation. However, dates from tuffs and basalts tell us something useful about the supply of fresh pyroclastic and other volcanic minerals, and U-Pb and Ar/Ar dates may be converted into a “rate of supply” (number of dates per million years) of these mineral particles. When tallied during the one-million-year interval immediately prior to a fauna or faunal horizon (see Table 8.8), the “rate of supply” increases progressively up section, as does hypsodonty. Seen through the lens of surface processes, this “rate of supply” relates to pyroclastic sediment availability. During the interval of the Sarmiento Formation, there was inter- mittant accumulation of pyroclastic deposits throughout the San Jorge Basin, and probably a more continuous reworking of tuffaceous sediment, judging by the evidence of erosional unconformities. Linear sedimentation rates might be considered a deep-time proxy for mineral particle flux. Sedimentation rates were variable and seem to show important differences between intervals of wet (fluvial) and dry (eolian) climates. As is generally true, sedimentation rates vary but are relatively constant during the Gran Barranca and Rosado Members. Sedimentation rates are generally higher in the Vera Member, and there is a peak of linear sedimentation rates near the top of the Vera Member, corresponding chronologically to Chron C13n and Oi-1. During the four-million-year interval between the Mus- tersan at El Rosado and the Tinguirirican at La Cancha, there was a rather large jump in the percentage of hypsodont notoungulates but little change in mean crown height within clades. Sedimentation rates were moderate in the Upper Puesto Almendra Member when crown height was increasing among Interatheriidae, Toxodontidae, and Notohippidae. After the hiatus of Discontinuity 10, sedimentation rates resume but are variable. These rates appear to decrease during the Lower Colhue-Huapi Member, and increase again, importantly in the upper portion of this member.

8.8.4 Marine productivity and hypsodonty

The marine sediment core from DSDP Site 511 on the Malvinas Plateau (Figure 8.4) preserves the EOT and the interval of time represented by the Vera Member at Gran Barranca. It was a time of high phytoplankton productivity. DSDP Site 511 off Pata- gonia does not preserve as complete a record as the ODP cores 689 and 748 farther downwind in the Southern Ocean. The more distant cores (ODP 689 and, even farther 8.8 Discussion 277

out, ODP 748) were better drilled and more completely recovered, and the temporal coincidences suggest that Patagonian dust may have reached the sea-surface farther out in the Southern Ocean. This would suggest that wind velocities (threshold detachment velocities) and continuities (wind run) were approaching more modern conﬁgurations. Unfortunately, the only published study of marine productivity in the middle Ceno- zoic and across the EOT (Schumacher and Lazarus, 2004) did not examine either Sites 512 or 513. The core from DSDP Site 512 on the Malvinas Plateau preserves marine sediment contemporaneous with the time interval represented by the Gran Barranca Member through Rosado Member. A comparison of the thickness of marine sediment associated with each polarity interval at Site 512 suggests that the Gran Barranca and Lower Puesto Almendra were times of slower mass accumulation rates (MAR) on the sea-ﬂoor, whereas Rosado was a time of higher MAR. DSDP Site 513 in the Argentine Basin is another potential source of downwind information about surface conditions in Patagonia. Site 513 preserves both Vera and Colhue-Huapi Member time in marine sediment. The comparison of changing rates in the taxonomic evolution of high tooth crowns with the downwind record of marine productivity in the Southern Ocean (Figure 8.4) shows peaks of phytoplankton (diatom) productivity during the accelerated taxonomic evolution of high tooth crowns that began about 33.4 Ma with Oi-1.

8.8.5 Geographic area

Geographic area and geographic isolation are particularly important in mammalian evolution. On a low and narrow peninsula like Patagonia, sea-level fluctuations may influence cladogenesis and rates of morphological evolution through area effects, where the influence of earth surface processes (the environmental agent of evolutionary change in tooth shape) matches the geographic range of its subject populations, and these populations cannot escape across even shallow marine barriers (see Chapters 5 and 6). The surface area of Patagonia under the influence of windborne or waterborne pyroclastic material can be estimated by the outcrop area of subdivisions of the Sarmiento Formation. As has long been observed, the geographic extent of lithostratigraphic subdivisions of the Sarmiento Formation is made difficult by lateral variation. However, the geographic distribution of fossil mammal assemblages representing coherent (taxonomically constant composition) levels or SALMAs provides a means of determining their distribution. For example, Vacan SALMA assemblages have the most restricted geographic distribution of all subdivisions of the Sarmiento Formation, being confined to exposures along a small part of the middle course of the Rio Chico del Chubut. The Barrancan SALMA is the second most geographically widespread subdivision of the Sarmiento Formation, and occurs in Chubut Province as far north as Scarritt Pocket and between Gran Barranca and the Atlantic coast. The Mustersan SALMA is known only from a few localities in the general vicinity of Lake Colhue-Huapi in central Chubut Province. Tinguirirican SALMA deposits of the Sarmiento Formation are few in Pata- gonia, and although the whereabouts of Cañadon Blanco is still a great mystery, deposits of this age extend in a straight line west to east between Gran Barranca and Camarones on 278 The middle Cenozoic of Patagonia

the Atlantic coast. The most widespread of the temporal units of the Sarmiento Formation are Deseadan SALMA deposits that extend from Rio Negro in the north to south of the Rio Deseado, and between Gran Barranca and the Atlantic coast. Colhuehuapian SALMA faunas are known from localities that extend from western Neuquen to Gaiman in NE Chubut, and as far south as Gran Barranca. Pinturan-age deposits are known only from two localities, the Pinturas Formation along the Rio Pinturas in NW Santa Cruz and Gran Barranca. Of the Patagonian occurrences of these SALMAs, three (the Deseadan, Colhuehua- pian, and “Pinturan”) extend in distribution to localities outside the San Jorge Basin and to rock units other than the Sarmiento Formation. Thus, almost all of the mammals known from middle Cenozoic SALMAs in Patagonia had their evolutionary history, in one way or another, tied up with the history of pyroclastic material of the Sarmiento Formation in the San Jorge Basin. In addition to the varying surface area of the San Jorge Basin that came under the influence of the erosion–transport–deposition cycles of pyroclastic sediments, the total surface area of Patagonia also varied with sea-level, and the changing spatial heterogeneity of surface elevations. All other things being equal, the surface area under the influence of mobilized pyroclastics was smaller during marine transgressions, and larger during regressions. In the ten-million-year interval from 40 Ma to 30 Ma, there was a period of transgression between 38.75 Ma and 37.4 Ma. This period of contraction of the surface area of Patagonia corresponds to the interval from the top of the Gran Barranca Member and through the Rosado Member. There followed three shorter intervals of high sea- level in the late Eocene and early Oligocene: (1) from 37.4 Ma to 36.7 Ma (with a peak at 36.9 Ma) during the Lower Puesto Almendra Member, (2) from 35.75 Ma to 34.7 Ma (with a peak at 35.4 Ma), and another (3) from 34.2 Ma to 33.2 Ma (with a peak at 34.1 Ma) during the Vera Member (Miller, 2005). The later and classic transgressions of the “Patagoniano” include the marine San Julián and Monte León Formations exposed along the Atlantic coast of Patagonia and the Centinela Formation in western Patagonia. 87Sr/86Sr measurements from the San Julián Formation yielded ages between 23.83 Ma and 25.93 Ma and between 21.24 Ma and 26.38 Ma for the Centinela Formation, suggesting a Deseadan or Upper Puesto Almendra age equivalence. A single whole-rock 40Ar/39Ar analysis from the Centinela Formation yielded an age of 20.480.27 Ma, suggesting the age of this marine unit may overlap that of the Lower Puesto Almendra Member (Parras et al., 2008). During this time, sea-level may have been sufficiently high for a marine seaway to have extended across Patagonia near the latitude of Gran Barranca.

8.9 Summary

The South American fossil record provides a unique and rich record of the evolution of mammalian tooth shape, especially structural features that serve to resist abrasive wear. However, there are few examples of well-documented morphological transitions. The 8.9 Summary 279

fossil record of “precocious” hypsodonty in Patagonia is discontinuous, as is the available record of downwind sedimentation on the sea-floor. One can find suggestive evidence for the operation of windborne sediment routing systems in the sediment source area and downwind in the sea-floor record of marine productivity. In the most relevant sea-floor sediment cores of the Argentine Basin and Malvinas Plateau, important intervals were not recovered. Where terrestrial fossil preservation permits, age- calibrated change in the evolution of tooth shape are observed, but we may be approaching the limits of resolution for this particular continental sequence. 9 Ever-growing teeth

9.1 Introduction

There is debate in the literature about the effects of grazing mammals on erosion rates (Butler, 1995; Evans, 1998). Either their effects are signiﬁcant (Evans, 1998) or they leave no detectable signature except through local disturbance (Butler, 1995). Given the number of clades that evolved ever-growing teeth and their impressive abundance in the fossil record of South America, one might suspect that ever-growing teeth might have been part of the engine of erosion and contributed to long-term erosion rates. But why? First, there is the fact of their accumulating proportions through time in fossil faunas at every latitude in the Andes. In Patagonia, for example, the proportion of completely elodont taxa increases from about 14% in the Barrancan at about 40 Ma to about 67% in the Mayoan at 11.8 Ma (Table 9.1). Similarly, in the altiplano of Bolivia, the proportion increases from 36% at Salla at 26 Ma to 85% in the late Miocene (10.0–8.5 Ma) at Quehua-Achiri, and in equatorial South America the proportion increases from 34%– 45% at La Venta at 13.61–12.01 Ma to 50% in the Letrero Formation of the Nabon Basin at 11.2 Ma. However, you have to be careful here, because by virtue of their high mineral volume, ever-growing teeth may be over-represented in sampled faunas. Second, as we have seen, while living mammal faunas with high proportions of taxa with high-crowned teeth are associated with topographic relief (mountains), and volcanic activity (andisols), mountain and volcanic environments are naturally highly erosive. In terms of a universal soil loss equation, the contribution of surface disturbance by mammals must have been relatively small by comparison with the role of slope, andisol or pyroclastic sediment cohesion, and plant cover. Similarly, while the proportion of elodont taxa increases through time, the frequency of volcanic eruption and topographic relief also does. For example, the surface area of Patagonia became more extensively covered with the products of pyroclastic volcanism (Ardolino et al., 1999), eruption activity in highland Bolivia accelerated (Trumbull et al., 2006), and sediments in equatorial South America became more ash-rich and preserve increasing evidence of eruption intensity. The coincidence among increasing elodonty, mountain building, and volcanism is certainly true for the Neogene, and especially the Miocene, but it is less clear in the

280 9.1 Introduction 281

Table 9.1 Fossil mammal-bearing stratigraphic sequences in Andean South America

Proportion Present Mammalian of elodont Age1 Paleoelevation2 Elevation taxa3 taxa4

(Ma) (m) (m) (N) (N/[Ne])

NORTHERN ANDES (Colombia–Ecuador) Magdalena Valley La Victoria Fm* (3 N) 13.10–13.61 <250 450 47 0.45 (21) Villavieja Fm*,þ (3 N) 12.01–13.10 <250 450 58 0.34 (20) Southern Ecuador Chinchin Fm (Cuenca) [42.8] ? 2000–3000 - Quingeo Fm (Cuenca) [34.9–42.2] ? 2000–3000 - Saraguro Fm (Cuenca) 20.6–26.6 ? 2000–3000 - [18.5–26.4] Biblián Fm (Cuenca)* 22–24.7 Sea-level 2650 4 0.75 (3) (2.75 S) [12.3–14.7] Burrohuaycu Fm (Sta [10.5–14.7] ? 1180 6 0.50 (3) Isabel)* (3.3 S) Inﬁernillo Mbr (Nabon)þ 13.1 [8.9] 700 2520 - Loyola Fm (Cuenca)þ,** 12.4–12.7 Sea-level 2650 - (2.75 S) [11.1–13.9] El Salado Mbr (Nabón)þ 12.0–12.2 885–1300 2600 - (3.3 S) San Cayetano Fm (Siltstone 12.0 [10.0] ? 2200 - Mbr, Loja)þ (4 S) Guapan Mbr (Cuenca)þ 11.1 [11.5] ? 2650 - Dumapara Mbr (Nabón)þ <11.2 [8.3] 1968 2680 - (3.3 S) Mangán Fm (Cuenca)*,þ 11.7 < 500 2800 2 0.50 (1) (2.75 S) [9.5–9.9] Letrero Fm (Nabón)*,þ,** 11.4–11.5 ? 2680 8 0.50 (4) (3.3 S) [9.0] Picota Fm (Nabón) 10.5 ? 2840 - [7.9–8.5] Llacao Mbr (Cuenca) 9.26 [5.1] ? 2650 - CENTRAL ANDES (Bolivia–NW Argentina) Altiplano Salla* (17.2 S) 25.8–27.0 500–1500 3785 45 0.36 (16) Chucal* (18.7 S, Chile) 17.5–21.7 1000–2500 4200 14 0.57 (8) Caracoles Fm, Potosiþ 13.8–20.7 0–1320 4300 - (19.6 S) Cerdas* (20.7 S) <16.5 800 [500–2000] 3800 22 0.86 (19) Qda Honda* (22 S) 11.9–12.8 750 [500–2000] 3500 30 0.50 (15) Jakokkotaþ (17.15 S) 10.7 550–1600 3940 - Quehua-Achiri* 8.5–10 1400–1500 3895–4000 13 0.85 (11) (17.2–20 S) [1750–3750] Pislepampaþ,# (17.18 S) 6–7 1200–1400 3600 - [2000–4000] Ayo-Ayo, Viscachani, La 3.0–3.27 2850 3274 18 0.67 (12) Paz Fm* [3250–4000] 282 Ever-growing teeth

Table 9.1 (cont.)

Proportion Present Mammalian of elodont Age1 Paleoelevation2 Elevation taxa3 taxa4

(Ma) (m) (m) (N) (N/[Ne])

SE Bolivia Tarija* (21.5 S) 0.021–0.044 ? 1800 57 0.33 (19) NW Argentina Pampa Grande (Lower ? 1800 14 0.0 (0) Lumbrera)* (25.8 S) Pampa Grande (Upper >39.9 ? 1800 - Lumbrera)* (25.8 S) Antofagasta de la Sierra 35–37.6 ? 3420 18 0.33 (6) (Geste Fm)* (26.06 S) Chinches Fm (32 S) 15.3–16.0 ? 25 0.52 (13) San José Fm (marine) 9.8 Sea-level 1800–2200 - (26.75 S) Chiquimil Fm B* >6.7 ? 1800–2200 (26.75 S) Chiquimil Fm A* <6.7 ? 1800–2200 (26.75 S) Andalhualá Fm* (26.87 S) 3.5–5.0 ? 1800–2200 33 0.61 (20) Corral Quemado Fm* < 3.5–4.0 ? 1800–2200 28 0.64 (18) (27.25 S) Uquia Fm* (23.3 S) >2.5 <500 2900–3000 38 0.63 (24) SOUTHERN ANDES (Patagonia) Central Patagonia (45.75 S) Barrancan (Gran 39.0–41.6 Near sea-level 450 29 0.14 (4) Barranca)*,** El Nuevo (Gran 38.5 Near sea-level 450 22 0.32 (7) Barranca)*,** El Rosado (Gran 37.0–38.0 Near sea-level 450 21 0.24 (5) Barranca)*,** La Cancha (Gran 33.7 Near sea-level 450 41 0.15 (6) Barranca)*,** La Cantera (Gran 30.8 Near sea-level 450 41 0.20 (8) Barranca)*,** Deseadan (La Flecha and 24.1–26.3 Near sea-level 200 53 0.30 (16) Cabeza Blanca)* Colhuehuapian (Gran 20.9 Near sea-level 450 77 0.16 (12) Barranca)*,** “Pinturan” (Gran 18.7–19.0 Near sea-level 450 23 0.48 (11) Barranca)*,** Santacrucian (coastal, 16.8–17.4 Near sea-level 25 49 0.35 (17) Levels 1–7)* (55 S) [16.4–17.8] Western Patagonia Boleadoras Fm* (47 S) >16 ? 1300–1450 29 0.48 (14) Río Frías Fm (Chile)* 16.87 ? 1000 38 0.40 (15) (45 S) 9.1 Introduction 283

Table 9.1 (cont.)

Proportion Present Mammalian of elodont Age1 Paleoelevation2 Elevation taxa3 taxa4

(Ma) (m) (m) (N) (N/[Ne])

Collón-Curá Fm* 15.71–16.1 ? 1100 36 0.55 (20) (42.75 S) Rio Chico* (41.77 S) 13.9–14.6 ? 866 16 0.623(10) “Rionegrense”* (42.75 S) 11.7–13.2 ? 850–1100 - - “Mayoense”*,þ (46 S) <11.78 ? 1000 15 0.67 (10)

* Fossil mammal-bearing unit. þ Fossil leaf ﬂoras: Colombia, from Madden et al. (1997); Ecuador, from Kowalski (2001); Bolivia, from Gregory-Wodzicki et al. (1998), Gregory-Wodzicki (2000). # Pollen: Ecuador, Schatz (1994); Bolivia, Graham et al. (2001). ** Phytoliths: Central Patagonia, Zucol et al. (2010), Strömberg et al. (2013). 1 Age of faunas and ﬂoras: Colombia, Ar/Ar, from Flynn et al. (1997) corrected; Ecuador, K-Ar from Lavenu et al. (1992), Baudino (1995), Marocco et al. (1995), Ar/Ar from Madden et al. (pers. com.) corrected, ZFT from Hungerbühler, et al. (1995, 2002), Steinmann (1997), Steinmann et al. (1999) [all in brackets]; Bolivia, K-Ar from MacFadden et al. (1990, 1994), Marshall et al. (1992), Ar/Ar from Kay et al. (1998), Coltorti et al. (2007); NW Argentina, detrital zircon U/Pb from De Celles et al. (2007), Del Papa et al. (2010), Ar/Ar from Kraemer et al. (1999) in Carrapa et al. (2005), ZFT from Jordan et al. (1996), Ruskin et al. (2011), K-Ar from Marshall and Patterson (1981), Butler et al. (1984); Patagonia, Ar/Ar from Franchi et al. (pers. com.), Ar/Ar from Re et al. (2010), U-Pb TIMMS from Dunn et al. (2013). Where magnetic polarity stratigraphies are available, duration of rock units uses the ATNTS of Gradstein et al. (2012). 2 Paleoelevation: Bolivia-Central Andes, Gregory-Wodzicki (2000), Graham et al. (2001), Garzione et al. (2006, 2008) [in brackets]; Ecuador, Kowalski (2001). At tropical latitudes, presence of crocodilians indicates paleoelevation <500 m, absence indicates >500 m based on modern distribution. 3 Fossil mammal taxa (*): Northern Andes (Colombia–Ecuador), Kay and Madden (1997), Madden et al. (pers. com.); Central Andes (Bolivia-NW Argentina), Saint-André (1994), López (1997), Shockey (1997a), Reguero and Cerdeño (2005), Croft (2007), Coltori et al. (2007), Reguero et al. (2007), Croft et al. (2009), Lopez et al. (2011), Powell et al. (2011), Ortiz et al. (2012); Southern Andes (Patagonia), Vucetich et al. (1993), Carlini and Scillato-Yané (1998), De Iuliis et al. (2008), Madden et al. (2010), Vizcaino (pers. com.). 4 Proportion of elodont taxa: N, total number of taxa/(Ne, number of taxa with complete elodonty). Complete elodonty is found in all known Xenarthrans, all Patagoniidae and Argyrolagidae, Mesotheriidae, most Hegetotheriinae, all Pachyrukhinae, all Interatheriinae, post-Santacrucian Toxodontidae, all Caviidae, post-Deseadan Chinchillidae, Huayquerian and later Ctenomyidae–Octodontidae.

older deposits of the Paleogene. With one or two exceptions (at Gran Barranca in Patagonia and possibly also in Central Chile), the Paleogene record is less clear. For example, a pre-Deseadan fossil mammal sequence has yet to be developed in Bolivia (although one has been slowly emerging for the Andes of Central Chile and NW Argentina), despite considerable expenditure of effort exploring and prospecting the thick and well-exposed sedimentary units of that presumed age (e.g., the Camargo Formation, the Potoco Formation). Early Cenozoic sediments in the Bolivian altiplano are devoid of evidence of volcanic activity. Most of the known fossil mammal record in the Altiplano begins with the onset of active volcanism (Trumbull et al., 2006). Most of the Salla fauna come from Units 3–6, a portion of the local stratigraphic section that 284 Ever-growing teeth

extends in age from about 26.55 Ma and 25.65 Ma (Kay et al., 1998). At the latitude of Salla, there was very little volcanism prior to this time, but thereafter volcanism was relatively constant in frequency and type (Trumbull et al., 2006). While Salla rodents show some evolutionary advance in tooth crown height over the oldest caviomorphs in Chile at 31.5 Ma and Patagonia at 30.8 Ma (Patterson and Wood, 1982; Vucetich et al., 2010), they are decidedly less hypsodont than their presumed contemporaries in the Deseadan of Patagonia at 24.1 Ma (Wood and Patterson, 1959). The more hypsodont Patagonian contemporaries are from the Sarmiento Formation, a thick middle Cenozoic section of nearly pure fine-grained pyroclastic sediments. All the available evidence is consistent in showing that low-crowned molars were characteristic of the oldest caviomorphs and those that underwent their early evolution in lowland environments at tropical latitudes; that is, the caviomorphs from Tremembé (Vucetich and Ribeiro, 2003), Amazonian Peru (Antoine et al. 2011), and Santa Rosa (Frailey and Campbell, 2004). Most of the evolution in crown height in caviomorphs occurred in Andean South America (including Bolivia and Patagonia) beginning in the Deseadan, with most of the evolution of elodonty occurring in the Neogene. The evolutionary acquisition of ever-growing teeth in other South American native mammals parallels that of caviomorphs. That is, the transition from hypsodont to elodont molars occurred in the Deseadan with the first appearance of elodont Mesotheriidae, Archaeohyracidae, and Hegetotheriidae in Patagonia and the Central Andes between 30 Ma and 24 Ma. The coincidence between the growing abundance and diversity of mammals with ever-growing teeth in the Central and Southern Andes, together with its long history of uplift and volcanism, combined with the theoretical implications of tectonism for topographic complexity and endemism (Qian et al., 2009; Badgley, 2010), the explosive and ash-rich nature of andesitic volcanism, and the outsized erosion signal downslope (Latrubesse et al., 2007, 2010; Wilkinson et al., 2010), seem to suggest that active surface processes were part of the environmental background during the evolution of ever-growing teeth. Third, besides these general coincidences of geography and timing, there is the implication of what ever-growing teeth really are. Developmentally, an ever-growing tooth results from the prolongation of the developmental process that transforms a low- crowned tooth into a mesodont and then a hypsodont crown. The simple continuation of this developmental process, or the developmental delay in the onset of root formation, ultimately yields an ever-growing tooth. What are the environmental consequences of an animal thereby becoming immune to excess tooth wear and premature dental senescence? Mammals with ever-growing teeth acquire higher levels of ecological flexibility. The distribution of elodont mammals today, around the world, is testimony of the benefits of elodonty to geographic expansion (Figure 9.1). By comparison to other continents, high prevalence of elodonty is a signature feature of South America, and the highest prevalence is found in aridlands. If we acknowledge that overgrazing by hypsodont goats and sheep contributes to desertification along the margins of aridlands today, what might be the potential of herbivores with ever-growing teeth to denude vegetation and accelerate erosion rates? If we remember that rabbits are completely elodont, with ever-growing incisors and cheek teeth, and recall how rapidly rabbits spread through Australia (Coman, 1999)and 9.2 Ever-growing teeth 285

0.4

0.3 North America

South America

0.2 Eurasia

0.1

Percentage elodont mammal species Percentage Africa 0 -60° -40° -20° 0° 20° 40° 60° Latitude

Figure 9.1 The geographic or latitudinal distribution of the prevalence of elodonty in living mammals.

New Zealand (Gibb and Williams, 1990, 1994), and how signiﬁcant rabbits (even at very low densities) are to vegetation change, and how their eradication radically accelerates vegetation recovery (Hall et al., 1964; Friedel 1985), restoration, and stabilization of island environments around the world (Watson, 1961; Flux and Fullagar, 1992), we glimpse something of the potential environmental impact of ever-growing teeth.

9.2 Ever-growing teeth

The term hypselodonty (hyps ¼ exaggerated; elo ¼ high; dont ¼ tooth) does not seem appropriate to describe the diversity of morphology of ever-growing teeth among mammals. All rodents and rabbits have ever-growing incisors, the anterior teeth used for gnawing. These teeth are ever-growing and prismatic (crown breadth dimensions do not change substantially with age or stage of wear, although such change can be very subtle, as in Hydrochoerus), and are sometimes called elodont. When and why rodents and rabbits evolved ever-growing incisors are open questions in paleontology (Wilson, 1951; Carroll, 1988). Many other groups of mammals evolved ever-growing incisors, including the wombats among marsupials, and among South American native marsupials, Groeberia, and while superﬁcially similar, there has not been a comprehensive comparison of the details of their morphology. Some ungulates have evolved ever-growing incisors; among these are the Vicugna, Myotragus, and Marremia, and many of the native South American notoungulates, including taxa of Toxodontidae, Interatheriidae, Mesotheriidae, and Hegetotheriidae. In some cases, this was accompanied by a reduction in incisor number. While we refer to all these examples as ever-growing incisors, these teeth are remarkably different in external form. Ever-growing teeth are not only found in the incisors or anterior dentition. In South American native rodents, the evolution of ever-growing molars occurred in caviids, 286 Ever-growing teeth

chinchillids, octodontids, and at least two other clades. Rodents with both continuously growing incisors and molars are sometimes called fully elodont (Kertesz, 1993). In South American native marsupials, ever-growing molars evolved in the Argyrolagidae, Groeberiidae, and Patagoniidae. In South American native ungulates, ever-growing teeth evolved at many cheek tooth positions, most conspicuously among the rabbit- and rodent-like typotherians and Toxodontidae (Figure 9.2). In fact, of the nearly 26 clades of South American mammals that evolved high molar tooth crowns, half or 13 clades went on to evolve ever-growing molars. None of these examples involves the retention of deciduous crowns (loss of polyphyodonty). It is tempting to assume that all these independent evolutionary events were the consequence of the same sort of developmental transformation, but this has yet to be demonstrated beyond some fundamental similarities in the regulation of the epithelial stem cell niche among laboratory rats, rabbits, guinea- pigs, and voles (Tummers and Thesleff, 2003; Ohshima et al., 2005). Ever-growing teeth have open-roots, that is, the definitive tooth root (or roots) does not form and the enamel and dentin crowns grow continuously throughout the animal’s life (Addison and Appleton, 1915; Shadle, 1936). The difference between a high- crowned or hypsodont tooth and an ever-growing tooth is both developmental and evolutionary. Developmentally, the transformation seems to involve an ontogenetic delay in the onset of root formation. More specifically, the epithelial dental organ does not differentiate into Hertwig’s root sheath. The detailed structural and histological differences in the soft-tissues responsible for crown and root formation in high-crowned and ever-growing teeth have been fairly well documented for laboratory rats, guinea pigs, and rabbits, and aspects of the histology and evolutionary paleohistology of the ever-growing teeth in living and fossil Xenarthra (Ferigolo, 1985), the armadillo (Spurgin, 1904; Simpson, 1932), have been described. Often accompanying the evolution of an ever-growing mechanism is a simplification of crown morphology with a reduction in the complexity of the enamel shearing structures or blades (see Figures 2.1 and 2.5). Furthermore, the continuous production of dense tooth mineral substance creates an obligatory demand for dietary calcium and the physiological requirements of an active dental developmental organ. In addition, to compensate for variable tooth wear rates over the life of the individual, ever-growing teeth require the retention of a mechanism for the facultative control of eruption rates (also known as rates of extrusion or axial migration), and hence, the periodontal apparatus is continually active, sensitive to occlusal pressure, and flexible in response to changing rates of wear (Taylor and Butcher, 1951; Matthews and Berkovitz, 1972; Proffit and Sellers, 1986). In ever-growing teeth, eruption rates are more variable than the rate of incremental growth in mineral substance at the elongating base of the crown (Table 9.2). Eruption rates, also termed axial migration or rates of extrusive growth, are usually measured by marking the crown and measuring the change in distance to the gingival margin (Addison and Appleton, 1915; Dalldorf and Zall, 1930; Rosenberg and Simmons, 1980). Eruption rates impeded by occlusion and unimpeded or potential eruption rates are often compared (Taylor and Butcher, 1951). Crown elongation by the incremental addition of mineral substance is measured by counts of periradicular lines in dentin or counts of cross- striations or perikymata or apposition rates in enamel from stable oxygen isotope variation (Risnes, 1986; Dean et al., 1993; Fricke and O’Neil, 1996; Klevezal, 1996). 9.2 Ever-growing teeth 287

Figure 9.2 Mandibular m3 pseudodevelopment in Pericotoxodon platygnathus (Toxodontidae, Notoungulata) showing how tooth size, crown length, and the proportion of trigonid to talonid change in an ever-growing or elodont tooth. Youngest individual, top, oldest individual, bottom. 288 Ever-growing teeth

Table 9.2 Daily rates of eruption and crown elongation in elodont incisor teeth

Species Daily rate (mm) Measure Reference

Oryctolagus Periradicular line count Rosenberg and Simmons, cuniculus 1980 Rattus norvegicus 0.016–0.024 Circadian increments in dentine Ohtsuke and Shinoda, 1995 Oryctolagus 0.285–0.351 Eruption Shadle, 1936 cuniculus Oryctolagus 0.24–0.89 Eruption Matthews and Berkovitz, cuniculus 1972 Cavia porcellus 0.85 Maximum rate of eruption Dalldorf and Zall, 1930 Rattus norvegicus 0.31–0.40 Eruption Addison and Appleton, 1915 Rattus norvegicus 0.4–0.6 Impeded eruption of lower Taylor and Butcher, 1951 incisor Mus musculus 0.156 (SD¼0.053) Impeded eruption Ness, 1965 0.414 (SD¼0.072) Unimpeded eruption Rattus norvegicus þ/-0.1 Unimpeded eruption Law et al., 2003 0.6þ/-0.1 Impeded eruption Rattus norvegicus 0.288–1.296 Impeded and unimpeded eruption Chiba et al., 1973 Rattus norvegicus 0.925 (SD¼0.11) Unimpeded eruption, mandibular Main and Adams, 1965 incisor

Daily eruption rates in elodont mammals are known to vary from 0.15 mm/d to 1.3 mm/d (Table 9.2). Considerable potential for facultative change in the daily rate of eruption has been demonstrated by comparisons of impeded and unimpeded occlusion (as much as 120% in Robinson et al., 1988; 164% in Law et al., 2003). Daily tooth elongation rates by dentinogenesis and enamel apposition vary from 0.004 mm in bunodont humans (Dean et al., 1993) to 0.11 mm in hypsodont molars of Ovis and Bos (Fricke and O’Neil, 1996), and 0.024 mm by dentinogenesis in elodont rabbit incisors (Ohtsuke and Shinoda, 1995). There is considerable variation in daily rates of enamel secretion (as much as 90% in Robinson et al., 1988) and incremental growth (12.1% in Law et al., 2003).

9.2.1 The measurement of crown height in ever-growing teeth

Measuring functional crown height in an unworn hypsodont tooth is straightforward and a measurement of crown height represents the amount of tooth crown available to the animal during its lifetime. Obtaining a comparable measure of the amount of crown available to an animal with an ever-growing tooth requires an estimation of the total crown height secreted during the animal’s lifetime, and is a completely different problem. Using the circadian recoding structures in dental mineral tissue, the amount of enamel and dentin secreted can be measured, and the variation described. From such a measurement of daily growth increments, the total amount of mineral substance secreted over a lifetime can be estimated. Circadian variation in growth increments are manifest differently in enamel and dentin. Dentinal tubules structurally constrain biomineralization in dentinogenesis to 9.2 Ever-growing teeth 289

elongation, whereas the absence of a structural precursor or organic matrix in enamel means that amelogenesis is unconstrained and growth is expressed as variation in the diameter or width of the prism.

9.2.1.1 Circadian growth structures in dentin Circadian rhythms in the biomineralizing activity of odontoblasts leave a permanent record in the form of incremental structures in the dentin of the ever-growing mouse incisor and these incremental growth lines provide a record of variation in day length. In incisors of some rodent species, incremental growth structures in the mineral tissue of the teeth record variation in circadian activity during the preserved portion of the functional life of the tooth. For some large rodents, a single incisor can preserve a significant fraction of total lifespan. In beavers, as much as 150 daily increments have been counted on a single incisor (Rinaldi, 1999). In smaller rodents, about one month is preserved in the mouse incisor. A mouse incisor measures about 15 mm in length and about 1 mm in width (Figure 9.3). A record of daily variation in the activity of tooth-forming odontoblast cells is preserved in the mineral structure of the incisor dentin. Variation in the rate of dentin formation (termed apposition) reflects variation in odontoblast secretory activity. The amount of dentin deposited in a day varies with the animal’s metabolism, which is subject to internal physiological and external environmental influences, especially temperature and daylength and daylight intensity. Through silver nitrate staining, these periradicular lines appear as alternating hypo- and hypercalcified bands, the degree of mineralization reflected by alternating dark- and light-stained bands. These bands can be counted and their thickness measured. In the mouse incisor, each band is about 0.3 mm thick. Variation in the thickness of periradicular bands reflects variation in the daily rate of dentin apposition. The daily rate of apposition is subject to variation in the environmental conditions that influence the metabolic activity of the odontoblast cells, and circadian photoperiodism is suspected to be the principal mechanism influencing the length of daily secretory activity and amount of dentin apposed by the odontoblasts. One dentin growth increment, comprising a hypercalcified and hypocalcified couplet, represents the daily or circadian rhythm in dentin calcification during appositional growth of rodent incisors (Schuor and Stedman, 1935). The circadian activity of odontoblasts is regulated by the internal circadian pacemaker, which is subject to variation in day length or photoperiod. The adjustment leading to synchrony with the natural diurnal solar cycle is achieved through the mechanism of entrainment. One dentin growth increment, comprising a hypercalcified and hypocalcified couplet, represents the daily or circadian rhythm in dentin calcification during appositional growth of rodent incisors (Schuor and Stedman, 1935). Growth increments can be seen in periradicular bands on the external surface of the incisors of trapped beavers (Castor canadensis), nocturnal rodents from eastern Kansas (Rinaldi, 1995, 1999; Rinaldi and Cole, 2004). The staining method used by Rinaldi (1995) involves submerging the tooth in a 2% silver nitrate solution for one hour, after which the tooth is rinsed with deionized water and placed in sunlight for 24–48 hours. The silver nitrate stains hypercalcification (elevated) dark, and hypocalcification (grooves) light. If staining is suboptimal (in older Figure 9.3 Ever-growing incisor in Sigmodontinae (Rodentia), (A). (From Hershkovitz, 1962, copyright Field Museum of Natural History, used with permission.) Rodent incisor tooth growth occurs through the secretion and apposition or build-up of a layer of mineralized dentine as a coating around the inside lining of the pulp cavity. The pulp cavity is conical in shape (B). Each day the odontoblasts secrete or appose a new conical-shaped layer of dentine on the inside of the previous layer (C). The tooth grows as a stack of nested cones of dentine. In longitudinal cross-section, the cones of dentine are visible as layers or growth lines and the edge of each cone is visible on the external surface of the tooth as periradicular lines or bands. These daily growth increments can be visualized by the naked eye on the medial surface of the incisor as low amplitude waves on surface topography (D), and in a high-resolution stack of microtomographs (E). (Courtesy of MicroPhotonics.com, Allentown, Pennsylvania.) 9.2 Ever-growing teeth 291

Determination of trap date from correlation between growth increment and day length 4

–1

Standardized daylength –2 Growth increment plot of trap date 290 –3 Growth increment plot for trap date 365

240 140 300 360 Day number Estimated trap date Reported trap date 0.65

0.645 0.64

0.635 0.63 Correlation 0.625

0.62 290 300 310 320 330 340 350 360 Trap date

Figure 9.4 Daily growth increments in the dentine of a beaver (Castor canadensis) mandibular incisor from Kansas, in relation to seasonal change in day length. The number of visible and measured daily growth increments (from Rinaldi, 1999) provides a chronometric measure of the amount of time preserved in the dentine of the ever-growing or elodont tooth. Adjusting the ﬁt between measured daily increment width and the day length curve for the capture site reveals the season of growth and date of death (trap date) of the individual.

individuals or smaller species or where sites have little diurnal temperature range), topography can be used to measure the distance between grooves. Measurements of these daily increments can be plotted against day length for the geographic locality of the animal, and when the kill date or trap date is unknown, it can be discovered by the ﬁt between measured daily increments and day length (Figure 9.4).

9.2.1.2 Circadian growth structures in enamel Among the incremental recording structures observed in the enamel of the ever-growing teeth of middle Miocene Toxodontidae (Mammalia, Notoungulata) are cross-striations and striae of Retzius. Incremental cross-striations are ﬁne transverse striations observed in transmitted light that correspond in position to a rhythmical or repeated sequence of alternating enlargement (vericosities) and constriction of the diameter of the prism. Boyde (1979) hypothesized that a cycle of variation in the metabolic activity of

ameloblasts during a 24-hour period leads to variation in CO2 concentration or the total carbonate content of “hydroxyapatite,” and this underlies the change in diameter and refractive index of the enamel prism. As this circadian activity cycle is coordinated in all the ameloblasts of the enamel-producing organ, it results in a coordinated pattern of 292 Ever-growing teeth

Figure 9.5 Enamel and dentine microstructure and daily incremental growth structures in the ever- growing molar of Pericotoxodon platignathus (Toxodontidae, Notoungulata). (A) A mandibular third molar sectioned longitudinally, and with exposed perikymata visible on the external face of the crown (orientation is pulp cavity to the left, occluding surface to the right). Proﬁle of gray shade values of the external surface revealing perikymata. (B) Scanning electron micrograph of a portion of the longitudinal section that has been polished and etched to reveal enamel microstructure, including perikymata, regular Striae of Retzius, and daily incremental growth of enamel prisms. (C) Laser confocal micrograph of the external enamel (small white rectangle in [A]) showing alignment of daily growth increments in the enamel prisms. (D) A fast Fourier transform of the daily growth increments in a portion of the enamel seen in (E) and (F) (the square highlighted in [C]). From a count of these daily increments, the total interval of time represented by the preserved tooth can be estimated.

changing diameter and refractive properties of the prisms. The effect is seen as a linear fabric (Figure 9.5B). In regular alignment, these lineations are normally oriented to the long axis of the enamel prism. Individual vericosities can sometimes be seen in enamel on fresh breaks by light and reﬂected light microscopy, and the aligned vericosities or striations can be seen on polished thin sections under polarized light, on polished and etched surfaces under the scanning electron microscope, and on highly polished thin sections by laser confocal microscopy. Growth layer groups or striae of Retzius are long-period lines hypothesized to correspond in some mammal species to a less well-known circaseptan periodicity in mammalian systemic physiology. There are two kinds of long-period lines, irregular and regular. Irregular striae of Retzius are non-rhythmic or non-incremental (Boyde, 1989) accentuated lines associated with a disturbance in the tooth-forming organ. Regular striae of Retzius are broad bands of hypomineralized enamel marking a surface of enamel formed at one time (Dean et al., 1993; Dean, 1995), and representing 9.2 Ever-growing teeth 293

rhythmic disruptions of amelogenesis resulting in a narrowing of prism diameter and a lateral displacement in the long axis of the prism. The alignment of these disruptions, displacements, or translocations indicate simultaneous coordination throughout the entire population of ameloblasts. Sometimes called brown striae of Retzius, striae of Retzius in the toxodont enamel can be discerned faintly in polished thin sections under reflected light microscopy, or more clearly distinguished by polarized light microscopy and in the scanning electron microscope. The continuously growing enamel in Toxodontidae, being the product of secretory cells, shows circadian and/or cercaseptan periodicities in microstructure similar to that of other mammals (Figure 9.5). While it is not possible to establish that such structures in Toxodontidae reflect chronometric physiological rhythmic variation in ameloblast secretory activity, I would argue that it is probable that these structures have chronometric significance by structural analogy with similar ultrastructure and the universality of this relation among mammal species in which it has been studied. A single tooth IGM 250474 (field number Col89–128), a right third mandibular molar of Pericotoxodon platignathus from Locality 106 in the middle Magdalena River valley, Huila Department, Colombia at 3.25 N latitude, was sectioned and imaged. IGM 250474 (Col89–128) comes from the La Victoria Formation, Honda Group, from sediment dated by 40Ar/39Ar calibrated magnetic polarity stratigraphy to Chron 5AAr (between about 13.14 Ma and 13.30 Ma). The external or labial surface was cleaned of consolidant and adhering matrix, and perikymata were identified (Figure 9.5A), counted, and marked on images taken with a Nikon CoolPix 990 digital camera under directional light. The specimen was embedded in epoxy resin (Buehler Epo-Thin) for thin sectioning. An embedded block was cut longitudinally and the surface polished using fiber optic connector grade polish films (Fiber Instrument Sales, Oriskany, NY, www.fisfiber.com) of graduated (from 15.0 µm to 0.3 µm) particle size. The polished surface was glued to a glass slide using transparent cyanoacrylate. From this mount, a 0.5 mm-thin section was cut with a Buehler diamond wafering saw. The cut surface was again polished, and viewed using green fluorescence at neutral density under a MRC-600 laser scanning confocal microscope at 25 objective magnification and imaged using Bio-Rad software. These images were processed using NIH Image (v1.62/3D) and Adobe Photoshop (v5.0). For scanning electron microscopy imaging, the surface of the embedded block was acid-etched with 10% hydrochloric acid for 10 seconds, washed, mounted and sputter-coated. For laser confocal microscopy, the distal portion of the tooth was embedded in unpigmented Buehler Epo-Thin low-viscosity epoxy resin. A 0.50-mm thick section was cut longitudinally from the occlusal surface to the open pulp cavity using a Buehler Isomet low- speed saw with a low concentration diamond wafering blade (No.11–4254). Both surfaces of the thin section were polished using a graded series of fiber optic connector grade polishing film (Fiber Instrument Sales, Inc.; www.fisfiber.com) from 15, 9, 3, 2, to 1 µm aluminum oxide grit. The sections were mounted to glass microscope slide using cyanoacrylate adhesive and the polished surface was examined under a laser confocal microscope. Images were captured using the MRC-600 laser scanning confocal imaging system (Bio-Rad) with the GFP green fluorescence, and processed using 294 Ever-growing teeth

NIH Image v1.62, without any further adjustments or filtering. A fast Fourier transform (FFT) was obtained of a 256 256 pixel square (Figure 9.5D, E, F). This transform was processed further by erasing all of the image spectrum except that representing incremental cross-striations. After the non-incremental portion of the FFT image was erased, an inverse FFT of the remaining transform revealed cross-striations as parallel grayscale bands. This inverse FFT image was compared with the original laser confocal microscopy images using Photoshop layers. Circadian incremental lines appear as cross-striations resulting from the coincidence or alignment of the changing diameter of enamel prisms. Aligned through coordinated response of all ameloblasts to serum growth hormone pulses, cross-striations reflect the sequence of enlargement and constriction in the diameter of the prism. Cross-striations are thought to result from circadian variation in the secretory activity of ameloblasts. By rather circumstantial evidence, its universality for all mammals is commonly assumed. Striae of Retzius are conspicuous in sectioned enamel of Toxodontidae, under light, laser confocal, and scanning electron microscopy. These striae or lines are produced by the coincidence of two or more cross-striations in adjacent prisms. The number of circadian cross-striations between striae of Retzius is commonly reported to be between seven or eight, but varies from between six and 14 (Hillson, 1986). While the etiology of the cercaseptan periodicity of striae of Retzius is unknown, the repeat interval suggests a physiological basis with a constant rhythm. Perikymata are the surface manifestation of the striae of Retzius (Figure 9.5B) and are continuous with underlying regular striae of Retzius. Perikymata are visible ridges and troughs formed at regular intervals around the circumference of the enamel crown and extending from the apex or occlusal surface to the base. The topographic trough of each perikymata corresponds to the point where a regular striae of Retzius reaches the outside surface of the enamel. In ever-growing toxodont lower molars, there is a one-to-one correspondence between perikymata and striae of Retzius as all striae reach the surface. To estimate the total crown height of an ever-growing tooth requires determining the interval of time represented by the tooth, as discussed previously, then estimating what proportion of total lifespan the single crown represents. How much tooth crown could an individual animal erupt during its lifespan? Lifespan in toxodonts can be estimated using the length and diameter of limb bones (Alexander et al., 1979), the length and breadth of the first lower molar and an all ungulate regression from Damuth and MacFadden (1990), and the mammal body weight/lifespan regression of Western (1979). In summary, the differences between high-crowned and rooted teeth and ever- growing and rootless teeth may involve: (1) the arrangement of the periodontal ligaments, (2) the disposition of the pulp cavity (epithelial diaphragm), (3) the duration and persistent incremental function of the enamel- and dentin-forming organs, (4) the proportion of dentin to enamel, (5) rapid collagen turnover, (6) the extent and distribution of cellular cementum, and (7) a reduced alveolar process in conformity with a more simplified crown. While these features are discussed separately, they all form part of Zajicek’s proliferon (Zajicek, 1976). 9.2 Ever-growing teeth 295

9.2.2 Periodontal ligaments

The arrangement of the periodontal ligaments is different in elodont and hypsodont teeth. The dorsoventral coverage of the transseptal ligaments that connect adjacent teeth above the alveolar crest may be greater in elodont teeth. The oblique ligaments that connect the tooth to alveolar bone and provide most of the support against masticatory forces, occur in moderate density along the sides of the roots in rooted teeth. In elodont teeth, they are extremely dense and are found on the lingual and labial surfaces of the anatomical root. They may appear to attach directly to enamel but microscopic examination reveals an extremely thin (1 µm) layer of cementum covering the mature enamel and enamel cuticle at the site of attachment. Alveolar crest ligaments extend from the alveolar crest to the tooth. In elodont teeth, the area above the alveolar crest generally has no well-defined fiber bundles because of dissolution associated with eruptive movements in the occlusal plane. The periodontal ligaments attached to the crest of the alveolar bone are essentially the same as the oblique ligaments. Apical ligaments are lacking in elodont teeth owing to continuous dental development in this region. By their configuration, the periodontal ligaments are involved in the continuous eruption of elodont teeth. It has been observed that the width and histological distinct- iveness of the intermediate plexus (the middle zone of the periodontal membrane of interwoven cemental group of fibers attached to the root and alveolar fibers) is related to the eruption rate of ever-growing teeth (Sicher, 1942). More recently, Phillips and Oxberry (1972) suggested that the formation of new oblique ligament bonds by the physiochemical splicing of the fiber bundles in the persistent intermediate plexus propels continuous tooth eruption in elodont teeth.

9.2.3 Persistent enamel-forming organ

The presence and persistent activity in the adult of the organic matrix and formative cells of the enamel-producing system deﬁnes continuous growth in the elodont mammal. The evolutionary transition from hypsodont to elodont involves the persistent function of the enamel-producing system into progressively later adult stages by pedomorphosis, the retardation of tooth maturation, and a developmental delay in the onset of root formation. In teeth that form roots, all the enamel becomes fully crystallized and no embryonic zone of enamel formation will be found once crown formation is complete and root formation initiated. In mammals with ever-growing teeth, the enamel cuticle persists and immature enamel may be seen around the anatomical root (open pulp cavity). Mature ameloblasts in the enamel cuticle are maintained in direct contact with the loose connective tissue of the stellate reticulum. The differentiation of cementoblasts from this connective tissue produces a thin layer of cement, which covers the mature enamel and enamel cuticle. This thin layer of external cementum can be deposited over the mature enamel of hypselodont teeth only so long as the enamel cuticle contacts the connective tissue of the stellate reticulum. 296 Ever-growing teeth

The migration of ameloblasts in the growth organ of an ever-growing tooth is accompanied by cell proliferation at the base of the tooth and degeneration and cell death following mineralization at the superior margin of the growth front (Moe, 1979).

9.2.4 Enamel crown simpliﬁcation

Often, ever-growing teeth are described as prismatic, with constant cross-sectional area. However, the circumference of an ever-growing crown may increase ontogenetically. The enlargement of circumference must occur evolutionarily by prolonging the function of odontoblasts and thereby increasing the volume of dentin. As this occurs in Tox- odontidae, the enamel organ becomes subdivided into independent organs or developmental fronts. With the progressive evolution of ever-growing crowns in Toxodontidae, the formerly fully circumferential enamel retreats from the salient angles of the crown both ontogenetically and phylogenetically. This is also true for many other notoungulates, where the subdivision of the enamel-forming organ occurs at or near the edges of the dentin crown. Enamel is deposited on primary dentin. Once dentin forms, ameloblasts receive nutrient supply through the outer enamel epithelium. Once the enamel is fully matured, ameloblasts pass through a brief protective stage, forming a stratiﬁed epithelial covering over the fresh enamel. When the reduced epithelium retracts from the surface of the mature cervical enamel, connective tissue comes into contact with the enamel and a layer of cementum begins to be deposited. The arrangement of the enamel is different in elodont teeth compared with their hypsodont and rooted evolutionary precursor. There is a retreat of the enamel from around the full circumference of the crown, its restriction to ﬂat surfaces as functional blades, and the loss of internal enamel-lined fossettes (or fossettids). Among xenarthrans, enamel was lost altogether and the loss might be assumed to have accompanied or shortly followed the evolution of ever-growing capability. Isolated enamel fossettes cannot be sustained physiologically in ever-growing teeth because of the physiological isolation of the enamel-producing organ (including four distinct layers: outer enamel epithelium, stellate reticulum, stratum intermedium, and inner enamel epithelium or ameloblastic layer) from its nutrient matrix. In effect, the enamel organ becomes physiologically isolated laterally and basally from its nutrient supply.

9.2.5 The arrangement of cementum

Cementum covers the anatomical roots of the teeth in most mammals. Functionally, cellular cementum provides an attachment site for the periodontal ligaments, which anchor the tooth. In rooted teeth, the cementum layer is thickest at the apex of the root. In both rooted and rootless molars, the cementum may become modiﬁed to cover all or part of the enamel of the crown (Hunt, 1959). The cementum covering the roots generally extends over the coronal enamel above the cementoenamel junction to some but variable extent. The superﬁcial layer of cementum covers the roots in mammal teeth 9.2 Ever-growing teeth 297

and serves as a medium for the attachment of ﬁbers that bind the tooth to surrounding structures. Where cement is covered by oral epithelium or exposed as part of the crown, it is acellular. The cementum extending over the coronal enamel above the cementoenamel junction is acellular, and associated lacunae are considerably more irregular and numerous. In elodont teeth, cementum is lacking from the apical half of the anatomical root because this portion is covered by maturing enamel and the enamel epithelium. The mature enamel above the enamel-forming front may be covered by a thin layer of cementum. The dentin exposed on the surface of the crown in enameless regions is covered by a narrow strip of cellular cementum which is a continuation of the cementum covering the anatomical roots in rooted teeth. This cellular cement may be thickened to serve as an external buttress around the crown.

9.2.6 Alveolar bone

Both lamellar bone of the inter-radicular septa and compact bone at the interdental septa occur in multirooted teeth. By contrast, the alveolar process around elodont teeth is reduced owing to their ever-growing nature and more simplified structure. Small pointed alveolar septa may occur in the interstices below the base of the cellular cementum (e.g., between enamel folds). These septa will consist entirely of bundle bone, reflecting the constant resorption and apposition resulting from continual growth of the teeth. Bundle bone can also be seen on the surface of the compact bone of the interdental alveolar septum where Sharpey’s fibers penetrate the alveolar bone. In some mammals with ever-growing cheek teeth (rabbits, for example), alveolar bone covering the base of the crowns projects upward into the orbit. This suggests there may be some constraint that limits crown height, or a structural compromise is required between mandible depth, palate height, and the structural demands of the special sensory systems. In the maxillary dentition in Toxodontidae, a limit is reached when the enamel forming fronts or pulp cavities of the right and left tooth rows arc over the palate and converge at the anatomical midline. In the mandibular dentition of Toxo- dontidae with ever-growing cheek teeth, one sometimes observes the open pulp cavities exposed through the bone, and judging from the position of the ever-growing incisor and m3 crowns, height may be compromised by functional requirements of the masticatory musculature. Pathological elongation of the ever-growing tooth crowns and encroachment on surrounding tissues are well known in clinical veterinary practice (Crossley et al., 1998). The domesticated chinchilla (Chinchilla laniger) with ever-growing cheek teeth, when removed from their highly abrasive natural habitat in the Andes, develop dental abnormalities in captivity, even on a diet of dried vegetation and hay. Apparently, a diet of dry herbage and grass alone does not satisfy the obligatory rate of tooth wear required to compensate for the growth capacity of the developmental organ. What these animals are lacking would seem to be volcanic ash soil as a supplement in their diet. 298 Ever-growing teeth

9.3 Why ever-growing teeth?

Why do ever-growing teeth evolve? Presumably, it is the evolutionary response to highly abrasive tooth wear. While it might be assumed that ever-growing teeth imply increasing dietary specialization to the grazing habitus (or increasing levels of abrasives in the diet), once evolved, these teeth just as likely permitted dietary diversification and the occupation of otherwise inhospitable environments. More speculatively, the simplified occluding surfaces of ever-growing teeth replace the more precise and complex enamel shearing mechanism of rooted teeth, with a more imprecise grinding mechanism. This seemingly illogical correlation of ever-growing mechanism and simplified crown might be explained if one beneficial consequence of the evolution of ever- growing teeth was that ingested mineral particles enhanced the mechanical reduction of plant material. Pulverizing rather than cutting plant tissue between occluding teeth thereby might serve to increase the exposed surface area of ingesta accessible to gut microbes. One can imagine many possible explanations for the evolution of ever-growing teeth. (1) Increase occlusal pressure. If one could examine bite force and the occlusal musculature of representatives of closely related mammals with diverse low, high, and ever-growing cheek teeth, and found the masticatory muscle complex similar in structure, mass (of individual muscle masses and total muscle mass), fiber orientation, and functional myography producing the same bite force, then high or increasing occlusal pressure would not be a very satisfactory explanation for the difference between rooted and ever-growing teeth. Scarano (2009) describes the notopithecine–interatheriine transformation from hypsodont to elodont cheek teeth wherein there is little or no change in the masticatory apparatus and nothing to suggest increased bite force. (2) Permit more voluminous food intake and enable a shift toward a diet based more on quantity than quality. Many different kinds of foods can be processed with the grinding action of a simple mortar and pestle; for example, an armadillo, which has simplified elodont teeth associated with high dietary diversity and habitat plasticity. As body size does not change across two well-known transformations among notoungulates (Notopithecinae–Interatheriinae and “nesodontine”–Toxodontinae), metabolic requirements presumably stayed the same. A diminution in food quality might imply that the number of chewing cycles would have to increase. (3) Permit the consumption of higher quantities of mineral abrasives, whether (a) silica phytoliths (variables: occurrence, concentration, size/shape, habitat specificity, or association with vegetation of limited complexity and architecture) or (b) soil mineral grit (variables: rainfall and vegetation, seasonality, habitat, exposed soil/erosion by overgrazing and footfall, wind, mineral hardness). This seems to be the case among extant Bovidae; that is, higher-crowned species are grazers in open habitat (Janis, 1995) and there is more soil in the diet in higher-crowned species (Kaiser et al., 2013). (4) Other explanations are also plausible. As high-crowned cheek teeth are demon- strably suitable for all kinds of herbivory and omnivory, higher-crowned and 9.4 Consequences of the evolution of ever-growing teeth 299

ever-growing teeth may be especially useful on small islands. In these settings of geographically variable and unpredictably and often scarce food resources, selection for increased reproductive lifespan (by all possible means, including pedomorphosis) may provide both proximate and ultimate causes for the evolution of higher-crowned and ever-growing teeth (Köhler and Moyà-Solà, 2009; Jordana and Köhler, 2011; Jordana et al., 2012).

9.4 Consequences of the evolution of ever-growing teeth

One possible consequence of the evolution of ever-growing teeth is liberation from selection by excess tooth wear and premature dental senescence, the opening of opportunities, and the potential to exploit marginal habitat, especially more highly abrasive environments (Figure 9.1). The first appearance of ever-growing teeth in a clade generally but not necessarily follows evolutionarily from a precursor stage that would be called hypsodont. The evolutionary appearance of elodonty seems to be accompanied by taxonomic proliferation, not reduction, and geographic spread. Even- tually, diversity within these clades seems to winnow, but whether this is the normal pattern for clades, or something distinctive of clades that evolve ever-growing teeth, is not known. What is the actual evidence for the occupation of marginal habitats or habitats characterized by higher mineral particle flux subsequent to the evolution of ever- growing teeth? Not much. For example, among Notohippidae, Argyrohippus (Colhuehuapian) and Notohippus (Santacrucian) were the last surviving notohippids out of a prolific Deseadan radiation, and the Colhuehuapian–Santacrucian interval in Patagonia is not known for high erosion rates, although erosional unconformities are numerous (Bellosi, 2010), and volcanism was intense (Ardolino et al., 1999; Ré et al., 2010) and sedimentary depositional environments were diverse. Nevertheless, the fact is, nobody has characterized the intensity of erosion in Patagonian middle Cenozoic environments where we can document the first appearance and subsequent accumulation of taxa with ever-growing teeth. Whenever and wherever fully elodont rabbits have been introduced, does an increase in surface erosion follow? There seems to be a natural tendency to blame prolific reproduction, population irruptions, warren excavation and toe-nails, rather than tooth morphology, for all the mischief rabbit introductions cause on the earth surface. However, studies seem to show a significant grazing impact on vegetation when rabbits are present, even at low and constant densities (Cooke, 1987). This is especially true on volcanic islands with tuffaceous soil parent material.

9.4.1 Rabbit introductions and eradications

The impact of elodonty on denudation and erosion might be approached by examining vegetation change and land degradation following rabbit introduction and ecosystem recovery following rabbit eradication. The consequences of rabbit introductions and 300 Ever-growing teeth

their impact on vegetation and the soil surface is difficult to study as most introductions occurred a long time ago (Flux and Fullagar, 1992), and experimental introductions for this purpose are unlikely to be approved today. However, there is a rich literature describing vegetation restoration following rabbit eradication. While recovery is not a simple reversal of the effects of introductions, studies of vegetation recovery in exclusion areas and following complete eradication provide useful insights into the potential of rabbits to influence surface processes. In general, the ecological damage caused by rabbits can be severe on islands, many of which have been denuded of vegetation and rendered vulnerable to erosion. On Philip Island, for example, rabbit-induced soil erosion reduced the island almost to bedrock and the surrounding sea was observed to turn brown with suspended sediment (Fullagar, 1978; Coyne, 1981). On Macquarie Island, rabbits reduced the vegetation to such an extent that soil loss and land-slip erosion became significant (Costin and Moore, 1960; Copson and Whinam, 1998). It has been shown that rabbits simplify vegetation by removing the forest understory, reducing overall plant diversity, increasing the age of canopy trees through seedling predation, and affecting the balance, distribution, and abundance of palatable and unpalatable plant species (North et al., 1994; Copson and Whinam, 1998; Chapuis et al., 2004). So tenacious is their occupation that even small numbers of rabbits cause major ecological damage and prevent the regeneration of native trees and shrubs (Cooke, 1987; Auld, 1990). So resilient are rabbit populations that complete eradication from large islands and continental landmasses has proven simply impractical. There are many interesting examples of the consequences of rabbits, including two examples of exclusions from small portions of larger landmasses and many examples of eradications from small islands, both volcanic and non-volcanic. It is especially interesting to review their environmental consequences in terms of soil erosion, and to the extent possible to distinguish among the activities of coexisting mammalian herbivores with different kinds of teeth, bunodont (as in pigs), hypsodont (but rooted, as in goats and sheep), partially elodont (as in murid rodents), and fully elodont (all teeth rootless or ever-growing, as in rabbits). Of special interest are examples where two or three tooth types; for example, bunodont (pigs), hypsodont (sheep or goats), and elodont mammals (rabbits) were introduced onto islands at different times, coexisted, and thereafter were controlled or eradicated sequentially, leaving one or the other to persist alone for a time. From anecdotal records it is difficult, maybe impossible to distinguish between the impact of partially elodont rodents (Muridae), hypsodont ungulates, and fully elodont rabbits. Do rodent or rabbit introductions have different effects on the vegetation and land surface (denudation or increased erosion through effects on vegetation)? Athens (2009) has argued recently that rats caused catastrophic loss of native lowland forest in Hawaii, but this opinion is controversial. By contrast, the impact of rabbits on island or continental ecosystems following their introduction is legendary. Rabbits have ever- growing incisors and ever-growing cheek teeth (molars) as well. On scanning the literature on rabbit-induced change in native floras, their role in the modification of vegetation structure and their contribution to surface denudation and erosion is quite 9.4 Consequences of the evolution of ever-growing teeth 301

clear. These mammals can and do have a detectable influence and their impact is felt through their burrowing or digging activity, their role as seed predators, and their effects as grazers. The consequences of rabbits for erosion on small volcanic and non-volcanic islands can be contrasted. As will be seen, small island ecosystem response to the control or eradication of rabbits is abundantly documented by change in vegetation and flora. Because the trophic cascades among mammals and between mammals and plants on small island ecosystems can be complex, the consequences of eradication are difficult to predict, and the attribution of cause to effect can be difficult to substantiate (Bergstrom et al., 2009a, b; Raymond et al., 2011), because descriptions of soil erosion by zoologists, ornithologists, or botanists are almost universally anecdotal. Detailed studies of erosion regimes and change in rates of erosion are very rare in the context of the eradication of invasive species. This is unfortunate, and might be remedied in ways I suggest at the close of this review. Nevertheless, the difference in the erosion caused by rabbits on volcanic islands and non-volcanic islands is noteworthy, as we shall see.

9.4.1.1 Australia and the arid rangelands From 24 individuals introduced to Australia in 1859, the population of Oryctolagus cuniculus grew and spread rapidly, advancing at a rate of 70–100 km/yr and extending over two-thirds of the continent by 1910 (Ratcliffe, 1959). As early as 1880, farms had to be abandoned because of de-vegetation by rabbits (McTainsh and Boughton, 1993). Rabbits spread more rapidly in the arid and semiarid part of Australia, more slowly along the wetter Paciﬁc coast. Their spread stopped near the Tropic of Capricorn. Rabbits spread through the dust source area of the Lake Eyre Basin in South Australia between 1880 and 1890. Anecdotal accounts of this “plague” describe a peak of rabbit abundance between 1890 and 1910 when there was an estimated one billion rabbits, but by 1926 this population had “exploded” to 10 billion (Williams et al., 1995). At the same time rabbit abundances were escalating uncontrollably, between 1887 and 1902 the number of sheep in Western New South Wales decreased from 15 to three million head (Condon and Stannard, 1956). The simultaneous increase in rabbit abundance and decrease in sheep abundance in the western Murray–Darling basin between 1880 and 1910 suggests competitive exclusion. Similar to what happened in the American West in the 1930s, the “dust bowl” years in Australia in the 1940s marked peak erosion on that continent in the twentieth century. As in North America, this event is attributed to a combination of human and natural causes, affected wide areas of the interior on both continents, and on both continents was accompanied by a plague of rabbits. In Australia in the years leading up to the 1940 peak, manifestations of increasing erosion were felt and public response included enactment of the South Australia Sand Drift Act to prevent sand drifting onto public roads, the work of the Sand Drift Committee between 1923 and 1933, enactment of the Soil Conservation Act in New South Wales, and authorization of the Committee on Soil Erosion in South Australia in 1938–1939. Coincident with the acceleration of erosion in the 1930s, livestock numbers recovered, and attained their highest numbers on record 302 Ever-growing teeth

just before the onset of a decade of severe droughts in the 1940s. By 1940, the interior of Australia was devastated by the combined overgrazing of sheep and rabbits (Pick, 1942; Pick and Alldis, 1944). This situation of combined drought and high grazing pressure lasted until the first wave of Myxoma in 1950. Myxoma virus was released in 1950 and killed 99.8% of infected rabbits. Once released from competition, there was a significant recovery in the wool and meat industries within three or four years. With time, rabbit resistance to Myxoma virus gradually increased until rabbit hemorrhagic disease (RHDV) or rabbit calicivirus was released in 1995 with great effect in arid parts of Australia. The 50-year period of maximum rabbit abundance between 1890 and 1940 (including the period between 1887 and 1902 when sheep numbers decreased), the control efforts through myxomatosis starting in 1950, the recovery after this Myxoma wave, and the re-depopulation by calicivirus in the late 1990s, describes a unique history of population fluctuation in Australian rabbits. This pattern of temporal change differs from that of sheep. Sheep decreased drastically between 1887 and 1910, recovered through the 1930s, declined during the droughts of the 1940s, and recovered again beginning in 1950. The differences imply that a unique rabbit signal may be present in continuous erosion records covering the period between 1850 and 2000. Is this unique “rabbit- induced erosion signature” detectable in either high-resolution lake or ocean sediments (off the mouth of the Murray–Darling system), in ice core dust records (for example, on the Tasman and Cook glaciers in the South New Zealand alps, or short snow and ice cores from Antarctica), or dust-storm event records? The best high-resolution records of erosion in Australia identify the beginning of European influence (McCulloch et al., 2003), and this record points to coincident dust events during a period of peak rabbit abundance. The coral Ba/Ca record of suspended sediment influx onto the Great Barrier Reef from plumes off the mouth of the Burdekin river in northern Queensland (about 19 30 m S) clearly identifies the onset of European settlement in 1870 (McCulloch et al., 2003). A 30% increase in baseline Ba/Ca (representing a five- to ten-fold increase in suspended sediment load), beginning in 1870, must be attributed to the initial and rapid introduction of sheep and then cattle. The process is accredited to the erosion of riverbanks by hooves, rather than the denudation of vegetation by grazing. However, a peak flood event in 1981 is attributed to a decade of land-clearing with the introduction of drought-resistant cattle (Bos indicus). A brief partial record of topsoil erosion preserved as sediment on the bottom of a reservoir is coincident with one particular event in the history of rabbit abundance (Clark, 1986). Clark (1986) developed pollen analysis as a chronometer and sediment tracer in cores from Burrinjuck Reservoir at the confluence of the catchments of the Yass, Murrumbidgee, and Goodradigbee rivers in western New South Wales. From these cores, an annual record of waterborne pollen was developed for the interval between 1938 and 1957, an interval that includes the Myxoma release of 1950. The combination of high pollen numbers per unit of weight of silt, low clay content, and a high proportion of damaged pollen grains is suggested as an indicator of topsoil erosion. 9.4 Consequences of the evolution of ever-growing teeth 303

The intensity of topsoil erosion falls precipitously in 1950 at the beginning of a low erosion period that extends through 1955. Particularly large dust transport events were observed downwind in New Zealand during the years of peak rabbit and low sheep abundances in Australia in the early twentieth century (Marshall, 1903; Marshall and Kidson, 1929; Marx and McGowan, 2005), and air parcel trajectories have the potential to distribute Australian dust from the Lake Eyre Basin and western New South Wales over a large part of the southern hemisphere (McGowan and Clark, 2008). Comprehensive sampling of sediments throughout the Murray–Darling Basin and their trace-element systematics (Marx and Kamber, 2010) permit precise dust- provenance studies. Given the unique composition of rare earth elements in SE Austra- lian dust (Marx and Kamber, 2010; Wegner et al., 2011), records from annually resolved short Antarctic ice cores (Ferris et al., 2011) or New Zealand alpine glaciers might eventually detect the rabbit signal, if it is as unique and significant as I suspect. Dust deflated off SE Australia appears in New Zealand peat bogs from Central Otago (Marx et al., 2009). Unfortunately, the uppermost 150 years of the record (the portion that would reveal a rabbit signal) cannot be age-calibrated because the surface was affected by disturbance with the local introduction of sheep in 1850. A huge acceleration in the sediment flux in the upper catchment of the Murrumbidgee River in SE Australia (including the southern tablelands and Canberra) followed European colonization and the introduction of livestock between 1820 and 1850. Through burning, clearing riparian vegetation, the introduction of rabbits, and the intensification of combined cropping and grazing production systems, erosion rates in the headwaters increased about 250 times compared to pre-European rates. Most of this acceleration occurred through gully erosion initiated by grazing. Subsequent to the time gully networks attained their maximum extension, and immediately following the widespread reduction in rabbit abundance in 1950, vegetation recovered and sediment yield began to decline to levels where it is now, only six times the pre-European rate (Wasson et al., 1998; Olley and Wasson, 2003; Olley and Wallbrink, 2004). In SE Australia, Wasson and Galloway (1986) found that sediment yield following European settlement (with overgrazing by sheep and rabbits) was 50 times greater than the average yield for the 3000 years before settlement, and Fanning (1994) found a 15- to 100-fold increase in soil loss. These findings generally are consistent with the observation that the former vegetation was fairly continuous, an even scatter of trees and grass with other groundcover plants. The removal of this continuous vegetation coincided with the introduction of sheep and rabbits. Following their introduction, land degradation accelerated and included increased runoff, incision erosion, surface stripping of the floodplain, and the disappearance of waterholes along main river channels (Fanning, 1994). The annual frequency of dust storms in SE Australia has decreased since the 1970s, and this reduction is attributed to a combination of rabbit control through myxomatosis starting in 1950, the spread of weeds, and the adoption of conservation tillage. Rabbit depopulation in the late 1990s following the release of calicivirus is thought to have promoted vegetation recovery and reduced wind erosion in SW Queensland, north South Australia, and west New South Wales (McTainsh, 1998; Neave, 1999). 304 Ever-growing teeth

9.4.1.2 New Zealand The impact of rabbits on both the non-volcanic South and volcanic North Islands of New Zealand is sometimes said to be significant, but their effects on erosion are very difficult or impossible to distinguish from sheep ranching. Rabbits were introduced onto the North Island in the Wairarapa about 1863 and had spread to Hawke’s Bay by the beginning of the twentieth century. They reached the far north of the North Island in 1946 (Peden, 2012). Grant (1965) showed how rates of erosion in Hawke’s Bay have varied between periods of relative stability alternating with periods of more rapid erosion. Average sediment transport rates on the upper Waipawa River (Ruahine Range) in the 1970s was 13 times that of the early-mid 1940s (Grant, 1977). In parallel to the increased sediment transport rates, James (1973) showed that the extent of eroded surfaces in upland areas exposed by mass movement increased by 60% between 1946 and 1963, and bare area increased by another 120% by 1974 (Cunningham, 1978), with the effects of mammals at least partly responsible (James, 1973; Cunningham, 1979). Significant event horizons are recognized in the sediment record of the Waipaoa catchment and sedimentary system in the northeastern North Island of New Zealand (Gomez et al., 2007), and cores from Lake Tutira near Hawke’s Bay (Page et al., 1994a; Wilmshurst, 1997), but these are not associated with significant events in the history of rabbits. For example, the Taupo eruption (1.718 ka) increased suspended sediment discharge by 190%, Polynesian arrival (about 0.56 ka) increased suspended sediment discharge by 140%, and European arrival (in 1835) (0.15 ka) increased it by 350% when lowland forest was cleared. Deforestation intensified, starting about 1850, and after 0.04 ka discharge increased by as much as 60% when pasture was extended up fragile or susceptible hill slopes (Gomez et al., 2007; Kettner et al., 2007). In addition to suspended sediment discharge, long-term sedimentation rates increased from about 3.3 mm/yr to >10 mm/yr, following the Europeans’ arrival and the onset of land conversion to pastoral agroecosystems (Orpin et al., 2010). None of these events are related to rabbits. Wilmshurst (1997) distinguished two phases to European settlement and deforestation in pollen zones of the Lake Tutira sediment cores. The first phase began around 1870 when the last forests and fern-scrubland of the lowlands and hill country were cleared and pollen from introduced plants first appears. This first phase is characterized by a decline in podocarp taxa, a stabilization of bracken, and an increase in grass. By 1930, most of the watershed was converted to pasture (Page et al., 1994a). A second phase documents the conversion of most of the remaining forest and bracken-scrubland to improved pasture. In this second phase, Poaceae pollen rapidly increases along with exotic taxa that are part of more sophisticated, productive, and diverse artificial pastureland. Erosion pulses characterize both phases, but these are thought to reflect the increase in the frequency of high-intensity rainstorm-induced erosion events or the increase in sheep pasture area, not the influence of rabbits. While the effects of rabbits on New Zealand ecosystems are difficult to separate from those of other herbivores (sheep) and burning (deforestation), significant reductions in rabbit abundance coincide with declines in the extent of bare ground and increases in plant and litter cover (Parkes, 1995). 9.4 Consequences of the evolution of ever-growing teeth 305

One might suspect that rabbit impacts on erosion might be greater in arid and semiarid environments, and there are reports of rabbit impacts on erosion on the South Island. The semiarid tussock grasslands in the rain-shadow of the Southern Alps in Central Otago have been utilized for sheep farming since 1850. Grazing pressure was increased in 1870–1880 by a rabbit irruption, such that by the early part of the twentieth century, parts of the area were described as a “man-made desert” of bare soil where erosion was accelerated (Mather, 1982). Rabbits were deemed to be responsible for this land deterioration and the general desert conditions in Central Otago and the Mackenzie country (Cumberland, 1944). Bare soil and rabbit feces are associated along a gradient of disturbance in the driest part of the Central Otago (Walker et al., 1995), and grazing by Oryctolagus cuniculus has a detectable inﬂuence on short-tussock grasslands, signiﬁcantly reducing pasture growth (Norbury and Norbury, 1996). A 40-year average annual soil loss of 10.2 t/ha was measured on sunny upper slopes where the combination of sheep and rabbit grazing was observed to deplete vegetation and increase the proportion of bare ground (Hewitt, 1996).

9.4.1.3 Small volcanic and non-volcanic islands The impact of elodonty on soil erosion is often difficult to establish on large landmasses and islands, where separating human from rabbit influence is nearly impossible. However, there are numerous small islands off New Zealand and Australia, and elsewhere across the South Pacific (for example, Laysan in Hawaii) and around the world, where rabbits were introduced and humans never colonized. In fact, the Euro- pean rabbit has been introduced onto 598 islands around the world (Flux and Fullagar, 1992). Around New Zealand, Macquarie Island is one particularly well-documented example, as is Bare Island off Hawke’s Bay. There are numerous other oceanic islands and coastal islands around Australia that inform as to the role of elodont mammals (Armstrong, 1982) and where rabbits are known to have become extinct because of overgrazing (Watson, 1961; Armstrong, 1982; Cooper and Brooke, 1982). It is estimated that more than 10% of rabbit introductions on small islands resulted in dramatic impoverishment of the vegetation and the rapid and natural extinction of the rabbits (Flux, 1992). The quality of observations about the consequences of rabbit introductions is variable, as the following case studies reveal, but their introduction is almost universally associated with de-vegetation and accelerated erosion.

9.4.1.3.1 Round Island Round Island, Mauritius (19.85 S; 57.783 E) is a 151 ha, rugged, uninhabited volcanic island 20 km NE of Mauritius. Rabbits and goats were introduced onto this extinct basaltic volcanic cone in the nineteenth century. The goat population was reduced by a severe cyclone in 1975–1976 and eradicated in 1978. Rabbits (Oryctolagus cuniculus) persisted and became especially abundant in 1982, and were eradicated in 1986. Vegetation change three years after rabbit eradication was described by comparing the vegetation in 1975 (when goats and rabbits were present), in 1982 (only rabbits), and in 1989 (after rabbits were eradicated) (North et al., 1994). Between 1982 and 1989, there was a marked increase in vegetation cover due to the spread of the grass Chloris barbata. 306 Ever-growing teeth

Prior to rabbit eradication, this grass was found in widely scattered tussocks on bare coastal fringes or inaccessible ledges. Once released from grazing pressure, it rapidly colonized extensive areas of bare earth. Three palms (Latania, Hyophorbe, and Pandanus) also increased along with the spread of palm savanna. Since eradication, the formerly abundant grazing-tolerant plants favored by high rabbit densities and/or rabbit-induced soil disturbance decreased, while plant species formerly kept at low abundances increased once released from the dietary pressure of rabbits. Following rabbit eradication, soil erosion was reduced and vegetation cover increased as did soil accumulation and soil water retention (North et al., 1994).

9.4.1.3.2 Phillip Island Phillip Island (29.12 S, 167.95 E) is an uninhabited island (highest point 260 m a.s.l.) of volcanic origin near Norfolk Island, between Sydney and Fiji. The basaltic tuffs and lavas of Miocene age were covered originally by impenetrable subtropical and vine- entangled pine, oak, and palm rain forest, with coarse native grass (Elymus) and Cyperus reeds. The great depth of the original soil was described in 1794 when it was completely riddled with nesting bird burrows. Soil parent material is thick, crumbly, reddish tuff and layered basaltic lava. Pigs were introduced in 1792–1793, and although the historical record is incomplete, their “rooting” of the seabird burrows was a significant disturbance to the tuffaceous soil surface, and the disturbed and erosion-prone parent material started to erode soon thereafter. With subsequent goat and rabbit introductions (probably around 1830), the island suffered sustained degradation of its plant cover. First, the ridges were stripped bare of vegetation and less palatable and thorny plants came to dominate. Within 25–65 years, the island was largely barren, with no grass, only scattered trees and a single stand of woody vegetation. By 1856, the pigs had died out, as did the goats by 1900, presumably because of competitive exclusion. Rabbits persisted for nearly 90 more years, preventing vegetation regeneration until they were eradicated in 1988. The first photograph of the island taken in 1906 shows it was generally barren, but paintings suggest it may have been mostly bare by as early as 1850. The 1906 photographs show that erosion was advanced and the roots of the few scattered trees and shrubs were exposed by two meters of soil loss. By 1960, the island no longer supported plant growth. Using erosion markers, annual soil loss rates in 1979–1980 varied from 20 mm on basaltic parent material to 62 mm on tuff. The consequences of free-ranging rabbits to vegetation were identified by comparisons with rabbit-free exclosures (Coyne, 2010). Immediately following the first introduction of Myxoma virus, seedling survival increased and plant regeneration became visible. Poisoning, gassing, trapping, and shooting were used to finish the job of eradication. Photo-point monitoring and vegetation mapping in 1977 (pre-eradication) and 2007 (post-eradication) documented the dramatic increase in vegetation cover, a 41% increase in native and introduced plant species, and the increased stature of the white oaks.

9.4.1.3.3 Carnac Island Carnac Island (32.12 S; 115.66 E) is a small (16 ha), uninhabited, low, exposed, and windswept island eight kilometers off Fremantle in south Western Australia. Without 9.4 Consequences of the evolution of ever-growing teeth 307

significant anthropogenic disturbance, non-volcanic Carnac Island supports low vegetation no taller than a meter. The island is one of very few among the 8300 islands along the Australian coast that has a long history of botanical observation. Regularly studied since 1951, the first vegetation map was made in 1957, and the vegetation was studied in 1975–1976 and in 1995. Rabbits were first introduced sometime before 1827 and were present for seventy years until 1897, shortly after cats were introduced. They were not observed again until 1965 and this second known introduction was eradicated in 1969 (Abbott et al., 2000). The extinction rate of annual plant species was greatest in the period coinciding with the occupation of the rabbit. In particular, the rabbits denuded the grassy vegetation (Abbott, 1980). Aerial photographs taken in January 1965, December 1972, February 1984, and January 1995 captured vegetation change associated with the “second” eradication event and subsequent decrease in the area of bare soil by infilling vegetation (Abbott et al., 2000). Two years after rabbit eradication, the vegetation was dense although plant species richness was diminished. There are no direct observations of change in rates of erosion or soil loss associated with the rabbit introductions and eradication.

9.4.1.3.4 Whale Island (Moutohora) Moutohora (or Whale Island) in the Bay of Plenty, New Zealand (37.85 S, 176.98 E) is a complex but dormant volcanic cone (143 ha or 240 ha, highest point 348 m a.s.l.). Feral goats were introduced in the nineteenth century, and by the late 1950s, goats had devastated the vegetation. Subsequent to eliminating human-induced ﬁres and ending sheep grazing (highest intensity between 1938–1943), goat eradication was undertaken starting in 1964 and completed in 1977. Nine years prior to goat eradication, rabbits were introduced to Moutohora in about 1968, and reached a density of 375/ha by early 1973 (Pedersen and Roche, 1973). Vegetation maps made in 1971, 1985, 2000, and 2002 document the process whereby large parts of the island were kept open by goats and rabbits until their eradication. The 1971 map documents vegetation prior to goat eradication and shortly after rabbit introduction, and the 1985 map shows vegetation after goat eradication but before rabbit eradication. For the 10-year period between 1977 (goat eradication) and 1987 (rabbit eradication), rabbits persisted alone on the island. Rabbits were observed to have grazed the 40-cm- high native grassland to a low turf and denuding extensive areas (permitting Kunzea shrub regeneration), and to otherwise hinder the regrowth of native plants. In an effort to enhance petrel breeding by denying fast-breeding Norway rats their dietary supplement of rabbits, rabbits were eradicated by poison in operations beginning in 1980 and culminating between 1985–1987. Following goat and rabbit eradication, coastal broadleaf Pohutukawa (Metrosideros) forest began to emerge (Ogle, 1990; Imber et al., 2000).

9.4.1.3.5 Île Saint-Paul Île Saint-Paul or Saint Paul Island, French Southern Territories, Indian Ocean (38.72 S; 77.53 E) (6–7km2, highest point 272 or 284 m.a. s.l.) is the top of an active volcano that last erupted in 1793. Located at middle latitudes in the Indian Ocean, Saint Paul is 308 Ever-growing teeth

85 km SW of Amsterdam Island and 3000 km south of Reunion, and has a cool temperate-subtropical oceanic climate. Saint Paul is an older tuff cone surmounted by a basaltic stratovolcano with a 1.8 km wide caldera, the subaerial part of the mostly submarine Amsterdam–St Paul Plateau or “hot-spot” with distinctive andesitic volcanism (Gunn et al., 1975). Rocky with steep cliffs on the east side, part of the crater rim collapsed in 1780, admitting the sea. The island was originally covered by tall coarse grass (original Phylica nitida forest?), ferns, and moss (Dahl, 1986–2004). European rabbits (Oryctolagus cuniculus), pigs (Sus scrofa), and goats were introduced in the nineteenth century or earlier, and cattle in 1871. Pigs and goats (Capra aegagrus) disappeared or were eradicated, and the rabbit was eradicated in 1996 along with the ship rat (Rattus rattus) (Micol and Jouventin, 2002). Detailed observations about the consequences of the rabbit introduction and eradication is still lacking.

9.4.1.3.6 Kerguelen Islands The Kerguelen archipelago, in the sub-Antarctic of the South Indian Ocean (48.42–50 S; 68.45–70.58 E) is more than 3500 km from the African and Australian coasts. Comprised of Tertiary flood basalts and plutonic rocks, the most recent volcanic activity occurred in the Holocene. Rabbits, domestic sheep, reindeer, and mouflon (Ovis musimon) have been introduced into the archipelago. Rabbits (Oryctolagus cuniculus) were introduced to the main island (6500 km2) in 1874, and nine other islands of the archipelago thereafter. With these introductions, soil erosion increased, sensitive native plant species disappeared by grazing and burrowing activity, and dominance shifted to nearly mono-specific Acaena magellanica. Myxoma virus was introduced into the archipelago in 1955–1956 (to which the rabbits soon developed resistance), and rabbits were eradicated on two islands in the Golfe du Morbihan starting in 1991, on Ile Verte (148 ha, 47 m a.s.l.) in 1992, and Ile Guillou (145 ha, 165 m a.s.l.) in 1994. On these two islands, rabbits were the only mammalian herbivore and their density was 9/ha. Detailed soil sampling (distinguishing mineral, thick and thin organomineral, organic and peat soils, scree on steep slopes, and halophilous mineral soil of the coast) and an exhaustive vegetation survey of the vascular flora (including windward and lee slopes, bare ground, and total plant cover) were made prior to eradication. These observations were repeated five to six years after eradication and compared to pre-eradication conditions. The results are complex, and while there are differences before and after eradication, the differences are relatively slight (Chapuis et al., 2001, 2004), probably reflecting the slower timescale of recovery at this latitude.

9.4.1.3.7 Macquarie Island The largest island ever targeted for rabbit eradication, Macquarie, sub-Antarctic (54.5 S; 158.95 E), is a low volcanic ridge-crest oceanic island (12 800 ha, 433 m.a.s.l.) at the conﬂuence of the Paciﬁc and Australian plates, with cool but rigorous sub-Antarctic maritime climate (920 mm MAP, MAT 3.8 C, 312 rain days/year, mean windspeed 18 knots, 89% relative humidity). Macquarie Island does not support trees or shrubs; instead, the island is covered in tundra-like vegetation of tussock grasses, megaherbs, 9.4 Consequences of the evolution of ever-growing teeth 309

and bryophytes. European rabbits (Oryctolagus cuniculus) were introduced in 1878 to the cat-occupied island. Extensive grazing was observed in the early 1950s (Taylor, 1955) and there was a catastrophic decline in grasslands by 1960 (Costin and Moore, 1960). Rabbit populations peaked in 1978 when Myxoma virus was released and the population plummeted. Following the virus release, vegetation recovered substantially within 10 years, including an increase in tall tussock grasslands and a decrease in herbfields (Copson and Whinam, 1998). Annual releases of the virus continued until 2006, although reduced efficacy was observed. Cats were placed under eradication in 1985 and the last individual was killed in 2000. After cat eradication and despite continued Myxoma virus spreading, rabbit numbers increased again, and in five years, large areas of the island were altered (Springer, 2006). Vegetation change between 2000 and 2007 was described using field plots and before versus after comparisons of satellite image pixel spectral reflectance and chlorophyll loss and gain by NDVI (normalized difference vegetation index) subtraction (Bergstrom et al., 2009a). There was substantial rabbit-induced island-wide change in vegetation following cat eradication, including but not limited to change in NDVI values indicating replacement of vegetation by bare ground. Considerable changes in vegetation and erosion are attributed to rabbits during the 27-year period between 1980 and 2007. During this interval, their population size declined from its peak of 150 000 in 1978 to 20 000 in 1985, then rebounded again to between 108 000 and 150 000 in the late 1990s after cats were eradicated (Scott and Kirkpatrick, 2008). Rainstorm- and seismic-induced landslip erosion is a natural form of erosion of the peat-soil coastal slopes. Rabbit grazing intensity influences vegetation recovery and succession on the landslip scars. With no rabbit grazing, a tall tussock grassland develops; with light grazing, a mixed herb field replaces the grassland; and with heavy grazing, a short grassland develops. Evidence of grazing includes the presence of scat, chewed leaves, and soil diggings. Although there was no evidence of an increase in bare ground with increasing grazing intensity, circumstantial evidence strongly suggests that grazing and digging cause an increase in erosion on the coastal slopes (Scott and Kirkpatrick, 2008).

9.4.2 The fossil record of rabbits

Thus, we know something about the recent impact of rabbits in Australia, New Zealand, and on diverse islands around the world, but what about fossil record of all the other invasions by evolutionarily derived fully elodont rabbits? Elodont crown lagomorphs (Leporidae þ Ochotonidae) share rootless adult teeth with crescentic valleys rapidly obliterated by wear, persistent hypostriae, and reduced third molars. The two clades are distinguished by the form of the shaft of the maxillary ever- growing molars (curved into the zygoma in Ochotonidae, straight into the orbit in Leporidae). True Leporidae (with ever-growing molars) ﬁrst appear in North America (Palaeolagus) in the latest Eocene (37–38 Ma), and Ochotonidae in Asia (Sinolagomys) in the Oligocene (about 30 Ma). This geographic distinction implies that complete elodonty may have been acquired independently in North America and Asia. 310 Ever-growing teeth

The first appearance of Leporidae in North America occurs in the Uintan 2 (late Uintan NALMA) with Procaprolagus Gureev, 1960 in the Swift Current Creek fauna of southwest Saskatchewan, Canada (Storer, 1984), and has a first appearance age of 44.75 Ma (Krishtalka et al., 1987). The leporid Procaprolagus is hypsodont (but not fully elodont) and the family immigrated into North America from Asia. Thus, the acquisition of hypsodonty occurred first in Asia, then full elodonty evolved later in North America and again independently in Asia. McKenna and Bell (1997) list Mytonolagus (Uintan2), Megalagus (Chadronian1), and Procaprolagus (Uintan2) in North America, and list Shamolagus as questionable in the early Eocene of Asia, but the family is definitely present in the middle Eocene of Asia, with Gobiolagus, Lushilagus, and Strenulagus. Following their initial immigration into North America during the Uintan–Duchesnean transition, the first appearances of crown Leporidae in the Chadronian and throughout the Oligocene are the result of in situ evolution in North America (Emry, 1992). The Uintan through Whitneyan interval was a period of isolation of the North American continent with little faunal exchange with either Europe or Asia (Prothero and Swisher, 1992). Therefore, the clades that evolved elodonty were native clades and the transition occurred in residence in North America. The Chadronian, and the following Orellan and Whitneyan NALMA ages were based on faunal composition changes coincident with lithostratigraphic divisions of the White River Group. While the bulk of the White River Group is eolian and volcaniclastic, there is a positive correlation between the amount of volcanic ash and the relative amount of eolian deposits. In South Dakota, the Chadron Formation changes from predominantly fluvial floodplain deposits to principally eolian deposits moving south- westward into central Wyoming. This change also occurs vertically, from the Chadron Formation upward through the Poleslide Member of the Brule Formation in South Dakota. Additionally, there is progressively more ash in less weathered condition from NE to SW, and similarly upward from Chadronian through Whitneyan deposits. Thus, following the arrival of Leporidae in the late Eocene, full elodonty evolved independently in North America, coincident with the shift in depositional environment from fluvial to dominantly eolian and pyroclastic. Thereafter, the fossil record of fully elodont lagomorphs documents many invasion events and the waxing and waning of rabbit diversity. There were invasions of small islands (Table 9.3) and large continents (Table 9. 4). Associated with any of these invasion events, is there evidence of rabbit-induced accelerations of erosion anywhere in the complex biogeographic history of the fully elodont crown clades Leporidae and Ochotonidae? There have been many notable invasions of fully elodont Lagomorpha onto islands both large and small (Table 9.3). The impact of these invasions is not known. In some of the intercontinental invasions (Table 9.4), there was a long lag time between first appearance and subsequent proliferation, and the record includes some impressive bursts of explosive diversification. For example, in Europe, lagomorphs arrived at 33 Ma, but eight million years elapsed before they diversified at about 25 Ma. Leporidae first arrived in Europe about 13 Ma, but are extremely rare until about 7 Ma. Ocotona arrived into North America about 6 Ma but was rare until 2 Ma. In these cases, 9.4 Consequences of the evolution of ever-growing teeth 311

Table 9.3 Notable invasions of fully elodont Lagomorpha onto large and small islands where impacts on vegetation, land degradation, and soil erosion are unknown

Island Age range

Prolagus sardus 1 Corsica, Sardinia ? to ca 300 yr BP Pentalagus furnessi 2 Ryukyus ? to extant today Hypolagus peregrines 3 Sicily Until the Pleistocene Nuralagus rex (¼Alilepus) 4 Minorca Messinian through much of Pliocene Hypolagus balearicus 5 Mallorca, Eivissa Messinian to early Pliocene Gymnesicolagus gelaberti 6 Mallorca Middle to late Miocene Lepus brachyurus Honshu (Japan) >0.5–0.6 to ? Lepus timidus ainu Hokkaido (Japan) >0.5–0.6 to ?

1 Vigne, 1992. 2 Yamada and Cervantes, 2005. 3 Marra, 2013. 4 Pons-Moyà et al., 1981; Quintana et al., 2011. 5 Quintana et al., 2010. 6 Mein and Adrover, 1982.

Table 9.4 Intercontinental invasion events by crown lagomorphs (Leporidae, Ochotonidae) with fully elodont cheek teeth

To From Group/taxon Age (Ma)

Europe Asia Amphilagus (Ochotonidae) 25 North America ? Oreolagus (Ochotonidae) 18–20 Africa ? (Ochotonidae) Australolagomys 18 India ? Ochotonidae indet 18 NW Africa Europe Prolagus 6 North America Asia Ochotona 7 Europe ? Ochotona 4 Eurasia North America Hypolagus (Archaeolaginae) 6 Europe North America Alilepus(Leporinae) 7 (may be earlier) Europe ? Leporidae indet 13

immigration was not followed by rapid geographic spread or conspicuous evolutionary success (as we understand these things in the fossil record). The most important explosive radiation occurred among Leporidae in the Pliocene, when more than 16 genera appeared in four continents, including seven genera of Leporinae. The radiation of species of Hypolagus (Archaeolaginae) sometime in the middle Miocene to Pliocene (15–2 Ma) is another example of rapid diversification. Rabbit taxon proliferation accelerated in the Pliocene (Table 9.5). Increased sedimentation rates of the last 4 myr have been attributed to the influence of climate change on erosion rates (Peizhen et al., 2001), not the spread and proliferation of elodont lagomorphs. Why is the possible role of elodont lagomorph invasions, proliferations, and diversifications ignored as a potential engine of erosion? 312 Ever-growing teeth

Table 9.5 Accumulating diversity of crown lagomorph genera (Ochotonidae and Leporidae) through time in North America, Europe, Asia, and Africa (in 2 myr intervals) (From Lopez-Martinez, 2008.)

Time intervals (myr) North America Europe Asia Africa Total

0–2444416 2–41177328 4–6635216 6–8241310 8–10 3 1 1 0 5 10–12 3 1 2 0 6 12–14 4 4 3 0 11 14–16 2 2 2 1 7 16–18 0 3 2 1 6 18–20 1 2 0 1 4 20–22 2 4 2 8 22–24 2 3 2 7 24–26 2 1 2 5 26–28 2 2 4 30–32 1 1 32–34 3 3 34–36 1 1 36–38 1 1

9.4.3 Rabbit-like notoungulates in South America

Ever-growing teeth are found across a great body size spectrum within and between clades of South American native mammals. For example, complete elodonty is found in smallish sloths in the Deseadan SALMA, living tree sloths, giant Pleistocene ground sloths, and between clades of persistently small pachyrukhine typotherians and persistently large toxodontine toxodontids. However, is there a common body size when elodonty first evolves, and does subsequent diversification in elodont clades trend toward larger or smaller body size? Reguero et al. (2010) examined these body size patterns among rodent- and rabbit-like typotherians, and found no evidence of body size trends subsequent to the first appearance of high-crowned teeth. While large body size was attained in some elodont clades (sloths, glyptodonts, and toxodonts), small body size was maintained in others (pachyrukhine hegetotheriids, interatheriid typotherians, and most caviomorph clades, with only a few exceptional examples among the largest eumegamyines and hydrochoerines). The oldest fossil record of fully elodont herbivorous mammals in South America is when sloths, glyptodonts, and armadillos first appear in the fossil record already fully elodont. The evolutionary relationship between elodonty and the basal radiation of xenarthrans, and the timing of their loss of enamel, is unknown (although there is suggestive evidence that elodonty evolved prior to the loss of enamel, at least in armadillos). The environmental impact of elodont xenarthrans is difficult to judge, but may have been significant, given the prevalence of armadillos and glyptodonts in Deseadan and younger faunas. 9.5 Environmental impact of ever-growing teeth in South America 313

There is a general increase in the proportion of elodont taxa in South American faunas over time (Table 9.1). In Central Patagonia, the proportion of elodont taxa increased from 14% in the Barrancan SALMA at about 40 Ma, and stayed relatively low (varying between 15% and 32%) through the Colhuehuapian SALMA at about 21 Ma. High levels of prevalence near or above 50% were reached only near the Southern Andes in Western Patagonia, beginning in the “Pinturan” (at about 19 Ma), reaching 55% in the Colloncuran SALMA at about 16 Ma, and stayed high (67%) through the Mayoan SALMA at about 12 Ma. In northwestern Argentina, the proportion of elodont taxa was very low in the Lumbrera Formation (>39.9 Ma), but increased to 33% by 35 Ma at Antofagasta de la Sierra. This prevalence increased to over 50% by 15.3 Ma. In the Central Andes of Bolivia, the proportion of elodont taxa went from 36% to 86% between 27.0 Ma and about 16.5 Ma (reaching over 50% sometime between 21.7 and 17.5 Ma), and stayed between 50% and 85% all the way into the middle Pliocene. The highest level of faunal elodonty (86%) recorded in South America is at about 16.5 Ma at Cerdas, in the Bolivian Altiplano. In the equatorial lowlands of Colombia, during the Laventan SALMA, the proportion of elodont taxa ranged between 34% and 45%. At about the same time in the Andes of southern Ecuador, despite the inadequate samples, higher proportions (50%–75%) prevailed at about the same time, between 14.7 Ma and 11.4 Ma. The highest levels of faunal elodonty occur in Andean faunas, and faunas reached 50% at about 19 Ma in the Southern Andes, 15.3 Ma in the Andes of northwest Argentina (the Puna), sometime between 21.7 Ma and 17.5 Ma in the Altiplano, and are known to have attained this level of prevalence in the equatorial Andes by at least 14.7 Ma. These are very high levels of prevalence.

9.5 Environmental impact of ever-growing teeth in South America

Of the deleterious impacts of elodont and other high-crowned herbivorous rodents in South America, Jackson (1988) mentions that (1) small phyllotines damage soils, range, and pastures through seed predation; (2) Ctenomys reduces forage, degrades habitat, and reduces food available to sheep; (3) the chinchillid Lagostomus maximus competes for range forage with livestock; and (4) the caviids Cavia aperea, Galea, and Microcavia damage crops and strip ground cover in dry zones. If one elodont taxon like the rabbit can wreak havoc, what could many of these seductive engines of erosion do? If the rabbit does its best work clearing plant cover, causing land degradation and acceleration of erosion on small islands, what could many of these elodont engines do to an isolated valley or an isolated peak in the Andes? If the impact of rabbits is felt even stronger on aridlands, what would be the impact of many elodont engines of erosion on the dry valleys and dry slopes of the Andes? Recent introductions of rabbits into South America document multiple consequences, including: (1) devastating effects on local biodiversity, both domestic and wild (Jaksic, 1998; Holmgren et al., 2006; Novillo and Ojeda, 2008); (2) competing for food with 314 Ever-growing teeth

other herbivores (Bonino and Amaya, 1984; Jackson, 1988); (3) contributing to the deleterious effects of overgrazing by denuding herbaceous ground cover (Jackson, 1988; Moreno et al., 1996); and (4) accelerating erosion through excavation (Butler, 1995). Four individuals of Oryctolagus cuniculus were introduced onto Tierra del Fuego in 1936, and by 1953 had attained a population of 30 million (Jaksic and Yáñez, 1983). Despite this irruption on Tierra del Fuego, there is little published record of impacts on soil erosion (Silva and Saavedra, 2008). In South America, there are several potentially informative examples of rodent and rabbit introductions into a naïve continent. When you consider the impact of rabbits elsewhere, it helps you imagine what the introduction of caviomorph rodents might have meant in the middle Cenozoic when they appear in the Andes of Chile and Patagonia, about 31 million years ago. By about 26 Ma, in Bolivia caviomorphs had evolved high-crowned molars (Patterson and Wood, 1982), and by 24 Ma, ever- growing cheek teeth in Patagonia (Wood and Patterson, 1959). Subsequently and long after the caviomorph introduction, South America was invaded by another important group of rodents, sigmodontine Muridae, sometime before about six million years ago (Verzi and Montalvo, 2008). While sigmodontines never evolved ever-growing cheek teeth, high-crowned molars probably evolved fairly rapidly, as judged by estimated divergence times for Reithrodon (Steppan, 1995; Steppan et al., 2004). More recently, during the Great American Biotic Interchange, the fully elodont lagomorph Sylvilagus and the rodent family Sciuridae invaded northern and central South America, but did not advance very far. In addition to these four immigration events, there have been several important introductions by humans, including the European hare (Lepus europaeus)in 1888 and rabbit (Oryctolagus cuniculus) in the early twentieth century, both introduced into southern South America (Grigera and Rapoport, 1983; Jaksic and Fuentes, 1991). Finally, the beaver (Castor canadensis) was introduced into Tierra del Fuego in 1946 (Lizarralde et al., 2004). How might we detect and describe the influence of these invasions on the pre-existing fauna, and in particular, any influence on rates of erosion? There does not seem to be wholesale extinctions among contemporaneous small- bodied and high-crowned typotherians, like interatheres and hegetotheres, following the arrival of caviomorphs into South America or following their subsequent evolution of elodont molars. As a matter of fact, precisely these groups of typotherians increase in diversity in Deseadan and later faunas along with the evolution of elodonty in caviomorphs (Reguero and Prevosti, 2010). What the combination of an increase in elodonty by rodent immigration events plus in situ diversification of elodont native notoungulates and other herbivores might imply for erosion rates is easier to imagine than reconstruct from the record of sedimentation. The evolution of elodonty and its accumulation in South American faunas through the Cenozoic does not seem to have left any discernable trace and there is no practical way yet devised to render their presence and accumulation in the sedimentary record of erosion. The trend of increasing elodonty during the Neogene, and the prevalence of elodonty in the modern South American fauna (Figure 9.1) seem to be a unique feature of South American herbivore evolution. Why? I suspect it evolves in response to high mineral particle ingestion in the mountainous, volcanically active, and rapidly eroding Andes, 9.6 The Vicugna 315

where elodont mammals accumulate through the Cenozoic. The relationship of elodonty with the Andes explains why there are so many elodont typotherian notoungulates, rodents, and xenarthrans in Miocene and younger faunas in western Patagonia, northwestern Argentina, Bolivia, and Ecuador, and why there are so few or no hegetotheres or mesotheres in Miocene faunas in lowland Ecuador, Colombia, Venezuela, and Brazil. What is the scale and magnitude of contemporaneous erosion in South America? The Andes is a long mountain range that extends all along the western Pacific margin at all latitudes, and through its eroding mineral products, exerts an influence that extends from the foothills out onto the eastern plain. The range was characterized by high relief and fairly extensive topographic complexity long before modern elevations were attained. The temporal variation in estimates of uplift rates is a reflection of both the long period of active orogeny and the amount of topographic relief it generated. Throughout the process of uplift, Andean South America became one huge sediment source area. In the case of the Andes, aligned N–S across different climate zones, prolonged mountain building created a continuous source of sediment that was distributed by zonally distinct and slope-dominant routing systems. The sub-Andean megafans at the eastern foot of the Andes are one manifestation of this (Wilkinson et al., 2010; Latrubesse et al., 2012), the thick sediment isopach of the western Amazon basins (Latrubesse et al., 2007) are another, as are the broad deposits of windblown sediment on the Pampas and the widespread Neotropical loess (Iriondo, 1997) found extensively throughout South America. What is it about Andean environments that stimulates the evolution of elodonty?

9.6 The Vicugna

The Vicugna (Camelidae, Artiodactyla) is among the very few living ungulates to have evolved ever-growing incisors. One of the protected areas where Vicugna occur today is the Laguna Blanca Vicugna Reserve in Catamarca Province, NW Argentina. The Laguna Blanca Reserve is located along an eolian dust path extending across the Andes in the hyper-arid latitude belt around 30 S latitude, where annual dust storm frequency is highest. In what follows, I discuss issues related to the estimation and measurement of: (1) soil ingestion, (2) soil load, (3) soil erosion, and (4) tooth wear in the herbivores inhabiting the dust path, as might be used on other oceanic or orographic islands. The Vicugna, a native Amerian camel, is endemic to the sparse arid and semiarid grasslands in the Central Andean Volcanic Zone at elevations from 3500 m to 5800 m in southern Peru, Bolivia, NW Argentina, and N Chile. The Vicugna is the only camel to evolve ever-growing incisors. The explanation for this is assumed to involve their diet and features of their environment. There are 44 active volcanoes in the area of the Vicugna’s distribution. In addition to these active sources of volcanic ash, there are over a thousand volcanic centers of late Cenozoic age in the same area, along with accumulations of the pyroclastic products of their long eruption history. 316 Ever-growing teeth

9.6.1 The Laguna Blanca Reserve

The UNESCO Laguna Blanca Biosphere Reserve (25.5– 27 S; 66.4–67.33 W) is a 973 000 ha protected area in the middle of the Andean Puna in NW Argentina. The nearest meteorological stations would be at Antofagasta de la Sierra, and the climate at Laguna Blanca is described as “severe,” with a great daily range of temperature, and frequent frosts. Rainfall is scarce (MAP between 100 mm and 250 mm) and falls from December to March. Strong and dry winds are frequent. Vegetation in the Reserve is mainly xerophilous steppe with a large proportion of bare soil. Borgnia et al. (2006) distinguish six habitat types in the Reserve: (1) grass steppe, (2) shrub steppe, (3) mixed steppe, (4) vega, (5) salt marsh, and (6) peladares. Among these, three types of shrub steppe vegetation are distinguished, based on the dominant shrub: (2a) Rica-rical (Acantholippia sp.), (2b) tolillal alto (Fabiana densa), and (2c) tolillar bajo (Fabiana spp.). In addition, three types of grassland steppe were distinguished: (1a) Stipa spp., (1b) Festuca spp., and (1c) Panicum chloroleucum steppe. Rabinovics et al. (1991) estimated carrying capacity of 7.6–7.9 vicuña/km2 in the Laguna Blanca Reserve. During daylight and most of the day, Vicugna forage on vega, the marshy area around Laguna Blanca, but they are observed to exploit only the margins of these areas, as domestic lifestock also feed preferentially on vega. Tolar (the shrub steppe on slopes) is the other preferred vegetation. Vicugna are observed mostly in the tolar of the mountainous foothills in the early morning and late in the afternoon, and they overnight in tolar. Vicugna are rarely observed in “peladar” (bare areas).

9.6.2 Dust sources and surface processes in the Puna

The relief of the Laguna Blanca Reserve reveals an asymmetry between windward and leeward slopes. The asymmetry is explained by the west to east prevailing wind and the accumulation of ﬁne-grained sediment on the leeward slope, and denudation on the windward slope. In addition to windblown loess in the Laguna Blanca Reserve, there is evidence of massive rock slope failure triggered by seismicity. These are the two dominant forms of erosion. A recent panoramic view of the NW Argentine dust path taken from earth orbit looking east from the crest of the Andes was posted at NASA Earth Observatory on May 17, 2010 and was acquired on April 26, 2010 by the International Space Station (ISS023-E-28353_lrg.jpg) when it was directly over the Atacama Desert. The high plains of the Puna appear in the foreground with a line of young volcanoes. Salt lakes occupy the basins between major thrust faults. Salar de Arizaro appears in the foreground. Salinas Grandes appear faintly in the middle distance and the Llanos de la Rioja on the far right [http://earthobservatory.nasa.gov/IOTD/view.php?id=43961]. Using the correlation between latitudinal variation in εNd in loess and Andean volcanic rocks, Smith et al. (2003) proposed west to east transport as the source of Argentine loess and suggested two possibilities for the mechanism: (1) northward (south to north) movement of Polar Front leading to increased intensity and frequency 9.6 The Vicugna 317

of westerly winds farther north than their modern limit, or (2) modern north-westerly (west to east) winds blowing downslope from the Altiplano, enhanced by glaciation and augmented by the subtropical jetstream. An example of a south to north dust storm was captured on July 25, 2011 by satellite over San Juan, Argentina [http://earthobservatory.nasa.gov/NaturalHazards/view.php? id=51467]. In this image, the Sierra Pie de Palo and the Sierra de la Huerta emerge above the relatively low-lying dust plumes and appear on the image. The dust appears to blow northward and concentrate along the slopes of the Andean foothills to the northwest. The dust sources are not easily discerned, but some appears to blow northward from the Pampa de la Salina (31.96 S; 66.7 W) or Pampa de las Salinas. The image extends northward to about 29 S to La Rioja, and in the NE corner of the image appears the Llanos de la Rioja. Other images of dust storms in this region include those of July 7, 2010 [http:// earthobservatory.nasa.gov/NaturalHazards/view.php?id=44581] and August 16, 2009 at Mar Chiquita [http://earthobservatory.nasa.gov/NaturalHazards/view.php?id=39827], an important dust source in northeastern Córdoba Province. An example of a west to east blowing dust storm deﬂating surfaces in the vicinity of the Salar de Antofalla on September 2, 1985 was captured by Shuttle mission [STS51I- 46–71 and 72]. Local dust source areas in the immediate vicinity of the Salar de Antofalla include middle Tertiary sediments. Another example of a west to east blowing dust storm off surfaces just east of the Salar de Arizaro was captured by an undated image from 1983 [STS008–46–933]. The point dust source areas are mostly east of the Salar de Arizaro, but there are more distant source areas that may be particular volcanic ediﬁces.

9.6.3 Mineral particle consumption

The quantity of mineral particles consumed by grazing herbivores can be measured by the acid-insoluble fraction of fecal DM (AIRf). AIRf levels above about 30% in sheep on the North Island of New Zealand result in excess tooth wear rates of about 1–1.8 mm of incisor crown height over six weeks and this season of peak tooth wear lasts 18 weeks or about four months. Individual sheep body mass ranges between 42 kg and 75 kg, and an individual can consume between 1.55 kg and 2.5 kg of plant DM each day (Avondo and Lutri, 2004). Assuming a digestibility of 60%, between 0.62 kg/d and 1.0 kg/d becomes fecal DM. If AIRf is pure plant silica (and no contaminant soil), a level of 30% AIRf implies that between 0.186 kg and 0.3 kg of plant silica is ingested daily. This represents 12% of the plant DM consumed. Twelve percent is an extraordinarily high percentage, given that grass DM is known to have a mean concentration of solid silica of about 0.739%, or less than 1% (Hodson et al., 2005). A daily consumption of between 1.55 kg/d and 2.5 kg/d of plant DM by an individual sheep implies only 7.75 kg to 12.5 kg fresh grass leaves each day (at 80% water content). Daily consumption of between 1.55 kg and 2.5 kg DM in grass leaves and stems, at a solid silica concentration of 0.739%, implies 0.0115 kg to 0.0185 kg of 318 Ever-growing teeth

phytoliths. At the mean concentration of silica in grasses (0.739%), a value of 30% AIRf would imply daily grass DM consumption of between 62.5 kg and 103 kg, or nearly one and a half times their body mass daily. And this is dry matter! What would be the daily consumption of grass if the water content of the leaves was 80%? Much more than an individual sheep could consume. Clearly, not all the AIRf that is known to drive excess tooth wear in New Zealand can be pure plant silica. While AIRf varies seasonally along with tooth wear rates, the acid- insoluble residue of pasture grasses (AIRp) remains relatively constant. Assuming that all ingested soil is being consumed off the surface of leaves, what does a level of 30% AIRf imply for the soil load on plants? To answer this, speciﬁc leaf area (SLA) is usually measured relative to DM. In a sample of 143 grass species, SLA (the ratio of leaf area to dry mass) varied from 22 m2/kg to 24 m2/kg DM (Garnier et al., 2001; Vile et al., 2005). Assuming an SLA of 23 m2/kg DM, a daily consumption of 1.55 kg to 2.5 kg of plant DM implies from 36 m2 to 58 m2 of leaf area. How do you convert this to soil load on leaf surfaces? Interestingly, given the distribution of solid silica particles in the grass leaf, what does this imply in terms of the comminution required to reduce this total area to particles that would pass through the anatomical gateways of the sheep (or Vicugna) gut? Soil load is usually measured as mass loading in grams of soil per kilogram of DM, rather than in relation to leaf surface area. Observed soil mass loadings in the literature range from 1 gm/kg to 500 gm/kg DM and has been measured in diverse settings using a variety of methods (most indirect). Soil mass loadings between 4 gm/kg and 190 gm/ kg DM have been reported for sheep in grazing systems. The upper limit of ingested soil off leaf surfaces in sheep grazing systems (0.190 kg) is very close to what would be estimated from 30% AIRf in New Zealand. The total daily intake of mineral abrasives (in gm/d), both intrinsic to plant tissues (phytoliths) and extrinsic (soil) in a variety of ungulate grazing systems, are quite variable, but the value of 30% AIRf implies that between 0.186 kg and 0.3 kg (or 186 gm to 300 gm) of soil mineral particles are ingested daily. To sustain a total mineral particle ingestion rate of 30% AIRf for four months in an experimental setting would require the administration of between 0.186 kg and 0.3 kg of soil mineral particles daily to each animal, depending on body weight. A sustained rate of soil ingestion for four months (120 days) of between 22.3 kg and 36 kg of volcanic ash or eolian dust for each individual animal implies a lot of ash.

9.6.4 A protocol for the ﬁeld study of tooth wear in the Vicugna

If one were to endeavor to study the relationship of earth surface processes, soil ingestion, and tooth wear in living Vicugna, the following recommendations might be helpful.

9.6.4.1 Sample the plants for soil load Sample, measure, and characterize the leaf surface area of the puna grasses and other forage plants in the Laguna Blanca Reserve. A quick grab sample would tell you something about the mineral composition of trapped soil. Are there published 9.6 The Vicugna 319

descriptions of the soils? Using mass loadings, calculate the number of soil mineral particles per unit area of leaf? Using the area of ingested leaves consumed daily, calculate a soil load from the total surface area of ingested plant DM. How does the amount of soil mass loading, if distributed evenly over the upper or adaxial surface, relate to particle count, and how does the soil particle count compare to the particle count of phytoliths?

9.6.4.2 Sample the plants and soil for phytoliths While Vicugna at Laguna Blanca use a wide range of plant species (39 of 75 available plant species), 59%–72% of their consumption is grasses, whereas shrubs comprise only 16%–19%. A steppe grass Panicum chloroleucum and a marsh “grass-like” plant Distichlis spp. represent nearly 50% of the diet. The botanical composition of the diet of Laguna Blanca Vicugna was determined by microhistology of fresh fecal material that was ﬁrst cleaned, ground, and sieved. Samples of the aerial parts of plants usually consumed by Vicugna were also collected, cleaned, ground, and screened prior to analysis (Borgnia et al., 2010). Note that in this study, both samples were washed and cleaned to remove “dirt.” They were then ashed, but not for phytoliths. In determining the number or concentration of phytoliths in puna grass and other plants in the diet, ﬁnd the number of phytoliths per mm2 (the unit of thickness of enamel) of leaf epidermis.

9.6.4.3 Sample Vicugna fecal material for AIRf Other domestic herbivores coexist with Vicugna in the Reserve. How do you distinguish Vicugna droppings from those of other domestic herbivores? Goats and sheep feed in mixed herds, so their fecal material is impossible to distinguish. However, unlike these ruminants, llamas and Vicugna leave droppings in concentrations. Thus, how are Vicugna droppings distinguished from those of the llama? Size? Once you work this out, collect the freshest turds (with minimum windblown dust coating) from the dung pile. Then, after carefully removing the surface contaminant, from the interior of the turd, distinguish and separate free mineral particles from mineral particles still embedded within and intrinsic to leaf epidermis.

9.6.4.4 Sample Vicugna jaw bones and teeth for tooth wear In the ﬁeld, photograph the jaw bones and teeth, measure them, sample the calculus, and obtain a mold of the occluding surface. Be prepared to clean and mold these in situ, rather than “export” them to the laboratory.

9.6.4.5 Measure the area of exposed soil Exposure can be estimated from plots or photographs using “charts for estimating the percentage of mottles and coarse fragments” from the FAO (2006), or by measuring the surface actually exposed on many small plots. Bare ground is extremely variable over short distances and within short time-spans. Surface soil (sediment) should be sampled from among the point source areas and at three different sites along the W to E gradient of the loess dust path. The sites along the 320 Ever-growing teeth

dust path might include: (1) down in the lowlands where dust storms deﬂate off the dry lake beds, (2) at the Laguna Blanca Vicugna Reserve, and (3) at the source volcanoes and ﬁne-grained volcaniclastic accumulations in the Puna. In addition to collecting a sample of volcanic ash from the source volcanics, we want to sample surface soil (which I suspect to be eolian loess, in part).

9.6.4.6 Petrology and grain size analysis of the surface soils Describe the soil particle size and mineral composition. Assume the mineral composition will be both pure ash and impure downwind dust and soil. Among other things, we need to know whether there is volcanic ash in all three samples. Are surface soils appearing in the AIRf and calculus? Measure and describe the mineral hardness. Compare soil phytolith particle size distributions with the standard scale of sediment particle size, and decide what is going to be the particle size used in the comparison of abundance. How should you describe these distributions? There are peaks at both 20 μm and 45μm. Do phytolith particle size distributions from soil samples differ from distributions from leaf epidermis?

9.6.4.7 Map local dust source areas These include active volcanoes, relict volcanic edifices, dry lake beds, and the pyroclastic products or ring deposits around volcanic centers (e.g., Cerro Galan), encompassing the vast ignimbrite fields. Obtain aerosol dust particle size distributions from surface soil accumulations and wind trap data. The eolian dust component of soil minerals can be distinguished and identified (or not) in various parts of a landscape. What are the size resolved mass concentrations of the aerosol dust, the volume size distributions of surface dust (both seasonal and daily variation), and the size resolved mass ratios of elements to Si scaled to aerodynamic diameter?

9.7 Engines of erosion?

9.7.1 Jackrabbits and the North American Dust Bowl

The North American drought of the 1930s persisted between 1932 and 1938 and extended geographically from Mexico to Canada, covering a considerable portion of North America (and two-thirds of the continental United States), and had its greatest effects in the southern Great Plains. Caused by sustained anomalously cool tropical Pacific SSTs and warm SSTs over the North Atlantic during the decade, the severity of the drought was accentuated by feedback interactions between atmosphere and land surface, especially summer soil moisture (Schubert et al., 2004). In addition to the oceanic drivers identified by Schubert et al. (2004), human land degradation was an additional contributor (Cook et al., 2009). Land-use degradation is any reduction in vegetation cover (e.g., crop failure, overgrazing) that results in a soil dust source area. Land degradation not only contributed to the drought but amplified 9.7 Engines of erosion? 321

the drought into a true environmental disaster. The replacement by humans of more drought-resistant perennial natural grassland with a seasonal and drought-sensitive wheat crop, led to major dust storms and high atmospheric dust loadings. The magnitude and intensity of these were unprecedented in the historical record. While the Dust Bowl drought was unique during the period of continuous instrument records, comparable droughts are known to have occurred in North America in each of the last four centuries and even earlier in the thirteenth and sixteenth centuries, and extending back into the Holocene. The mega-droughts of the Holocene and Medieval Climate Anomaly were noted for their exceptional persistence rather than severity. These mega-droughts were longer and more intense than the Dust Bowl and were accompanied by large-scale dune movement over the Great Plains (Forman et al., 2001; Herweijer et al., 2007). While ENSO-like SST anomalies are understood to be the primary contributor, denudation (the striping bare of vegetation) and remobilization of dune fields across the Great Plains are the most conspicuous features of these mega- droughts (Forman et al., 2001). Was overgrazing by elodont jack rabbits part of these surface processes? The prolonged multiyear drought in the Dust Bowl of the Southern Great Plains was accompanied by frequent dust and sand storms, repeated failure of the wheat crop, and the abundance of jackrabbits (Worster, 1982). It was a remarkable coincidence. The biggest enigma in this suite of features is the proliferation of jackrabbits into a plague at the same time that sources of plant food (wild and crop) and all other animals (domestic and wild, and predators) were diminished. What enables rabbits to proliferate when all other herbivores are in decline? Black-tailed jackrabbits (Lepus californicus) are hunted by a host of aerial and terrestrial predators, including diverse hawks, owls, eagles, coyotes, badger, mountain lions, and bobcat. These jackrabbits prefer shrubland and like the cover it provides. Moreover, because they require forage with a relatively high water content, when not available at or above ground level, they dig for roots. There is a Holocene record of Lepus californicus, and the replacement of moist- climate and mesic-habitat small-mammal assemblages (comprising Lepus townsendii, Marmota flaviventris, Reithrodontomys megalotis, Brachylagus idahoensis) by dry- climate and xeric-habitat-adapted small-mammal assemblages (composed of Lepus californicus, Neotoma lepida) (Schmitt et al., 2002). In zooarchaeology, a “lagomorph index” is sometimes used to track the relative abundance of Sylvilagus and Lepus, and ascribe this change to climate or drought (Blanco and Villafuerte, 1993; Verdú and Galante, 2002). One wishes for a record of Lepus abundance of sufficient temporal resolution to track the dramatic climate fluctuations of megadroughts, and ideally, to ascertain the cycle of Lepus abundance in relation to the onset and duration of these drought cycles (or events). The longest records of hare abundance in North America are those of L. americanus (MacLulich, 1937, 1957; Elton, 1942), but these records are insufficient to show whether Lepus is a contributor or driver of dune reactivation and dust storm frequency, or whether Lepus was a victim of these natural surface processes. Are stratified cave deposits of raptor pellet-derived assemblages sufficiently resolved to 322 Ever-growing teeth

answer such questions? On the one hand, time-averaging in raptor accumulations in cave-ﬂoor records does not permit this kind of temporal resolution (Terry, 2008). However, Terry suggests that perhaps “death assemblages” that compare recent and subfossil pellet-derived accumulations with modern and historical trapping surveys might permit higher resolution over shorter timescales (Terry 2010a, b). 10 Summary and conclusions

10.1 Summary

During the Cenozoic, as many as twenty-six clades of South American mammals evolved high-crowned teeth. Of these, as many as half went on to evolve ever-growing teeth. The prevalence of hypsodonty in South American mammals is an expression of the long geographic isolation of the continent, and the many natural experiments of accommodation to South American environments that culminated in this extraordinary evolutionary convergence. The prevalence of hypsodonty may be higher among South American mammals than on any other continent. The prevalence invites explanation. The prevalence of high-crowned teeth in South American mammals is the accumulation of independent evolutionary events that occurred more or less continuously throughout the Cenozoic. The oldest manifestation of hypsodonty in South America is found in the late Cretaceous or Paleocene Dryolestida and Gondwanatheria. Some- time thereafter, the Xenarthra evolved ever-growing tooth crowns. It still is not known whether the three principal clades of xenarthrans, Tardigrada, Cingulata, and Vermi- lingua, evolved this feature independently. High tooth crowns also appear in middle Cenozoic Marsupialia, among the Groeberiidae, Patagoniidae, and Argyrolagidae. Numerous examples can be found among the native “meridiungulates” of South America, about which much has been written. There are also many examples of this among the native caviomorph rodents, subsequent to their arrival into the continent about 43 million years ago and occurring at different times throughout the Neogene. The prevalence of hypsodonty extends to some groups of living mammals that partici- pated in the Great American Biotic Interchange, including Camelidae, and importantly, the small mice or Sigmodontinae (Muridae). The prevalence of hypsodonty among South American mammals is an example of the more general problem of the evolution of structural enhancements to prolong the functional longevity of the dentition. The approaches taken in my exploration of the problem have included establishing the early history of this evolution in the South American fossil record. Additionally, this exploration has extended to the environmental correlates in the geographic distribution of high-crowned teeth among living mammals of South America. This pointed to a unique correlation to earth surface

323 324 Summary and conclusions

processes that were then explored in the geographic distribution of high-crowned teeth among mammals globally. From these emerging patterns of association, I turned to a fresh consideration of tooth wear in the best-known living mammals, domestic sheep and goats. These results increased my suspicion that earth surface processes drive excess tooth wear at ecological timescales, and this in turn toward an explanation of the prevalence of structures to resist tooth wear at evolutionary timescales. Armed with this emerging model, I turned to tests of predictions arising from these correlations, looking to examples of the evolution of hypsodonty on Mediterranean islands, and then comparing tooth wear rates in island populations of goats and sheep. Following this, using a coupled marine and continental record preserving both the suspected causal agents (terrestrial sediment) and a fossil record of their consequences for tooth shape evolution, I examined the role of erosion and the ﬂux of mineral particles across the land surface and through the herbivore environment. Earth surface processes are responsible for the relentless denudation of the continental surface and the transport of mineral particles through routing systems in the atmosphere and rivers, downwind and downstream to the coast, out over the oceans, and eventually through rainout, to accumulate in ultimate repose on the sea-ﬂoor. To understand the role of earth surface processes in the delivery of mineral abrasives causing tooth wear and the evolution of hypsodonty, I have attempted to follow these mineral particles from source to sink. I then returned to the South American fossil record to examine coincidences in the reconstructed sediment cascade of middle Cenozoic Patagonia. Lastly, I have explored the potential consequences of the evolution of elodonty and the prevalence of elodont mammals to earth surface processes themselves, turning around the chain of causation.

10.1.1 Hypsodonty in modern mammals

Using faunal inventories of mammal species at 80 sites throughout South America, 560 species of mammals have been classified into diet and molar crown-height classes. Using the standard classification of mammal diets from zoology, we find that grazers and herbivores are mostly hypsodont wherever they occur in South America. We also note that half of all folivorous and insectivorous mammals have high tooth crowns, as do some granivores and frugivores, but no carnivorous and only very few animal- ivorous mammals have high-crowned teeth. When the 80 sites are partitioned into those that occur in mountains and those in lowlands, we find that mountain environments exert a positive influence on the prevalence of hypsodonty, and herbivores in Andean faunas are uniformly more hypsodont. Partitioning the sites in another way, we find that areas of active volcanism (where mammals live on volcanic ash soils of recent origin) exert a much stronger positive influence on faunal hypsodonty across most diet classes (except insectivory and granivory). To inquire further about the environmental correlates (direct and indirect) of the prevalence of hypsodonty (direct and indirect) in South American mammals, 26 continuous and nominal environmental variables were compiled for the same 80 sites. These 10.1 Summary 325

variables are from physical geography, plant physiological ecology, general ecology, production biology, and an understanding of environmental stress on plant tissues. In addition, the obvious differences in sampling intensity between sites or inventories and the geographic area of the 80 sites are controlled using covariables. Partial direct canonical community ordination depicts most of the variation in tooth crown height along the horizontal axis, and finds the prevalence of hypsodonty to be related to a dichotomy between warm and wet conditions (or sites) at one extreme versus dry and cool climate conditions (sites) at the opposite extreme. The remaining variation in the vertical axis correlates with topography (relief) and open vegetation. Forward selection from among these environmental variables reveals volcanic ash soils, mean annual temperature and mean annual precipitation driving the variation in tooth crown height along the first or horizontal axis. Going one step further, when all the variation in prevalence attributable to climate variables (meteorology) is partialled out (mean annual temperature, mean annual precipitation, the range of mean monthly temperatures, and the mean monthly temperature of the coldest month), and the residual variation is plotted on an outline map of South America, we discover discontinuities between geographic areas of high residual hypsodonty. The zones of high residual hypsodonty are arrayed along the western Andean margin of the continent. Comparing the extent of these areas of disjunct distribution with the two principal sources of mineral particles in Andean environments (volcanic ash and glacial loess), we find that areas of high residual hypsodonty correspond with the latitudinal distribution of active volcanoes, not glaciers. Even more significantly, the area of highest residual hypsodonty coincides with the intensity of the earth surface processes that mobilize volcanic ash and transport it across the land surface and through the animal’s environment. In this case, the routing system is wind as expressed by annual dust storm frequency. These geographic coincidences implicate both sediment source areas (in this case active volcanism), and the earth surface processes that deflate and transport volcanic ash across the land surface. If we remember that fluvial erosion rates are high in tectonically active or mountainous areas, but much higher still in regions of active volcanism, we begin to appreciate the role of earth surface processes as the agents of sediment delivery that underly the prevalence of hypsodonty. For a few important reasons, volcanic ash is particularly suspect as an environmental agent associated with high tooth wear and hypsodont tooth crowns: (1) formed at high temperatures, their weak chemical bonds are naturally susceptible to weathering; (2) microporosity imparts high permeability and also the qualities of volcanic ash that make it an abrasive of industrial significance; (3) when sorted by wind and deposited as silt or tephric loess, accumulations of pyroclastic sediment are notoriously incohesive and susceptible to erosion; and (4) this, combined with general conditions of dry or seasonally dry climates, where exposed mineral particles are readily mobilized by wind (or in some circumstances, in wet climates where rain and rivers drain areas of pyroclastic sediment accumulation). The prevalence of hypsodonty among herbivorous mammals in 256 modern mammal faunas around the world reveals that the highest levels of faunal hypsodonty in the northern continents are coincident at around 30 N latitude. There is an evident mirror 326 Summary and conclusions

of this zonal distribution at 30 S. Recall that the northern hemisphere continents are in a terrestrial hemisphere with high seasonality and aridity, whereas the southern continents are in an oceanic hemisphere with moderated seasonality and higher moisture levels. The latitudinal bands at 30 degrees latitude correspond with the high atmospheric pressure bands of the Hadley cell circulation, the latitudinal bands of zonal aridity, high evaporation, low weathering, and desert vegetation, and this association is fairly clear even for the southern continents. We ﬁnd latitudinal bands of high faunal hypsodonty to be consistent with aridity, and less clearly related to the latitudinal distribution of grasslands. Finally, as with South America, we ﬁnd a rather striking visual association among the latitudinal prevalence of hypsodonty, dust source areas, and dust storm frequency, that peak in the 30 degree latitude bands in both southern and northern continents.

10.1.2 Tooth wear in New Zealand

We know more about tooth wear in domestic sheep than any other living mammal, thanks to the labors of veterinary pathologists in New Zealand. On the North Island of New Zealand, excess tooth wear is chronic and endemic in some areas. The problem was identified originally during the war years when wool production was limited by premature dental senescence. At that time, the geographic and temporal scales of the problem were unknown, but the data that permit us to understand these today were diligently gathered. Then, the explanation for excess tooth wear seemed to be complicated by myriad etiology, but despite the apparent complexity, the essence of the problem was discovered and multiple effective remedies were found. The biological and evolutionary consequences of excess tooth wear in sheep can be expressed in terms of both mortality and fecundity. In the areas of endemic excess tooth wear, premature dental senescence required the culling of ewes from herds due to loss of condition. The implications of this premature mortality for fecundity are significant, as it truncates most of the reproductive lifespan; in essence, a significant decrease in fitness. Once we acknowledge its significance in sheep, we examine both the temporal and spatial variation in excess tooth wear. Over the annual cycle, seasonal variation in tooth wear is driven by soil ingestion. In the classic studies of Ludwig, Healy, and Cutress (1966) on the problem of endemic and chronic excess tooth wear in sheep in the Wairarapa region of the North Island, tooth wear and soil ingestion peak during the southern hemisphere winter, when cooler temperatures slow plant growth. The austral winter on the North Island also coincides with the season of highest rainfall, and in addition, with the period of highest energy demand in the reproductive cycle. Researchers found the abundance of mineral particles intrinsic to forage plants was not driving variation in tooth wear rates because the concentration of phytoliths in pasture grasses is essentially unvarying throughout the year. Moreover, when phytoliths are segregated from among the acid-insoluble residue in sheep fecal material, they comprise a very modest and unvarying proportion. By contrast, soil mineral abundance in fecal material varies seasonally and is very much greater during winter when animals 10.1 Summary 327

feed aggressively and crop close to the soil surface. As winter tooth wear accumulates year after year, the enamel crowns wear away, and eventually animals can no longer feed adequately and must then be culled. When all available long-term studies of tooth wear in sheep are compiled, interannual variation in soil ingestion is pronounced. If annual tooth wear is plotted against the multivariate El Niño–Southern Oscillation (ENSO) index, an expression of climate variability in New Zealand, a suggestive coincidence is seen between the highest rates of tooth wear and positive anomalies. At longer decadal timescales, there is a vague suggestion that even longer-term climate cycles play a role in tooth wear variation. Positive anomalies of the Pacific Decadal Oscillation (PDO) are associated with higher scientific output (number of publications) in studies of both soil erosion and tooth wear. Government support of science in New Zealand, as elsewhere, responds to circumstance and public need, and scientists shamelessly and necessarily take advantage of funding opportunities. If catastrophic soil erosion events are more frequent and disastrous when ENSO cycles are accentuated by the PDO, then naturally it shows up in patterns of scientific research productivity, and in studies of both tooth wear and soil erosion. When tooth wear variation for study sites on the North Island is superimposed onto a map of the intensity of surface erosion represented by an event-proxy, the percentage of surface area affected by the February 2004 cyclonic rainstorm event, tooth wear rates are higher within the area affected by the soil erosion induced by this rainstorm. The area affected by the February 2004 cyclonic rainstorm is a single-event proxy for long-term average soil loss. In numerous studies of excess tooth wear, a geographic association is found between the rate of tooth wear and the susceptibility of soils and soil parent material to erosion. The area of endemic excess tooth wear identified by veterinary pathology on the North Island is enclosed here by a polygon and mapped in relation to the area affected by the same storm event; there is a rather close geographic coincidence. Subtropical cyclones deliver rainstorms over the North Island at intervals of about 3.7 years (the ENSO periodicity), and their consequence “melts” the land surface (i.e., resulting in regional slumping or slipping). This kind of soil erosion brings soil onto the pasture grasses preferred by sheep. Landslip scars from recurrent ENSO erosion events are areas of constant soil-contaminated pasture. Furthermore, these rainstorms are associated with suspended sediment load in the rivers. For all study sites (or sheep stations) where excess tooth wear and soil ingestion have been measured, long-term average and specific sediment yields in the local 15 km2 hydrographic basin draining each site yields a linear relationship. While the precise shape of the line summarizing the relationship between annual tooth wear and suspended sediment yield is debatable, this is a strong relationship. The area affected by the storm-induced erosion event of February 2004 has a disjunct geographic distribution on both sides of the axis of the Wellington–Wairarapa right- lateral strike-slip fault complex. These faults are among the most active on Earth. The displacement of the areas affected by erosion reveals the susceptibility of soil parent material (the regolith) to erosion. The properties of soil parent material, not surface soils, contribute to the susceptibility to erosion. Soil parent material on the 328 Summary and conclusions

North Island is Quaternary tephric loess, the accumulated volcanic ash or ash-rich sediment mixed with the erosion products of older marine rocks. Rivers carry the rainstorm-eroded volcanic ash-rich sediments downstream and into lakes, where they get deposited as storm events on the lake bottom. Recovered sediment cores reveal a record of the chronology of storm-induced erosion events. The frequency and magnitude of these events are coincident with positive phases of the PDO or Interdecadal Paciﬁc Oscillation and their inﬂuence on the intensity and frequency of cyclonic rainstorms. Of course, tooth wear in North Island sheep has many correlates and veterinary pathologists have been diligent in examining almost everything thought to contribute to tooth wear, including heredity, nutrition, jaw biomechanics, and many other potential environmental causes. Through all this research into the etiology of excess tooth wear, there is woven a single thread of historical primacy, the association of excess tooth wear with soil ingestion.

10.1.3 Tooth wear and tooth size in Australia

Australia is the driest continent on Earth after Antarctica, and also the lowest and flattest. It is situated astride the southern horse latitudes, the latitudinal climate zone of high atmospheric pressure where evaporation exceeds precipitation, and where we find the highest levels of faunal hypsodonty. Much of Australia is semiarid, arid, and hyper-arid desert with characteristically intense seasonality, and surrounding the deserts is a fringing halo of dry country grasslands. Australia is renowned for its climate variability where extreme events are news headlines frequently. Dust storms, wildfires, floods, and cyclones (typhoons) punctuate the most highly variable agricultural productivity of all major grain exporters. From the perspective of our problem, the evolution of high-crowned teeth, Australia ought to provide the perfect test case. Like South America, a unique mammalian (or metatherian) fauna evolved in Australia in geographic isolation from the rest of the world. However, unlike South America, and with only a few exceptions, there are very few high-crowned marsupial herbivores in Australia. For a land dominated by aridlands and grasslands, it is remarkable that so few elements of its native terrestrial fauna evolved high-crowned teeth. Some have argued that because of structural and functional constraints, the characteristically lophodont teeth of kangaroos cannot evolve hypsodonty. Others have observed that Australian macropodids prolong the functional longevity of their dentitions by the progressive replacement of the worn-out crowns of earlier-erupting teeth pushed out by later-erupting crowns as they migrate forward. In addition to this effective mechanism of tooth replacement, the posterior teeth increase in size. Whether Australian native marsupials confronted excess tooth wear during their evolutionary history, Australia seems ideal for testing the hypothesis that earth surface processes play a role in the evolution of tooth shape. For this, we have another remarkable study of tooth wear in sheep, conducted at the same time as the work on the North Island of New Zealand. These are the results of a 10.1 Summary 329

two-year study of sheep tooth wear conducted at the Dickson Experimental Station in Canberra and extending through three successive winters. As on the North Island of New Zealand, silica ingestion peaks in June, July, and August when ewes are pregnant and lactating. Significant interannual variation in silica ingestion was highest in the winter of 1960, and there were smaller but evident peaks, at least at high stocking rates, in the winters of 1959 and 1961. The Australian researchers measured the acid- insoluble residue in fecal material (AIRf), which includes ingested soil silicates in addition to plant silica. Phytolith abundance in the AIRf was measured by counting fields of view on microscope slides, with no attention to the actual fraction of AIRf, and during the two-year course of the study, tooth wear was measured only three times. These deficiencies are unfortunate, as more careful and frequent measurements could have revealed whether wear was associated with phytolith abundance or ingested silica. The annual pasture cycle in southern New South Wales is evident in both the AIRf and phytolith abundance data. Treatment effects (stocking rate or grazing intensity) influence both soil ingestion and phytolith abundance. Soil ingestion is highest at high stocking rates, and phytolith abundance in pasture grasses is lowest at low stocking rates. The combination of the pattern of tooth wear, treatment effects, and the increased demand associated with the reproductive cycle suggests animal behavior through surface disturbance by feeding and is the mechanism of soil silica ingestion. Other than its phytolith fraction, the remainder of the silica content of fecal material was not described. Presumably, it is soil. The study site was located on a limestone shelf or bench with an alluvium cover that contains a distinctive eolian component. The eolian contribution is carbonate, the reworked parna surface that covers much of the surrounding area of southwestern New South Wales. To the extent that acid preparation would have dissolved away the carbonate, AIRf underestimates ingested soil. The mineral composition of modern soil at the study site is a balance between accession and soil loss. Atmospheric dust accession (by both wet and dry deposition) is the predominant mode of mineral particle input, and sheetwash and rill erosion is the dominant form of soil loss. The study site in Canberra is just east of the Murray–Darling River Basin, and in addition to receiving all the erosion products off the eastern uplands, the study site is on the southeastern dust path. The Lake Eyre Basin, the principal dust source region in Australia, is to the west and upwind of the study site. To answer the question of whether active earth surface processes contribute to or coincide with the seasonal peak AIRf, annual patterns of both dry and wet deposition were examined. Dust storm frequency and intensity are functions of effective soil moisture and wind run (fetch). The seasonal calendar of dust storm activity reflects their interaction. Dust storm frequency is not coincident with AIRf, and dust storms are not delivering silica minerals into the grazing environment. However, during winter when AIRf peaks, rainfall is relatively high all across New South Wales and dust deposition also peaks. In Canberra, atmospheric dust samples are collected using rain gauges, as the gauges not only collect rainfall but also the dust that is washed out of the atmosphere. Sheet and rill erosion rates are low through much of the year in Canberra, but accelerate with winter rains after the seasonal break. This form of erosion is highest 330 Summary and conclusions

from July through August. Thus, rains bring mineral particles out of the atmosphere and rain-splash can contaminate pasture plants, especially for those varieties of Phalaris grass that are prostrate and palatable to sheep. Any working hypothesis about sheep tooth wear in this classic study in Australia should begin by pointing out the obvious, that Australia is a stable continent and the Indo-Australian plate (an amalgam of stable cratons) has no significant internal tectonics or volcanism. This was not always the case, as the rifting of Australia away from Antarctica during the Eocene was accompanied by a lot of volcanic activity. Today, and evidently for much of the evolution of its living marsupials, there was little orogeny (mountain building) or volcanism. What this implies is that there is little available sediment, sediment isopachs are very shallow everywhere, and Australia is starved for surface sediment. Australia boasts the requisite interplay of climate controls on surface processes, and all the requisite eolian and fluvial routing systems, but precious little surface sediment available for movement by these systems. The average erosion rate in Australia is about 4.1 t/ha/yr and is negatively skewed toward lower rates, with 28% of the continent eroding at less than 0.5 t/ha/yr, but only 8% of the continental surface erodes at a rate greater than 10 t/ha/yr. Compare this to the North Island of New Zealand where erosion rates vary between 11 t/ha/yr and 89 t/ha/yr and are positively skewed, or to Ethiopia where erosion rates vary between 16 t/ha/yr and 300 t/ha/yr (mean¼42 t/ha/yr) and are also positively skewed. The largest teeth among modern humans are found among the aboriginal inhabitants of Australia. The largest are found in southeastern Australia, along the Murray River, where the river meets the area influenced by the southeast dust path. Tooth wear among aboriginals is highest in this area where aerosol dust deflated off fresh surfaces created by fluvial-eolian interaction gets transported through the environment. Levels of surface flux were much higher during the Quaternary than today. The relationship between high tooth wear and large tooth size in aboriginals is similar to that between tooth wear and hypsodonty in ungulates; tooth size in bunodont humans is another expression for the increased volume of tooth mineral substance in the dentition. The highest tooth size among modern humans in Oceania is geographically coincident with the Andesite Line, the surface expression of intense explosive and pyroclastic-rich volcanism associated with the zone of subduction between oceanic and continental crustal plates.

10.1.4 Tooth evolution and tooth wear on islands

There are at least six examples on islands in the Mediterranean of ruminant artiodactyls evolving exceptionally high-crowned cheek teeth and two examples of their evolving ever-growing incisors. In addition to these, diverse dental structures for resisting abrasion evolved in other ungulates (suids and cervids) and rodents (glirids). That such diverse morphological contrivances are found on islands throughout the Mediterra- nean suggests coincident causation. Explanations advanced in each particular case (specialized food acquisition in Myotragus from the Balearics, feeding on Gramineae for “Megaceroides cretensis” of Crete) seem inadequate to explain the convergent 10.1 Summary 331

evolution. Yet a sweeping claim in favor of a single encompassing explanation involving the earth surface processes of erosion, volcanism, and wind in island ecosystems, while perhaps plausible, seems hardly more convincing. The available information on temporal and spatial variation in earth surface processes through the five-million-year history of dental adaptation in the Mediterranean is frustratingly incomplete, and the fossil and rock records from Mediterranean islands do not permit reconstruction of coincident timing and geographic distribution between agency and evolutionary response. To examine the role of surface processes on tooth wear in unmanaged island ecosystems, relative tooth wear in feral ungulates has been compared between islands with contrasting vegetation, surface soils, and topography. The importance of islands to evolutionary morphology should be obvious to everyone, as it was to Darwin and especially to David Lack and Peter Grant. Islands witness high rates of evolution, they have unstable environments where mortality is always significant demographically and genetically, and where the geographic scale of agency often matches that of the population affected by it (another way of saying that there is no escape). Finally, islands are mostly unmanaged. In unmanaged ecosystems, dental senility in sheep and goats is expressed as the progressive wearing down and eventual structural collapse of the anterior premolar and molar tooth crowns, until finally the largest and last tooth position in the tooth row (m3) fails. In view of this pattern of tooth wear in unmanaged populations, natural selection likely targets m3 for structural enhancements to functional longevity (and thereby increase the reproductive lifespan and fitness of the individual). A comparison of relative tooth wear is made on three islands in the South Pacific, two islands in the Kermadec group (Macauley and Raoul Islands) and Campbell Island in the sub-Antarctic: on Macauley Island, a browser grazing on a volcanic ash soil; on Raoul Island, a browser feeding in a closed forest on the slopes of an active volcano; on Campbell Island, a grazer in a grassland on an organic peat soil (with no mineral soil exposed at the surface). Relative tooth wear rates are compared across species (Capra hircus, Ovis aires) among these islands, using dental eruption and the onset of wear as developmental benchmarks of comparison, and by comparing tooth wear stages at all tooth positions anterior to the erupting crown. Comparisons of modal wear stages for premolar and molar crowns in Macauley, Raoul, and Campball Islands’ ovicaprines at comparable stages of dental eruption include: (1) m1 erupting into wear, (2) m2 erupting into wear, and (3) m3 erupting into wear, and reveal important differences in relative wear rates among the islands. Tooth wear is most rapid on subtropical Macaulay Island, where a browser (Capra hircus) grazes on low grass growing on a thick pumice and ash soil. Relative tooth wear rates are intermediate on subtropical Raoul Island, where a browser (Capra hircus) browses in forest vegetation on the slopes of an active volcano. Relative tooth wear rates are lowest on sub-Antarctic and stormy Campbell Island, where a grazer (Ovis aires) grazes grasses in a tussock grass shrubland growing on a thick organic peat soil and where there is no exposed mineral soil. 332 Summary and conclusions

10.1.5 Tooth shape evolution in the Plio-Pleistocene of East Africa

Direct evidence of a relationship between the intensity of soil erosion and tooth shape evolution can be made in mammals of the Plio-Pleistocene of NE Africa, where there is a temporally coupled marine record that preserves a history of surface erosion in NE Africa where the mammals lived. The fossil record in East Africa makes a legitimate claim to be the best fossil record of mammal evolution on Earth. The extinct animals that are preserved there have living descendants that are very well known biologically and ecologically. The rift valleys of northern East Africa occur in a mountainous area, the Rift System, characterized by high relief and active volcanism. Of particular interest is the Turkana Basin, a topographic low point in the rift system, surrounded to the north by the Afar Plateau of Ethiopia and to the south by the East African plateau. The Turkana Basin is a low intermountain basin, and this has consequences for erosion. The Ethiopian plateau presents some of the highest erosion rates anywhere in Africa, experiences very high winds, and has the highest potential of all of Africa for the development of wind-energy. The Turkana Basin is swept by the Turkana nocturnal low-level jet, the most intense wind in Africa, a summer monsoon wind the intensity of which is enhanced by channel effects. It blows down through the basin, sweeping up the fine-grained volcaniclastic sediment left by erosion and eruption in the volcanic uplands, lofts this dust high into the atmosphere, and carries it out over the Arabian Sea where it rains out and eventually drifts down through the water column to accumulate on the sea-floor. Taking advantage of the fact that the region is presently a theater of war and many resources are brought into focus to predict dust storms for the benefit of the Pentagon’s ordnance and democracy delivery systems, we see the intensity of erosion in NE Africa and two satellite-based methods documenting the transport of mineral particle dust by wind off the Horn of Africa and out over the Arabian Sea. Over the Arabian Sea, the mineral particles rain out and fall to the sea-floor, where they have been recovered through the nearly miraculous efforts of the DSDP/ODP. The DSDP/ODP Site 721–722 record of terrestrial sediment input to the Arabian Sea floor displays a lot of temporal variation. This is not surprising, given that erosion operates at all timescales, under the influence of many climate cycles (seasonal, interannual, decadal, millennial, orbital, etc.). To this record, smoothing functions are fitted to capture the longer-term orbital timescale average trends in the intensity of soil erosion. The terrestrial sediments on the Arabian Sea floor are, in part, volcanic. The record of volcanic eruption events and the volcanic glass shard counts show both the frequency and periodicity of preserved eruption events and the more constant delivery of volcanic ash by wind. The temporal coupling between the marine and continental records is clear and the curve of changing long-term average erosion intensity is matched by lithologic change in East African rift basin sediments. The temporal coupling reveals local controls on this erosion system that are otherwise hidden among orbital timescale variation and earth surface processes that operate at shorter timescales. For example, 10.1 Summary 333

the apparent relationship between lacustrine diatomite sedimentation in rift valley lakes and high eolian export may be explained by a fluctuating co-dominance between fluvial and eolian processes operating at shorter timescales. The relationship between soil erosion and tooth shape evolution have been examined in two lineages of Plio-Pleistocene Suidae: (1) Metridiochoerus, and (2) Nyanzachoerus–Notochoerus. In these lineages, the m1 wears out early, and there is a steep gradient of wear from m1 to m3. The crowns of m3 are elongate and multicuspate, and have thicker enamel. Enamel thickness not only increases from m1 to m3, but also from anterior to posterior cusps on m3. Metridiochoerus is a well-supported clade with a paleospecies lineage in which dental evolution is characterized by an enlarging m3, with increasing crown complexity and crown height. This lineage is also characterized by an evolutionary increase in body size. Using only material from the Turkana Basin, m3 tooth size (length width ¼ crown area) captures the evolution of crown height and megadonty, which additionally contribute to total enamel volume. The evolutionary trend in Metridiochoerus’ m3 crown area when plotted against long-term average erosion intensity in the sea-floor sediment record reveals that most of the evolutionary trend toward larger tooth size occurs during the interval of most intense soil erosion. There is as yet no body of theory that provides us with an expectation of what we ought to see in a relationship between soil erosion and mammal tooth evolution. We might be seeing periods of directional evolution alternating with periods of evolutionary stasis, and when we project these changes in evolutionary rates against the erosion curve, we find they coincide with change in the intensity of erosion. The evidence suggests that when erosion crosses above some imaginary threshold, it triggers an evolutionary response in m3 tooth size or total enamel volume. Another possible interpretation might be that we are seeing a single evolutionary trend, the initiation of which coincides with a change in the erosion or dust flux regime, perhaps triggered by change in the orbital timescale controls on erosion. The Nyanzachoerus–Notochoerus lineage of suids is another well-supported phylogeny with an embedded paleospecies lineage. In addition to dental evolution in m3, this lineage is characterized by an evolutionary increase in body size. All paleospecies of this lineage occur in the Turkana Basin, where stable carbon isotopes reveal little or no change in their diets. The Nyanzachoerus–Notochoerus lineage is characterized by a pattern of evolution in m3 wherein the crown elongates, becomes multicuspate through addition of cuspules posteriorly, and increases in crown height. This lineage is also characterized by the evolution of m3 megadonty whereby the m3 crown enlarges relative to the other molars. When m3 tooth size in Nyanzachoerus–Notochoerus is plotted against the record of erosion intensity, accelerations in directional evolution of m3 correspond to peaks of high erosion intensity. This appears to be a record of alternating stasis and directional evolution, with directional evolution responding to periods when erosion exceeded a threshold value that triggered a change in the rate of tooth evolution. Evolution of m3 in Theropithecus can be described as a simple monotonic trend of increasing tooth size, or after fitting a smoothing spline to the data, with some 334 Summary and conclusions

variation in evolutionary rates. In particular, there are three intervals of directional evolution that are coincident with peaks in the terrigenous percentage input to the sea- floor record. Here again, a threshold effect seems to trigger the onset of directional evolution. Both the direction and magnitude of delay in the evolutionary response is consistent with the record of erosion intensity. Additionally, the evolutionary response is delayed after the moment of change and the onset of each significant acceleration of erosion. Australopithecine dental evolution is characterized by two major features, an increase in enamel thickness and molar megadontia (an increase in tooth size relative to body size). Both trends result in an evolutionary increase in enamel volume. When australopithecine m3 tooth size evolution is plotted in relation to long-term average erosion intensity, there are three moments during the Plio-Pleistocene when australopithecine m3 tooth size evolution accelerated. These three periods correspond with intervals of high erosion intensity. As among both lineages of Suidae and also Thero- pithecus, we seem to be confronted by yet another example of m3 tooth enlargement in response to soil erosion when the intensity of erosion exceeds some threshold value. As I have tried to show, the preferred hypothesis is that change in tooth shape (or crown area, a proxy for the amount of tooth mineral substance) should reflect the intensity of tooth wear as determined by the amount of abrasive mineral grit on foods. This causal relationship leads to a set of predictions about the coincidence between environmental variables related to the intensity of surface processes and the evolutionary response. These predictions are: (1) as the rate of erosion changes, so should change in tooth shape; (2) the direction of change in each should be similar; (3) if there is any offset or lag, the evolutionary response should occur after the change in erosion; (4) to the extent that any lack of coincidence is related to sampling deficiencies, temporal coincidence should improve with the quality of the fossil record (increasing abundance of fossils); (5) of the four environmental variables, lithogenic flux should provide the best fit to the evolutionary response; and (6) given the nature of the routing system, lithogenic flux should drive coincident change in all four lineages. The environmental variables were sampled at uniform intervals along a marine sediment core recovered from the floor of the Arabian Sea. This downwind record of environmental conditions in the sediment source area of the East African rift system is expressed as four different variables: (1) the terrigenous fraction of the marine sediments (terrigenous percentage), (2) sedimentation rate, (3) lithogenic flux, and (4) volcanic ash shard counts. Terrigenous percentage is the fraction of sediment of terrestrial origin in the total mass of each sample. The linear sedimentation rate is a measure of the rate of sediment accumulation on the sea-floor. The lithogenic flux is the amount of terrestrial sediment falling through the water column per unit time, and is related to the amount of dust that rains out of the atmosphere onto the sea surface less the amount scavenged by surface phytoplankton. The count of volcanic ash shards is the number or abundance of fragments of volcanic ash in the terrestrial sediment fraction. The response variables are measurements of tooth size in Metridiochoerus, Nyanza- choerus–Notochoerus, Australopithecus, and Theropithecus, and the mammalian herbivores that inhabited the dust source area. Tooth size captures the volume of tooth 10.1 Summary 335

mineral substance, which is the evolutionary response to the amount of mineral substance lost by abrasive tooth wear during the animal’s life. The four mammal “curves” respond most convincingly to flux, less convincingly to terrigenous percentage, and least well to shard count. Shard count could be more interesting, when ash productivity coincides with lithogenic flux. That is, we should expect to find the most pronounced changes in evolutionary rates occurring when all volcanic variables (frequency, intensity, and average ash) coincide with total lithogenic flux, given all the properties of ash that make it such an important abrasive.

10.1.6 Tooth shape evolution in the middle Cenozoic of Patagonia

Returning to consider the South American fossil record of precocious hypsodonty, in my view, there were grasses in Sarmiento Formation time (as indeed the phytolith record shows), abundant dung-beetle brood balls (as the ichnofossil record shows), and possibly a variety of structurally distinct kinds of vegetation, including what we might call gradations between closed and open vegetation, somewhere in the region sampled by the phytoliths that we find at Gran Barranca. All these things may co-occur in the Sarmiento Formation. In addition, we find evidence for the appearance of mammalian herbivores with higher-crowned, even hypsodont teeth, and their rate of faunal evolution (increase in mean hypsodonty index within clades) varies through Sarmiento time. Environmental conditions, as revealed by depositional environments, alternate between fluvially dominated and eolian-dominated systems. Eolian-dominated sedimentation coincides with increases in faunal hypsodonty. Conventional oxygen and carbon stable isotopes do not change dramatically during Sarmiento time, and the subtle changes we find in atmospheric mean annual temperature, precipitation, and humidity do not seem to be of a magnitude sufficient to indicate we have crossed thresholds between forest and more open conditions. Apparently, subtle changes in mean annual precipitation are coincident with change in depositional environments from fluvial to eolian and evolutionary pulses of increasing hypsodonty. Soil ingestion drives most variation in tooth wear rates, and is the cause of excess tooth wear. While other causal agents have been implicated in the etiology of excess tooth wear, most involve soil ingestion. If there were grasses (whether in forest or open country) during Sarmiento time, then herbivores were almost certainly attracted to them and fed closer to the land surface. While we do not have much evidence in the way of postcranial bones, we can assume that native meridiungulates were terrestrial, many other mammalian herbivores were probably burrowing or digging animals, and many herbivores among meridiungulates were small and lived close to the land surface. Furthermore, mammalian herbivore foraging behavior itself almost always generates surface disturbance and mobilizes mineral particles onto plant surfaces. Everywhere we look around the world, we find convincing evidence that the intensity of surface processes contributing to long-term average mineral particle flux (the movement of mineral particles across the earth surface) coincides with high faunal hypsodonty and change in evolutionary rates of hypsodonty. 336 Summary and conclusions

Not surprisingly, wherever we find a positive relationship between the intensity of erosion and either tooth wear or the evolution of hypsodonty, the soils and sediments are volcaniclastic or pyroclastic. This is not because of some special relationship between volcanism, per se, and tooth wear or hypsodonty, but rather because volcaniclastic sediments, when present, are very abundant and have unique properties that make them especially susceptible to weathering and erosion (the highest rates of mineral particle flux occur in volcaniclastic settings). Moreover, volcanic ash or glass, the primary constituent of pyroclastic sediment, is an abrasive of universally recognized and even industrial significance. What might be construed as being interesting is that the three “episodes” of more rapid increase in hypsodonty in Patagonia coincide with “pulses” of increased eruption activity (or frequency). Of these three “pulses,” two of them are accompanied by active sediment accumulation (as defined by any linear sedimentation rates at all), the oldest and youngest. Therefore, one might conclude that the oldest and youngest “episodes” of increasing hypsodonty occur at a time of active volcanic eruption and high sedimentation rates. The middle “episode” is more difficult. It seems to suggest that when high eruption frequencies are not accompanied by active sediment accumulation, they have relatively little influence on hypsodonty. A comparison of the timing of the three hypsodonty episodes set beside the available downwind record of marine productivity in the Southern Ocean reveals peaks of marine phytoplankton productivity during the hypsodonty episodes. The nearest core (DSDP 511) record is an incomplete record because of poor core recovery, but more distant cores (ODP 689, and even farther out, ODP 748) show evidence of fertilizing aerosol dust reaching the sea-surface farther out in the Southern Ocean, illustrating some of the consequences of the progressive, step-wise changes in configuration and depth during the prolonged process of the Drake Passage opening.

10.1.7 The evolution and implications of ever-growing teeth

For at least 13 clades of South American mammals, hypsodonty was merely a temporary moment along the evolution of ever-growing teeth. The ever-growing tooth never wears out, and so is a deﬁnitive solution to premature dental senescence. A mammal with ever-growing teeth can eat anything and the slurry of ingested soil between the teeth can be harnessed to pulverize all kinds of vegetable matter into a suitable substrate for gut microbes. There are rather notorious examples among mammals. The rabbit ought to be worshipped. Peaceful conqueror of continents and hundreds of islands around the world, the rabbit, with its fully elodont dentition, leaves a detectable imprint on sediment cascades. It is estimated that over 10% of rabbit introductions on naïve islands resulted in the complete denudation of the vegetation by overgrazing and eventual extinction of the rabbit. The only thing that saves the rabbit from the results of overgrazing is its capacity to recover from population crashes through its unrivaled reproductive capacity. If one elodont mammal is devastating and detectable, what might be the impact and footprint of elodonty in Andean South America where half of all mammal 10.2 The metaphysics of causation 337

species became elodont in the Neogene? Might they have eaten the land naked andkickedupsomedust? How does elodonty evolve? The Vicugna is the best-known living example of a ruminant that evolved ever-growing teeth, and the modern environment of the Vicugna may deliver an explanation. The combination of aridity, active volcanism (and ash accumulations), plenty of exposed soil, an active routing system that is measured in frequent dust storms, and low grazing by a hoofed mammal ought to result in high leaf soil load and high fecal AIR.

10.2 The metaphysics of causation

Plausible and convincing arguments about causation have many properties: (1) immanence, the cause immediately precedes the consequence and both are congruent in space and time; (2) individuation, or independence of examples; (3) adicity, how many causal relata are involved and can these be resolved; (4) connection, what is the nature and pathway of causation; (5) direction, can the direction of causation be established even where obscured by timescales and incomplete records; and (6) selection, distinguishing sequences that include the cause from those that involve mere conditions. A satisfactory causal explanation should include elements of material, formal, efﬁcient, and ﬁnal causes, and there should be convincing arguments about why the relationship has not been noticed before. Finally, there is the obligation of explaining why popular approaches have been misleading and offer little prospect of contributing to further resolution.

10.2.1 Immanence

Does the cause immediately precede the consequence? In a historical science like paleontology that does not preserve animal behavior and the fossil record of increasing crown height is collected from stratigraphic records that rarely preserve geomorphic processes, immediate precedence is not easy to establish. The prevalence of hypsodonty is a result of evolutionary change and paleontologists have tried to become zoologists and behavioral ecologists to understand the process better. Precedence is easier to manage at ecological timescales, and this is why much of this book is devoted to an understanding of tooth wear, soil ingestion, and the earth surface processes that deliver mineral abrasives into the animal’s environment. Erosion events are always followed by exacerbations of excess tooth wear, and dust storms precede the accession of aerosol dust to surface soils. Surface disturbance always precedes the ingestion of soil and its mastication by teeth. Excess tooth wear always precedes dental senescence, and when premature dental senescence and mortality truncates reproductive lifespan, the pressure of natural selection increases and evolutionary response becomes the consequence. If precedence is difﬁcult to establish, are cause and effect otherwise in the same space–time? Much of this book wrestles with the problem of matching temporal and 338 Summary and conclusions

spatial scales, and finding appropriate records of both process and consequences. The ODP 721–722 sea-floor sediments are the downwind record of erosion where mammals inhabit the sediment source area in the Lake Turkana Basin. Volcanic eruption events and volcaniclastic sediments are emissions from geographically coincident source areas, and a plausible mechanism exists for delivering these sediments to Owen Ridge in the northern Arabian Sea and the ODP 721–722 marine sediment cores. Temporal resolution of the sea-floor sediment record and the terrestrial fossil-mammal record in the Turkana Basin are very different. While we apply the same method of curve fitting to these data to extract time-averaged change, we make an assumption about our ability to establish their geographic coincidence in time. It is a long way from the Arabian Sea to the Turkana Basin. We analyze the fossil record of tooth size evolution from specimens collected on all sides of the Turkana Basin and the Ethiopian rift as if they were one population and a coherent geographic entity. The source area of the sediment cascade and the routing system I have implicated may correspond to the source of the volcanic component in the sea-floor record, but probably not to the source area of all components of the terrestrial sediment. Rainstorm sediment pulses in a lake bottom sediment core from Lake Tutira occur in the same timescale as the variation in excess tooth wear. However, the Lake Tutira drainage basin is not the same as the Wairarapa and Whanganui drainage basins where tooth wear studies were conducted. Therefore, these observations are not appropriately matched in space–time. Our use of the 2004 February rainstorm erosion signal as a single-event proxy for the regional susceptibility of soils and soil parent material to erosion and its application to comparisons of coincident geography between tooth wear rates and erosion intensity might be questioned. The tooth wear study sites on the North Island of New Zealand occur in the same 15 km2 drainage for which suspended sediment yield was obtained, all are within the Manawatu-Whanganui (S and SE North Island), and all occur within the area affected by the February 2004 MORLE (multiple-occurrence regional landslide event). The Dickson Experimental Station in Canberra is a single study site; thus, there is no known geographic variation in tooth wear or ingested silica in domestic sheep of Australia. Yet geographic variation is observed in the routing mechanisms (wind and rainout) known as atmospheric dust flux. This study site has a complex relationship with the routing systems; it is downwind but upstream, and these routing systems recycle sediment particles in a fluvial-eolian interaction. The Murrumbidgee drains to the Murray River mouth, and the southeast Dust Path blows aerosol dust out over the South Pacific (Tasman Sea). The mechanism is fluvial-eolian interaction, much like we see today in the volcanic Katmai Peninsula of Alaska, and much like the evidence we find on the North Island of New Zealand. When we match changing rates of mammalian tooth evolution in the middle Ceno- zoic Sarmiento Formation of Patagonia with diatomaceous ooze in DSDP cores from the Malvinas Plateau, Argentine Basin, and the more distant records of phytoplankton productivity in the eastern South Atlantic and the Southern Ocean, we establish a space– time coincidence and assume the operation of a mechanism linking the upwind and downwind records of the developing West Wind Drift. 10.2 The metaphysics of causation 339

10.2.2 Individuation

I have taken a very general geographic coincidence between hypsodonty, aridlands, and dust storm frequency, and explored it through as many individual case studies as possible. I have dissected apart the details of the sediment cascades on oceanic islands as well as orographic islands. The book examines each case study in excruciating detail for clues as well as evidence. The independent case studies are both geographic as well as temporal, and coincidence is presented in both dimensions for as many of the case studies as possible. Each case, whether continent, oceanic island, or orographic island, reveals surprising new features and each of these are incorporated into a maturing understanding of the complexity of the interaction between surface processes and tooth wear and tooth shape evolution. Apparent failures of coincidence or association (e.g., in Australia, with regard to the contribution of surface processes to ingested silica) have been found insightful, and have led to an understanding of thresholds, unexpected processes, and critical variables, and these in turn have shaped the direction of inquiry. While each example is useful, each is limited in scope, and each is vulnerable to critical appraisal. Pieces of each complex puzzle will almost certainly tumble under critical scrutiny, but the whole, presented in entirety, may just survive, and hopefully lead to a growing understanding of the role of earth surface processes in mammalian tooth evolution.

10.2.3 Adicity

How many causal relata are there? In South American living mammals, we examined a host of causal agents in a multivariate ordination. A procedure for selecting the variables eliminated most of these, but left four. Three were continuous climate variables (not likely direct, but contributing agents), and after removing their association, a map of the remaining residual variation revealed geographic coincidence with sediment sources and a particular routing system. The global data seemed to confirm this, by coincident peaks at the same latitude bands where the same routing system prevails (dust storm frequency). In New Zealand, through my reading of the history of the study of excess tooth wear, I dismissed all the other suspected causal relata in favor of soil ingestion as the single common feature implicated by all. Soil ingestion is the common thread that is found, one way or another, in all suspected causes. I made a claim for historical primacy by arguing that soil ingestion was the first or original suspect. Sheep ranchers had many ideas initially. I wonder how old the rancher was who suggested soil ingestion? Had he seen ENSO storm-induced erosion before, where younger ranchers had no experience with this sort of erosion? In Australia, we systematically worked our way through a whole host of suspected influences or causes, and eliminated them, one-by-one, because of their lack of coincidence. We found only one, wet deposition, to be temporally coincident with high silica ingestion. However, this was also eliminated because it did not affect sheep 340 Summary and conclusions

grazing at the lowest densities. In the end, we settled on population density itself (stocking rate) as the best explanation of the observed pattern of variation in silica ingestion, and thereby imply that grazing pressure and behavior can be the cause of soil ingestion and tooth wear. It was painful to have to abandon such a beautiful example of a routing system, but the mechanism was invoked later to explain something unexpected, tooth size and tooth wear in aboriginal humans. At this point, tooth size or tooth mineral volume was substituted for crown height as the evolutionary structural expression of a response to high dust storm frequency in Australia. In this case, we are not dealing with the evolutionary addition of tooth mineral substance, but the evolutionary slowing of the rate of loss of mineral substance. The loss of tooth mineral substance has been a hallmark feature of tooth shape evolution in modern humans since the time of their divergence from australopithecine ancestry. In the Mediterranean, our search for a single cause to the many independent examples of the evolution of high tooth crowns was necessarily superﬁcial. Other explanations have been offered to explain the evolution of ever-growing incisors and high-crowned molars in Mediterranean mammalian herbivores. Here, eventually, one might hope for a better coupling of marine and terrestrial records, but the sporadic and relatively poorly dated fossils will hinder sorting through the possibly causal relata and impede any detailed rendering. In the Plio-Pleistocene of East Africa, tooth shape evolution in ungulates, contemporary terrestrial herbivores, and even australopithecines could be caused by many different things from diet to vegetation, many of which have been investigated using microwear and an improved understanding of the physical properties of foods. I have examined this record in some detail, and humbly proffer a new interpretation to the certain delight of the wolves, jackels, and hyenas of paleoanthropology. Good hunting!

10.2.4 Connection

What is the connection or pathway of causation? Most of our examples of cause and effect are not sequential, but simultaneous at the levels of resolution available to us. We are trying to explain dental senescence, the wear accumulated over a lifetime. We are not examining the contribution of each ingested mineral particle to the tooth wear produced with each mandible adduction cycle. We assume ingestion and wear have this relationship. We are also invoking a process, erosion, that is happening around us all the time. When its intensity varies, at all timescales, it is associated with effects that are also assumed to have a cause–effect relationship. In essence, this is the problem of the smoking gun. For this thesis, the smoking gun is the sediment cascade and routing system, the pathway of mineral particles from their source in processes of generation (volcanism and glaciation), through their detachment and transport to temporary deposition in intermediate basins, and ﬁnal repose on the deep sea-ﬂoor. Where we have been able to couple marine and terrestrial records, and where we can piece together the elements of the routing system and its intensity, we can make the connection to tooth wear and tooth shape evolution. 10.2 The metaphysics of causation 341

10.2.5 Direction

The direction is sometimes obscure, because what we observe appears to be simultaneous. Mass accumulation rates of sea-floor sediments are causally unrelated to tooth shape evolution, and yet they are essentially simultaneous. In fact, they are joint effects of a common cause. I claim that this cause is sediment particle flux, or a particular detour of part of the stream of a sediment cascade, the part that briefly passes between occlusing teeth and through the herbivore digestive system. Many will not like the lack of an experimental demonstration of cause and effect, because only such a presentation would complete the etiology. What my explanation does, is make this demonstration an imperative. Let us say that we did the experiment, and it turned out to be true, that soil ingestion causes excess tooth wear. Despite the fact that this has been amply demonstrated by Healy, Rudge, and others, what would be gained by an experiment? Would the idea garner more laboratory-coated adherents, and would this matter? The direction of causation seems very clear at ecological timescales. The direction of the evolutionary response also seems comprehensible. The response is discontinuous in time and often delayed. The direction of evolutionary change can slow, and can reverse. In the case of tooth size evolution in modern humans, the loss of tooth mineral substance and decreasing tooth size is well documented. In Australian aboriginals and Oceanic people living along the Andesite Line, surface processes must be invoked to explain a slowing down of an evolutionary trend of diminishing tooth size. Of course, this could be explained by food, behavior (digging), or any of a myriad different causes. However, as large tooth size in modern humans is almost always associated with people living and foraging outdoors in or near dust source areas, we reject other agency. Another way the direction of causation can reverse is after the evolution of ever- growing tooth crowns when mammalian herbivores become significant engines of erosion.

10.2.6 Selection

Finally, we must distinguish sequences that involve the cause from those that involve mere conditions. It is the operation of earth surface processes that generates the conditions; the cause is the abrasion of ingested mineral particles that are mobilized by surface processes. We examined an example from Australia and discovered that our preferred mechanism was unnecessary to explain the observed soil ingestion and tooth wear. All the details about earth surface processes merely describe the conditions under which the animals lived during the study, they did not explain the observed pattern of tooth wear. Similarly, in Plio-Pleistocene East Africa, we examined the track of many environmental conditions, and learned that some of them do not serve to explain the evolutionary patterns of tooth shape evolution. In the middle Cenozoic of Patagonia, we examined everything we could about the prevailing conditions through the lens of earth surface processes and found some cherished features of the past are unrelated to the precocious evolution of hypsodonty. 342 Summary and conclusions

10.3 The past and prospects for the future

10.3.1 Why was this not noticed before?

This is a good question. Disciplinary boundaries, inexcusably poor scholarship leading to blind belief in mistaken causes, specious equivalences between modern and past high-wear environments might be considered. Modern high-wear environments, while rare, are insightful, but may be inappropriate and misleading about the prevalence and intensity of high-wear environments in the past. The reason we have not noticed the relationship between tooth wear and soil erosion is that we have not looked. Our practice in zoology, botany, and geomorphology intentionally ignores the presence of soil or mineral particles in stomach contents, the soil load on plant surfaces, and the interaction of herbivores with the land surface. We always wash our specimens, and wash away any adhering soil as contaminants that cloud our view of biology. The only scientists who have seen it are the few who are concerned about the soil ingestion pathway and our growing body burden of radionuclides and other toxins. These scientists have the most sophisticated theory and their models parameterize soil ingestion, soil load on plants, and the climate controls on particle flux. Our experience is also colored by the fact that we live in very benign times, the best of the Holocene, when dust flux to the polar ice caps is essentially nil. Yet ice cores demonstrate that most of the Pleistocene witnessed much higher atmospheric dust flux. Nevertheless, of course, we do not know what these high fluxes might have meant for soil ingestion or tooth wear. In addition, we are insulated from the hostility of the Earth by fossil fuels and shielded from atmospheric particle concentrations by buildings with air-conditioning. Imagine living in the world outside, and without benefit of fossil fuels. Firewood from forests enabled humans to populate severely seasonal environments and survive long cold winters, just as petroleum and other fossil fuels enable us to prosper, monopolize resources, and explore Antarctica. Yet another aspect of our detachment is our infatuation with catastrophy. Our fixation on sensational events obscures our understanding of processes that operate almost imperceptibly in the present, but significantly at longer and evolutionary timescales. For example, volcanic eruptions are understood in terms of their mortality at ecological timescales, not as sources for the accumulation of volcaniclastic deposits, or the role of ash accumulations to long-term average dust flux, soil ingestion and tooth surface abrasion, and consequences over evolutionary timescales. Most notions about the interplay of volcanism on life arise out of direct human experience (Sheets and Grayson, 1979). This experience conditions us to view volcanic eruptions as events, singular events or catastrophes that provoke disruption and horror at varying scales, depending on the energy of the eruption. The energy released at eruption determines the volume of the ejecta and the geographic scale of the influence of the ejecta. These variables, the volume of output and the geographic extent of the distributed ash, and the resulting patterns of destruction and mass mortality are the usual dimensions of discourse (Bullard, 1976; Sheets and Grayson, 1979). In ecology, our treatment of volcanism has also been oriented toward single eruption events and their 10.3 The past and prospects for the future 343

impact on flora and fauna. Ecologists note the curious heterogeneity of the consequences of eruption on different plant and animal species, and the dynamics of the resulting mass mortality. Documenting the consequences of singular events (Birks and Lotter, 1994) also dominates discourse in Quaternary paleoecology, and especially for mechanical abrasion and the premature senescence of the precision machines of our culture. Even in mammalian paleontology, when viewed at Cenozoic timescales, most treatments of the relationship between volcanism and mammalian evolution have also tended to concentrate on the trace left by single eruption events (Voorhies, 1985; Anderson et al., 1995; Cronin et al., 2000). In this study, we are not interested in single eruption events, but rather the history or historic trends in pyroclastic eruption, the definition of periods of volcanic activity, the reconstruction of the chronology of changing eruption intensities, and eruption styles through geologic time. I should point out that even at evolutionary timescales, single eruption events can be detected in the rock record, but just as single eruptions impact faunas episodically through mass mortality, it is difficult to imagine how longer- term trends in a tephrochronology might relate to mammalian evolution, particularly at temporal scales and temporal intervals that would appear in the fossil record as something other than a mass mortality or an extinction event. We therefore make a distinction between volcanism at ecological timescales and volcanism at evolutionary timescales. What is the difference? It is the difference between discrete events with expression in mortality and sustained or prolonged processes with expression as evolutionary rates. In other words, the difference between a volcanic eruption event that precipitates mass mortality and a prolonged period of pyroclastic volcanism, and/or the continuous erosion of ash accumulations, and the windborne transport of ash across the land surface. These are the mechanisms that contribute abrasive grit onto mammalian foods and thereby accelerate tooth wear, thus shortening the functional lifespan of the teeth, and shortening individual reproductive lifespan in a population-wide phenomenon, sustained over a period of time sufficient for natural selection to favor higher tooth crowns, and for such structures to evolve and such trends to be detected in the fossil mammal record. Why? Just as volcanism can be studied as either discrete single eruption events (at ecological timescales) or as periods of changing intensity through time (at evolutionary timescales), the windborne distribution of volcanic ash can also be studied at different temporal scales. Another way of explanation is, dust storms as single events versus periods of prolonged denudation and transport by wind, or alternating periods with and without dust storms, change through time in the frequency of windstorms, or change in the strength or prevailing direction of surface winds. Long after an eruption event, an episode of volcanic activity, or a prolonged period of volcanic ash production, the accumulated pyroclastic deposits can come under the influence of wind and wind erosion, and become reactivated, or actively transported and distributed through a landscape. Thus, there is a complex interaction between volcanic activity (or the production of ash deposits), the geographic distribution of ash accumulations, change in the vegetation cover and stratigraphic overburden that protect ash deposits from erosion, and the history of wind as the agent of erosion and transport. These interactions 344 Summary and conclusions

complicate the story. In addition to the evolutionary temporal scale of volcanic activity and changes in the occurrence and intensity of volcanic activity through geologic time, we are interested in broad patterns of change in the geography of volcanic activity.

10.3.2 If true, what should we be looking for?

Most objections invoke the lack of a smoking gun and involve probably unrealistic expectations about the analytical power to resolve unique microwear fabrics or mesowear resulting from phytolith and soil ingestion. We have learned that excess tooth wear, while cumulative, occurs seasonally and tooth wear varies from year to year with soil ingestion and the intensity of surface processes. Microwear suffers the “last supper” problem, but in addition, if evolutionarily signiﬁcant, cumulative wear is produced over an animal’s life but only during three months of each year, and varies from year to year (in some years wear from seasonal soil ingestion is nearly indistinguishable from background wear); should we look to microwear for evidence of causation? Assuming we could distinguish between the role of wear by phytoliths and diverse soil minerals, given the dimensions of variability in surface processes, what are the chances a herbivore tooth selected randomly from a population of sheep or a fossil assemblage will show soil mineral abrasion? Mesowear is thought to preserve evidence of more long-term average tooth wear, with high-wear environments associated with ﬂat occlusal relief and wear tables, and low-wear environments with high occlusal relief and irregular wear tables. Mesowear is known to vary with tooth shape and with animal age, and therefore, young adults of similar age in the same taxon are selected for description and comparison. Contrasting mesowear reliefs should not become manifest until after all permanent teeth are erupted. These sorts of comparisons have greater promise, but comprehensive studies of mesowear in large samples of many individuals of known age of the same species, from populations living in contrasting “wear environments” (or gradients of wear, whether temporal or spatial) are not known, to my knowledge. Do such samples exist? Have experimental studies been undertaken to demonstrate how long after a change in diet an individual will show contrasting mesowear relief?

10.3.3 What is reasonable to expect?

What would excess tooth wear look like in the fossil record? Heavily worn tooth crowns are more fragile and naturally more rare as fossils. Heavily worn m3s, or dental series with heavily worn m3s, are not common as fossils. Thus, excess tooth wear may not show up in the fossil record. While the evolutionary consequences of excess tooth wear appear in the fossil record (for instance, hypsodont tooth crowns), they are more likely to show up long after they evolved. That is to say, when they do appear in the fossil record, their evolution has already occurred. Except in exceptional circumstances, the fossil record may not reveal much about the process itself. After all, erosion removes sediment, and higher erosion rates remove sediment faster. Evidence of the highest erosion rates may be preserved downstream or downwind, but these records likely will 10.3 The past and prospects for the future 345

not preserve hypsodont teeth, and the upstream records that yield hypsodont teeth are scattered geographically and temporally ephemeral.

10.3.4 Apparently spurious relationships

Of course, some of the relationships I have developed here appear spurious. Why? Well, in part, they are outside our experience, but more important, the connection is not clear because it is not direct. Consider the plot of tooth wear on suspended sediment yield (Figure 4.12). The two variables do not appear to have any possible relationship to each other, and if they do (that is, if tooth wear is the effect, and sediment yield part of the causal cascade), the causal agent (the abrasive mineral particles) are not in direct contact with the tooth surface, and in fact, are being transported through the animal’s environment and away from it. Because some of this appears to be out of sequence, is this a spurious relationship? Moreover, the crux of causation occurs at the occluding surfaces of teeth, not downstream from them.

10.3.5 The future

Much of mammalian tooth shape evolution resides at the interface between the earth and life sciences, and geomorphology needs to be introduced into the study of evolutionary morphology. This has not yet been done. Resolution of the complexities, plausibility, and universality of the interaction between morphological evolution and geomorphology will require contributions from a wide variety of specialties, including volcaniclastic sedimentology, geomorphology, paleoceanography, mammalian functional morphology and paleontology, environmental paleobotany, radioecology, and isotope geochemistry. The universal currency should be mineral particle flux. At ecological timescales, soil ingestion explains variation in tooth wear rates and annual tooth wear rates are positively correlated with soil loss when expressed as mineral particle flux. In terrestrial environments, both direct soil ingestion and the soil load on plants may be significant, but are rarely distinguished. On islands, where rates of morphological evolution are high and the selection pressure imposed by the environment is unavoidable, variation in tooth wear rates appears to reflect the type and amount of soil exposed at the surface, and the agents that deliver soil to the herbivore. Erosion rates are high in tectonically active (orographic) areas with high relief, but are still higher in volcanic landscapes. At evolutionary timescales, the intensity of tectonism (mountain building and volcanism) and topographic complexity have high positive correlations with species richness, origination, and extinction rates, but the relationship between mountains, volcanoes, and the evolution of dental structures for resisting abrasion remains very poorly understood. Apart from the coincidences that suggest earth surface processes contribute to the evolution of hypsodonty, how this influence is exercised is also not well understood. Where fossil mammals are recovered from volcanic sediments and where a downwind record of erosion intensity is preserved in marine sediments, we find 346 Summary and conclusions

a remarkable correlation between rates of dental evolution and the intensity of erosion. The production and accumulation of volcanic ash provides a potential long-term source of mineral particle abrasives. Where earth surface processes deliver these abrasives into and through the herbivore environment, we find evidence of evolutionary response. In practical terms, how we convert downwind sediment accumulation rates on the sea- floor to atmospheric mineral particle flux and the intensity of surface erosion in the source area, and relate these to the evolution of hypsodonty, is the essence of the problem for geomorphology. Relating sediment accumulation on the sea-floor to the earth surface processes operating where herbivores live (and evolve), requires following mineral particles from their source to their ultimate sink. A particularly relevant example of the uniformitarian gulf between timescales is volcanism, a process that introduces some of the most abrasive mineral particles into the herbivore environment. Catastrophic volcanism can be overwhelming to herbivore populations, but the consequences of volcanic activity extend across all timescales. Mass mortality is virtually instantaneous in violent Plinian and sub-Plinian eruptions, whereas morbidity and mortality due to acute fluorosis through the consumption of windblown ash occurs over somewhat longer timescales (weeks and months). Conse- quences of an entirely different sort are manifest at even longer timescales. Years after an eruption, enamel lesions induced by soil fluoride ingestion can accelerate tooth deterioration and lead to structural failure and collapse, resulting in premature dental senescence. Over even longer timescales, accumulations of volcanic ash and windblown tephra become parent material for soils in which high micro-porosity, permeability, and incoherence make them susceptible to erosion. Erosion processes in both dry and wet climates deflate, remove, mobilize, and resuspend soil minerals of pyroclastic origin and transport them onto plant surfaces, from where they are ingested and accelerate tooth wear. To the extent premature dental senescence truncates herbivore reproductive lifespan, volcanism is potentiated to become significant over evolutionary timescales. The periodic or continuous erosion of tephra deposits accumulated over long periods of volcanic activity can sustain the earth surface processes that lead to deflation, mobilization, and ultimately, resuspension whereby pyroclastic abrasives come to adhere to the surface of forage plants. From this, it is not difficult to imagine change in the intensity of erosion over evolutionary timescales where natural selection shapes structural modifications of teeth that serve to prolong their functional longevity. If meaningful future tests of the plausibility of the idea are ever to be fashioned across disciplines so diverse, to serve the needs of research at both ecological and evolutionary timescales, much needs to be accomplished, including the construction of a mathematical model that describes the movement and fate of mineral particles originating from volcanic source areas, brought by routing systems into the herbivore environment and across herbivore tooth surfaces and through their digestive system, and finally to the ultimate accumulation as sediment on the sea-floor. Many components of such a model already exist. For example, the routing systems that deliver surface mineral particles into herbivores is best understood by the health physics community where radionuclide transfer from source to soil, onto plants, and ultimately through soil ingestion to herbivore tissues (for example, PATHWAY, GENII v2). Components to 10.3 The past and prospects for the future 347

be added to complete the models from radioecology might include; (1) geomorphology (the diffusion equation for volcanic edifices), (2) volcaniclastic sedimentology (fine- grained pyroclastic components of mass balance in terrestrial and marine basins), (3) functional morphology (the arrangement of enamel volume in the tooth crown and its delivery to the tooth wear surface), (4) earth surface processes (RUSLE for eolian systems dominated by the dust cycle in arid climates, and for fluvial systems where rainstorm-induced erosion dominates on hillslopes in wet climates), and (5) paleoceanography (time series analysis of the terrestrial dust and related biogenic and organic fractions of marine sediment cores). To test the universality of the idea, a research strategy and field protocol need to be developed for an integrated study of variation in surface soil loss, soil load on plants, soil ingestion, and tooth wear for feral ungulate populations on oceanic and orographic islands under diverse climate–erosion regimes. For this work, radionuclides may prove valuable for tracking soil loss, the transport of mineral particles as flux across the earth surface, soil ingestion by herbivores, and measuring tooth wear rates. This research would be designed to examine the universality of this new explanation for the evolution of tooth mineral volume and high tooth crowns by demonstrating the role of earth surface processes in tooth wear. In addition, this work may provide a more diverse empirical foundation for transfer factors in the soil ingestion pathway of radioisotope movement, and calibrate threshold values of mineral particle flux in coupled terrestrial and marine records that appear to be significant to evolutionary morphology. In particular, methods are required for measuring: (1) inadvertent soil ingestion by fecal ash and the separation of soil from phytoliths, acid-insoluble residue, and soil ingestion using indirect methods (titanium concentration and radioisotope tracers); (2) erosion or soil loss using fallout radiocesium, remote sensing methods of mapping soil erosion intensity and exposed soil, and historical approaches; (3) soil contamination of plant surfaces by ashing and washing, the use of soil markers (Sc, Ti, Pu, Pb, Cs), and a combination of ground-based Leaf Area Index with measures of soil mineral particle flux from soil loss; and (4) chronometric measures of tooth wear rates. References

Abbazzi, L., M. Benvenuti, G. Boschian, and S. Dominici, 1996. Revision of the Neogene and Pleistocene of the Gargano region (Apulia, Italy). The marine and continental succession and the mammal faunal assemblages in an area between Apricena and Poggio Imperiale (Foggia). Memorie della Società Geologica Italiana, 51:383–402. Abbazzi, L., F. Masini, and D. Torre, 1993. Evolutionary patterns in the first lower molar of the endemic murid Microtia. Quaternary International, 19:63–70. Abbott, I., N. Marchant, and R. Cranfield, 2000. Long-term change in the floristic composition and vegetation structure of Carnac Island, Western Australia. Journal of Biogeography, 27:333–346. Abbott, J. 1980. The distribution and cover of plant species on Carnac Island, Western Australia. Journal of the Royal Society of Western Australia, 63:39–45. Acosta, J., E. Ancochea, M. Canals, M.J. Huertas, and E. Uchupi, 2004. Early Pleistocene volcanism in the Emile Baudot Seamount, Balearic Promontory (western Mediterranean Sea). Marine Geology, 207:247–257. Addison, W.H.F. and J.L. Appleton Jr., 1915. The structure and growth of the incisor teeth of the albino rat. Journal of Morphology, 26:43–96. Agnolin, F.L. and N.R. Chimento, 2011. Afrotherian affinities for endemic South American “ungulates.” Mammalian Biology–Zeitschrift für Säugetierkunde, 76:101–108. Agrawal, V.C., 1967. Skull adaptations in fossorial rodents. Mammalia, 31:300–312. Agustí, J. and S. Moyà-Solà, 1990. Neogene–Quaternary mammalian faunas of the Balearics. Atti Convegni Lincei, Accademia Nazionale dei Lincei, 85:459–468. Albani, S., N.M. Mahowald, B. Delmonte, V. Maggi, and G. Winckler, 2012. Comparing modeled and observed changes in mineral dust transport and deposition to Antarctica between the Last Glacial Maximum and current climates. Climate Dynamics, 38:1731–1755. Alcover, J.A. and J. Agustí, 1985. Eliomys (Eivissia) canarreiensis n. gen. n. sp.; nou Glirid del Pleistoce de la cova de Ca Na Reia (Pitiuses). Endins,10–11:51–56. Alcover, J.A., B. Seguí, and P. Bover, 1999. Extinctions and local disappearances of vertebrates in the western Mediterranean islands. In MacPhee, R.D.E., ed., Extinctions in Near Time. New York, NY: Plenum Press, pp. 165–188. Alexander, R.D., J.L. Hoogland, R.D. Howard, K.M. Noonan, and P.W. Sherman, 1979. Sexual dimorphisms and breeding systems in pinnipeds, ungulates, primates and humans. In Chagnon, N.A. and W. Irons, eds., Evolutionary Biology and Human Social Behavior: an Anthropo- logical Perspective. Boston, MA: Duxbury Press, pp. 402–435. Ameghino, F., 1887. Enumeración sistemática de las especies de mamíferos fósiles coleccionados por Carlos Ameghino en los terranos eocenos de la Patagonia austral y depositados en el Museo La Plata. Boletin Museo de La Plata, 1:1–26.

348 References 349

Ameghino, F., 1897. Mammifères crétacés de l’Argentine: Deuxième contribution à la connais- sance de la faune mammalogique des couches à Pyrotherium. Boletín del Instituto Geográfico Argentino, 18:406–521. Ameghino, F., 1904. Investigaciones de morfología filogenética en los molares superiores de los ungulados. In Torcelli, A.J., ed., Obras Completas y Correspondencia Cientifica de Florentino Ameghino, vol. 14. La Plata (1933). Ameghino, F., 1906. Les Formations Sédimentaires du Crétacé supérieur en du Tertiare de Patagonie avec un paralléle entre leurs faunes mammalogiques et celles de l’ancien continent. Anales del Museo Nacional, Buenos Aires, 8:1–568. Anders, M.H., K.M. Gregory-Wodzicki, and M. Spiegelman, 2002. A critical evaluation of late tertiary accelerated uplift rates for the eastern Cordillera, central Andes of Bolivia. Journal of Geology, 110: 89–100. Anderson, B.C. and M.S. Bulgin, 1984. Starvation associated with dental disease in range ewes. Journal of the American Veterinary Medical Association, 184:737–738. Anderson, D.K., J. Damuth, and T.M. Bown, 1995. Rapid morphological change in Miocene marsupials and rodents associated with a volcanic catastrophe in Argentina. Journal of Verte- brate Paleontology, 15:640–649. Andreis, R.R., 1972. Paleosuelos en la Formacioń Musters (Eoceno medio), Laguna del Mate, provincia del Chubut, Republicá Argentina. Revista de la Asociacioń Argentina de Miner- alogia,́ Petrologiá y Sedimentología, 3:91–97. Andrews, C.W., 1915. A description of the skull and skeleton of a peculiarly modified rupicaprine antelope (Myotragus balearicus, Bate), with a notice of a new variety, M. balearicus var. major. Philosophical Transactions of the Royal Society of London, Series B, 206:281–305. Androver, R. and B. Angel, 1968. El proceso de masticación en el genero Myotragus. Boletin de la Sociedad de Historia Natural Baleares, 14:69–101. Anduaga, S. and G. Halffter, 1991. Escarabajos asociados a madrigueras de roedores (Coleoptera: Scarabaeidae, Scarabaeinae). Laboratorio Cienciometria, Información e Infor- mática Biológica (CIIB, Facultad de Ciencias, Universidad Nacional Autonoma de Mexico). Antoine, P.-O., L. Marivaux, D.A. Croft, et al., 2011. Middle Eocene rodents from Peruvian Amazonia reveal the pattern and timing of caviomorph origins and biogeography. Proceedings of the Royal Society London, B, Biological Sciences, 279: 1319–1326. Aragón, E., F.J. Goin, Y.E. Aguilera, et al., 2011. Palaeogeography and paleoenvironments of northern Patagonia from the Late Cretaceous to the Miocene: the Palaeogene Andean gap and the rise of the North Patagonian High Plateau. Biological Journal of the Linnean Society, 103:305–315. Aragón, E. and E.J. Romero, 1984. Geología, paleoambientes y paleobotánica de yacimientos Terciarios del occidente de Río Negro, Neuquén y Chubut. Actas del IX Congreso Geológico Argentino, San Carlos de Bariloche, 4:475–507. Arca, M. and C. Tuveri, 2006. La sezione di Paleontologia. In Ausilia Fadda, M., ed., Il Museo Archaeologico Nazionale di Nuoro, Collana Sardegna Archeologica, Serie “Guide e Itinerari” 17, Sassari, Carlo Delfino Editore, pp. 12–15. Ardolino, A., M. Franchi, M. Remesal, and F. Salani, 1999. La sedimentación y el volcanismo terciario en la Patagonia extraandina. 2. El volcanismo en la Patagonia extraandina. In Caminos, R., ed., Geología Argentina. Instituto de Geología y Recursos Minerales, Anales, Buenos Aires, 29:579–612. 350 References

Armstrong, P., 1982. Rabbits (Oryctolagus cuniculus) on islands: a case study of successful colonization. Journal of Biogeography, 9:353–362. Arnold, G.W., W.R. McManus, and I.G. Bush, 1964a. Studies in the wool production of grazing sheep. 1. Seasonal variation in feed intake, liveweight and wool production. Australian Journal of Experimental Agriculture and Animal Husbandry, 4:392–403. Arnold, G.W., W.R. McManus, and I.G. Bush, 1966. Studies in the wool production of grazing sheep. 5. Observations on teeth wear and carry over effects. Australian Journal of Experimental Agriculture and Animal Husbandry, 6:101–107. Arnold, G.W., W.R. McManus, I.G. Bush, and J. Ball, 1964b. The use of sheep fitted with oesophagal fistulas to measure diet quality. Australian Journal of Experimental Agriculture and Animal Husbandry, 4:71–79. Arnold, G.W., W.R. McManus, and M.L. Dudzinski, 1965. Studies in the wool production of grazing sheep. 3. Changes in efficiency of production. Australian Journal of Experimental Agriculture and Animal Husbandry,5:96–100. Arthur, W.J., III and A.W. Allredge, 1979. Soil ingestion by mule deer in northcentral Colorado. Journal of Range Management, 32:67–71. Asher, R., N. Bennett, and T. Lehmann, 2009. The new framework for understanding placental mammal evolution. Bioessays, 31:853–864. Asner, G.P. and R.E. Martin, 2011. Canopy phylogenetic, chemical and spectral assembly in a lowland Amazonian forest. New Phytologist, 189:999–1012. Asner, G.P., R.E. Martin, D.E. Knapp, et al., 2011. Spectroscopy of canopy chemicals in humid tropical forests. Remote Sensing of Environment, 115:3587–3598. Asner, G.P., J.M.O. Scurlock, and J.A. Hicke, 2003. Global synthesis of leaf area index observations: implications for ecological and remote sensing studies. Global Ecology and Biogeography, 12:191–205. Athens, J.S., 2009. Rattus exulans and the catastrophic disappearance of Hawaii’s native lowland forest. Biological Invasions, 11:1489–1501. Auld, T.D., 1990. Regeneration in populations of the arid zone plants Acacia carnei and A. oswaldii. In Saunders, D.A., A.J.M. Hopkins, and R.A. How, eds., Australian Ecosystems: 200 Years of Utilization, Degradation and Reconstruction. Proceedings of the Ecological Society of Australia, 65:267–272. Australian Academy of Science, 2006. Interview with Dr Alec Costin. [http://www.science.org. au/scientists/interviews/c/ac.html]. Avondo, M. and L. Lutri, 2004. Feed intake. In Pulina, G. and R. Bencini, eds., Dairy Sheep Nutrition. CABI, pp. 65–78. Aze, T., T.H.G. Ezard, A. Purvis, et al., 2011. A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data. Biological Reviews, 86:900–927. Azzaroli, A., 1981. Cainozoic mammals and the biogeography of the island of Sardinia, Eastern Mediterranean. Palaeogeography, Palaeoclimatology, Palaeoecology, 36:107–111. Badgley, C., 2010. Tectonics, topography, and mammalian diversity. Ecography, 33:220–231. Baker, B.H. and J.G. Mitchell, 1976. Volcanic stratigraphy and geochronology of the Kedong– Olorgesailie area and the evolution of the South Kenya rift valley. Journal of the Geological Society, 132:467–484. Baker, G., L.H.P. Jones, and I.D. Wardrop, 1959. Cause of wear in sheep’s teeth. Nature, 184:1583–1584. Baker, G., L.H.P. Jones, and I.D. Wardrop, 1961. Opal phytoliths and mineral particles in the rumen of the sheep. Australian Journal of Agricultural Research, 12:462–473. References 351

Baker, P.E., W.J. Rea, J. Skarmeta, R. Caminos, and D.C. Rex, 1981. Igneous history of the Andean Cordillera and Patagonian plateau around latitude 46dS. Philosophical Transactions of the Royal Society, Series A, Mathematical and Physical Sciences, 303:105–149. Baker, R.G., E.A. Bettis III, R.F. Denniston, et al., 2002. Holocene paleoenvironments in southeastern Minnesota–chasing the prairie-forest ecotone. Palaeogeography, Palaeoclimatology, Palaeoecology, 177:103–122. Balasse, M., A.B. Smith, S.H. Ambrose, and S.R. Leigh, 2003. Determining sheep birth seasonality by analysis of tooth enamel oxygen isotope ratios: the Late Stone Age site of Kasteelberg (South Africa). Journal of Archaeological Science, 30:205–215. Barker, P.F., P.J. Barrett, A.K. Cooper, and P. Huybrechts, 1999. Antarctic glacial history from numerical models and continental margin sediments. Paleogeography, Palaeoclimatology, Palaeoecology, 150:247–267. Barker, P.F., G.M. Filippelli, F. Florindo, E.E. Martin, and H.D. Scher, 2007. Onset and role of the Antarctic Circumpolar Current. Deep Sea Research Part II: Topical Studies in Ocean- ography, 54:2388–2398. Barker, P.F. and E. Thomas, 2004. Origin, signature and palaeoclimatic influence of the Antarctic Circumpolar Current. Earth-Science Reviews, 66:143–162. Barkla, J.W., P.J. Dilks, T.C. Greene, and R. Griffiths, 2008. Homalanthus polyandrous (Euphor- biaceae) on Macauley Island, southern Kermadec Islands, with notes on that island’s vascular flora. New Zealand Journal of Botany, 46:373–379. Barnicoat, C.R., 1947. Some results of surveys of the problems of wear in sheep’s teeth. Proceedings of the 10th Annual Meeting of Sheepfarmers, Massey College, Palmerston North, New Zealand, pp. 98–101. Barnicoat, C.R., 1957. Wear in sheep’s teeth. New Zealand Journal of Science and Technology, A38:583–632. Barnicoat, C.R., 1959. Wear in sheep’s teeth. VI. Chemical composition of teeth of grazing sheep. New Zealand Journal of Agricultural Research, 2:1025–1040. Barnicoat, C.R., 1963. Attrition of the hypsodont (sheep’s) tooth. In Sognnaes, R.F., ed., Mechanisms of Hard Tissue Destruction. Publication No. 75, American Association for the Advancement of Science, Washington DC, pp. 155–170. Barnicoat, C.R. and D.M. Hall, 1960. Attrition of incisors of grazing sheep. Nature, 185:179. Barreda, V.D. and L. Palazzesi, 2007. Patagonian vegetation turnovers during the Paleogene– Early Neogene: origin of arid-adapted floras. Botanical Review, 73:31–50. Barreda, V.D. and L. Palazzesi, 2010. Vegetation during the Eocene–Miocene interval in central Patagonia: a context of mammal evolution. In Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge, UK: Cambridge University Press, pp. 375–382. Barthram, G.T. and S.A. Grant, 1984. Defoliation of ryegrass-dominated swards by sheep. Grass and Forage Science, 39:323–331. Basher, L.R., 2000. Surface erosion assessment using 137Cs: examples from New Zealand. Acta Geologica Hispanica, 35:219–228. Batjes, N.H., 1997. A world dataset of derived soil properties by FAO-UNESCO soil unit for global modeling. Soil Use and Management, 13:9–16. Baudino, R., 1995. Evolution des Andes d’Equateur au Neogene: les enseignements de l’etude des basins intramontagneux. PhD Dissertation, L’Universite de Pau et des pays de l’Adour, Academie de Bordeaux No. 267. 352 References

Beadle, N.C.W., 1948. The Vegetation and Pastures of Western New South Wales with Special Reference to Soil Erosion. Soil Conservation Service, Sydney, Australia. Behrensmeyer, A.K., R. Potts, T. Plummer, et al., 1995. The Pleistocene locality of Kanjera, Western Kenya: stratigraphy, chronology and paleoenvironments. Journal of Human Evolution, 29:247–274. Bell, B.D. and R.H. Taylor, 1970. The wild sheep of Campbell Island. Forest and Bird Magazine, New Zealand Forest and Bird Protection Society, 178:6–10. Bell, D.H., 1976. High intensity rainstorms and geological hazards: Cyclone Alison, March 1975, Kaikoura, New Zealand. Bulletin of Engineering Geology and the Environment, 13:189–200. Bellosi, E.S., 2010a. Physical stratigraphy of the Sarmiento Formation (middle Eocene–early Miocene) at Gran Barranca, central Patagonia. In Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge, UK: Cambridge University Press, pp. 19–31. Bellosi, E.S., 2010b. Loessic and ﬂuvial sedimentation in Sarmiento Formation pyroclastics of the middle Cenozoic of central Patagonia. In Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge, UK: Cambridge University Press, pp. 278–292. Bellosi, E.S. and M.G. González, 2010. Paleosols of the Middle Cenozoic Sarmiento Formation, Central Patagonia. In Madden R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge, UK: Cambridge University Press, pp. 293–305. Bellosi, E.S., J.H. Laza, M.V. Sánchez, and J.F. Genise, 2010. Ichnofacies analysis of the Sarmiento Formation (middle Eocene–early Miocene) at Gran Barranca, central Patagonia. In Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge, UK: Cambridge University Press, pp. 306–316. Beresford, N.A. and B.J. Howard, 1991. The importance of soil adhered to vegetation as a source of radionuclides ingested by grazing animals. Science of the Total Environment, 107:237–254. Berg, J.G. and M.R. Johnston, 2003. Geology of the Wellington Area, 1:250,000 Geological Map, QMAP 10. Institute of Geological and Nuclear Sciences Ltd., Lower Hutt, New Zealand. Bergametti, G., L. Gomes, E. Remoudaki, et al., 1989. Present transport and deposition patterns of African dusts to the Northwestern Mediterranean. In Leinen, M. and M. Sarnthein, eds., Paleoclimatology and Paleometeorology: Modern and Past Patterns of Global Atmospheric Transport. New York, NY: Kluwer Academic Publishers, pp. 227–252. Berger, G.W., B.J. Pillans, and A.S. Palmer, 1992. Dating loess up to 800 ka by thermolumin- escence. Geology, 20:403–406. Bergqvist, L.P., E.A. Abrantes, and L. Dos Santos Avilla, 2004. The Xenarthra (Mammalia) of Sao José de Itaboraí Basin (upper Paleocene, Itaboraian), Rio de Janeiro, Brazil. Geodiversitas, 26:323–337. Bergstrom, D.M., A. Lucieer, K. Kiefer, et al., 2009a. Indirect effects of invasive species removal devastate World Heritage Island. Journal of Applied Ecology, 46:73–81. Bergstrom, D.M., A. Lucieer, K. Kiefer, et al., 2009b. Management implications of the Macquarie Island trophic cascade revisited: a reply to Dowding et al. (2009). Journal of Applied Ecology, 46:1133–1136. Berhanu, B., A.M. Melesse, and Y. Seleshji, 2013. GIS-based hydrological zones and soil geo- database of Ethiopia. Catena, 104:21–31. References 353

Bermúdez de Castro, J.M., M. Martinón-Torres, S. Sarmiento, et al., 2003. Rates of anterior tooth wear in Middle Pleistocene hominins from Sima de los Huesos (Sierra de Atapuerca, Spain). Proceedings of the US National Academy of Sciences, 100:11 992–11 996. Berry, E.W., 1925. A Miocene flora from Patagonia. Johns Hopkins University Studies in Geology, 6:185–252. Berry, E.W., 1928. Tertiary fossil plants from the Argentine Republic. Proceedings of the United States National Museum, 73:1–27. Berry, E.W., 1934. Miocene Patagonia. Proceedings of the National Academy of Sciences of the United States of America, 20:280–282. Berry, E.W., 1937. A Paleocene flora from Patagonia. Johns Hopkins University Studies in Geology, 12:33–50. Bertoldi de Pomar, H., 1970. Fitolitos y zoolitos: su significado geológico en sedimentos continentales. Boletin de la Asociación Geológica de Córdoba, 1:21–31. Bertoldi de Pomar, H., 1971. Ensayo de clasificación morfológica de los silicofitolitos. Ameghini- ana, 8:317–328. Bertoldi de Pomar, H., 1975. Los silicofitolitos: sinopsis de su conocimiento. Darwiniana, 19:173–206. Beyene, E.G., 2010. Geospatial Analysis to Study Environmental Change: Climate Variability and Vegetation Cover Dynamics in Ethiopia and the Horn of Africa. Dissertation, Fachbereich Geowissenschaften der Freien Universität Berlin, Berlin, Germany. Beynon, A.D., M.C. Dean, and D.J. Reid, 1991. On thick and thin enamel in hominoids. American Journal of Physical Anthropology, 86:295–309. Beynon, A.D. and B.A. Wood, 1986. Variations in enamel thickness and structure in East African hominids. American Journal of Physical Anthropology, 70:177–193. Bierwirth, P.N. and R.S. Brodie, 2008. Gamma-ray remote sensing of aeolian salt sources in the Murray-Darling Basin, Australia. Remote Sensing of the Environment, 112:550–559.

Bijl, P.K., A.J.P. Houben, S Schouten, et al., 2011. Transient Middle Eocene atmospheric CO2 and temperature variations. Science, 330:819–821. Bijl, P.K., S. Schouten, A. Sluijs, et al., 2009, Early Palaeogene temperature evolution of the southwest Pacific Ocean. Nature, 461:776–779. Billet, G., 2011. Phylogeny of the Notoungulata (Mammalia) based on cranial and dental characters. Journal of Systematic Paleontology, 9:481–497. Biondi, F., A. Gershunov, and D.R. Cayan, 2001a. North Pacific decadal climate variability since AD 1661. Journal of Climate, 14:5–10. Biondi, F., A. Gershunov, and D.R. Cayan, 2001b. Pacific Decadal Oscillation Reconstruction. International Tree-Ring Data Bank. IGBP PAGES/World Data Center for Paleoclimatology, Data Contribution Series #2001-001. NOAA/NGDC Paleoclimatology Program, Boulder CO [http://www.ncdc.noaa.gov/paleo/pubs/biondi2001/biondi2001.html]. Birks, H.J.B. and A.F. Lotter, 1994. The impact of Laacher See volcano (11,000 yr B.P.) on terrestrial vegetation and diatoms. Journal of Paleolimnology, 11:313–322. Bishop, L.C., 2010. Suoidea. In Werdelin, L. and W.J. Sanders, eds., Cenozoic Mammals of Africa. Berkeley, CA: University of California Press, pp. 821–842. Blanco, J.C. and R. Villafuerte, 1993. Factores ecológicos que influyen sobre las poblaciones de Conejos. Incidencia e la enfermedad hemorrágica. Technical Report 12081, Instituto Nacional para la Conservación de la Naturaleza, Ministerio de Agricultura, Pesca y Alimenta- cion, Madrid. 354 References

Bloemendal, J. and P.B. DeMenocal, 1989. Evidence for a change in the periodicity of tropical climate cycles at 2.4 Myr from whole-core magnetic susceptibility measurements. Nature, 342: 897–900. Bobe, R., A.K. Behrensmeyer, and R.E. Chapman, 2002. Faunal change, environmental variability and late Pliocene hominin evolution. Journal of Human Evolution, 42:475–497. Bobe, R. and G.G. Eck, 2001. Responses of African bovids to Pliocene climatic change. Paleobiology, 27:1–48. Bodmer, R.E., 1991. Influence of digestive morphology on resource partitioning in Amazonian ungulates. Oecologia, 85:361–365. Bohaty, S.M. and J.C. Zachos, 2003. Significant Southern Ocean warming event in the late middle Eocene. Geology, 31:1017–1020. Bohaty, S.M., J.C. Zachos, F. Florindo, and M.L. Delaney, 2009. Coupled greenhouse warming and deep-sea acidification in the middle Eocene. Paleoceanography, 24:PA2207. Bonaparte, J.F., 1990. New Late Cretaceous mammals from the Los Alamitos Formation, northern Patagonia. National Geographic Research, 6:63–93. Bond, M., A.A. Carlini, F.J. Goin, et al., 1995. Episodes in South American land mammal evolution and sedimentation: testing their apparent concurrence in a Palaeocene succession from central Patagonia. Actas del VI Congreso Argentino de Paleontología y Bioestratigrafía (Trelew), pp. 47–58. Bond, M. and G.M. López, 1993. El primer Notohippidae (Mammalia, Notoungulata) de la Formación Lumbrera (Grupo Salta) del Noroeste argentino: consideraciones sobre la sistemá- tica de la familia Notohippidae. Ameghiniana, 30:59–68. Bonino, N.A. and J.N. Amaya, 1984. Distribución geográfica y control del conejo silvestre europeo (Oryctolagus cuniculus) en la Argentina. Departamento de Documentación e Información, Instituto Nacional de Tecnología Agropecuaria INTA, Buenos Aires, IDIA, 429–432:25–50. Bonnefille, R., 2010. Cenozoic vegetation, climate changes and hominid evolution in tropical Africa. Global and Planetary Change, 72:390–411. Bonnefille, R. and U. Mohammed, 1994. Pollen-inferred climatic fluctuations in Ethiopia during the last 3000 years. Palaeogeography, Palaeoclimatology, Paleoecology, 109:331–343. Bonnefille, R., R. Potts, F. Chalié, D. Jolly and O. Peyron, 2004. High-resolution vegetation and climate change associated with Pliocene Australopithecus afarensis. Proceedings of the National Academy of Sciences of the United States of America, 101:12 125–12 129. Borgnia, M., A. Maggi, M. Arriaga, et al., 2006. Caracterización de la vegetación en la Reserva de Biósfera Laguna Blanca (Catamarca, Argentina). Ecología Australia, 16:29–45. Borgnia, M., B.L. Vilá, and M.H. Cassini, 2010. Foraging ecology of vicuna, Vicugna vicugna, in dry Puna of Argentina. Small Ruminant Research, 88:44–53. Bourke, C.A., 1998. The association of soil cobalt with the incidence of the “staggers” form of Phalaris aquatica poisoning in livestock. In Agronomy–Growing a Greener Future. Pro- ceedings of the 9th Annual Australian Agronomy Conference, Charles Sturt University, Wagga Wagga, NSW. Bover, P., 2004. Noves aportacions al coneixement del gènere Myotragus Bate, 1909 (Artiodac- tyla, Caprinae) de les Illes Balears. PhD Thesis, Universitat de les Illes Balears, Palma de Mallorca. Bover P. and J.A. Alcover, 1999. The evolution and ontogeny of the dentition of Myotragus balearicus Bate, 1909 (Artiodactyla, Caprinae): evidence from new fossil data. Biological Journal of the Linnean Society, 68:401–428. References 355

Bover, P and J.A. Alcover, 2003. Understanding late Quaternary extinctions: the case of Myotragus balearicus (Bate, 1909). Journal of Biogeography, 30:771–781. Bover, P., J. Quintana, and J.A. Alcover, 2008. Three islands, three worlds: paleogeography and evolution of the vertebrate fauna from the Balearic Islands. Quaternary International, 182:135–144. Bowman, I., 1916. The Andes of southern Peru: Geographical Reconnaissance along the Seventy-Third Meridian. American Geographical Society, New York. Boyde, A., 1979. Carbonate concentration, crystal centers, core dissolution, caries, cross striations, circadian rhythms, and compositional contrast in the SEM. Journal of Dental Research, Supplement, 58:981–983. Boyde, A., 1989. Enamel. In Berkovitz, B.K.B., A. Boyde, R.M. Frank, et al., eds., Teeth. Heidelberg, Germany: Springer–Verlag, pp. 309–473. Brace, C.L., 1980. Australian tooth-size clines and the death of a stereotype. Current Anthropology, 21:141–164. Brace, C.L., 1995. Biocultural interaction and the mechanism of mosaic evolution in the emergence of “modern” morphology. American Anthropologist, 97:711–721. Brace, C.L. and R.J. Hinton, 1981. Oceanic tooth-size variation as a reﬂection of biological and cultural mixing. Current Anthropology, 22:549–569. Brace, C.L., K.E. Rosenberg, and K.D. Hunt, 1987. Gradual change in human tooth size in the late Pleistocene and post-Pleistocene. Evolution, 41:705–720. Branford, D., D. Fowler, and M.V. Moghaddam, 2004. Study of aerosol deposition at a wind exposed forest edge using 210Pb and 137Cs soil inventories. Water, Air and Soil Pollution, 157:107–116. Braun, J.K., 1993. Systematic Relationships of the Tribe Phyllotini (Muridae: Sigmodontinae) of South America. Special Publication, Oklahoma Museum of Natural History, Norman, 50 pp. Bredenkamp, G.J., F. Spada, and E. Kazmierczak, 2002. On the origin of northern and southern hemisphere grasslands. Plant Ecology, 163:209–229. Breshears, D.D., J.J. Whicker, M.P. Johansen, and J.E. Pinder III, 2003. Wind and water erosion and transport in semi-arid shrubland, grassland and forest ecosystems: quantifying dominance of horizontal wind-driven transport. Earth Surface Processes and Landforms, 28:1189–1209. Breshears, D.D., J.J. Whicker, C.B. Zou, J.P. Field, and C.D. Allen, 2009. A conceptual framework for dryland aeolian sediment transport along the grassland–forest continuum: effects of woody plant canopy cover and disturbance. Geomorphology, 105:28–38. Brothers, R.N. and E.J. Searle, 1970. The geology of Raoul Island, Kermadec Group, Southwest Paciﬁc. Bulletin of Volcanology, 34:7–37. Brown, F.H., A.M. Sarna-Wojcicki, C.E. Meyer, and B. Haileab, 1992. Correlation of Pliocene and Pleistocene tephra layers between the Turkana Basin of East Africa and the Gulf of Aden. Quaternary International,13–14:55–67. Brown, L.R., 1978. The World-wide Loss of Croplands, Worldwatch Paper 24, 49 pp. Brown, L.R., 2006. Plan B 2.0: Rescuing a Planet Under Stress and a Civilization in Trouble, New York, NY: W.W. Norton and Company [www.earthpolicy.org/Books/PB2/index.htm) (su1)]. Bruere A.N., D.M. West, M.B. Orr, and M.W. O’Callaghan, 1979. A syndrome of dental abnormalities of sheep. I. Clinical aspects on a commercial sheep farm in the Wairarapa. New Zealand Veterinary Journal, 27:152–158. Bullard, F.M., 1976. Volcanoes of the Earth. Austin, TX: University of Texas Press. 356 References

Burkart, A., 1975. Evolution of grasses and grasslands in South America. Taxon, 24:53–66. Burleigh, R. and J. Clutton-Brock, 1980. The survival of Myotragus balearicus Bate, 1909, into the Neolithic on Mallorca. Journal of Archaeological Science, 7:385–388. Burnham, R.J. and K.R. Johnson, 2004. South American palaeobotany and the origins of neotropical rainforests. Philosophical Transactions of the Royal Society of London, B., 359:1595–1610. Busacca, A.J., H.M. Marks, and R. Rossi, 2001. Volcanic glass in soils of the Columbia plateau, Paciﬁc Northwest, USA. Soil Science Society of America Journal, 65:161–168. Butler, B.E., 1956. Parna, an aeolian clay. Australian Journal of Science, 18:145–151. Butler, B.E. and J.T. Hutton, 1956. Parna in the riverine plain of south-eastern Australia and the soils thereon. Australian Journal of Agricultural Research, 7:536–553. Butler, D.R., 1995. Zoogeomorphology: Animals as Geomorphic Agents. Cambridge, UK: Cam- bridge University Press. Butler, R.F., L.G. Marshall, R.E. Drake, and G.H. Curtis, 1984. Magnetic polarity stratigraphy and 40K-40Ar dating of late Miocene and early Pliocene continental deposits, Catamarca Province, NW Argentina. Journal of Geology, 92:623–636. Caloi, L. and M.R. Palombo, 1995. Functional aspects and ecological implications in Pleistocene endemic cervids of Sardinia, Sicily and Crete. Geobios, 28:247–258. Caminos, R., ed, 1999. Geología Argentina. Servicio Geologico Minero Argentina SEGEMAR, Anales, 29:1–796. Campagnucci, R.H., 2011. Atmospheric circulation over Patagonia from the Jurassic to present: a review through proxy data and climatic modeling scenarios. Biological Journal of the Linnean Society, 103:229–249. Campbell, K. and C.J. Donlan, 2005. Feral goat eradication on islands. Conservation Biology, 19:1362–1374. Campbell, R.N., 1974. St. Kilda and its sheep. In Jewell, P.A., C. Milner, and J. Morton Boyd, eds., Island Survivors: The Ecology of the Soay Sheep of St. Kilda. University of London, London, UK: Athlone Press. Campbell, S. and R. Mitchell, 2005. Dust Storms: Origins in Central Australia. Australian Aerosol Workshop, University of New South Wales, Sydney, Australia. Candela, A.M. and M.G. Vucetich, 2002. Hypsosteiromys (Rodentia, Hystricognathi) from the Early Miocene of Patagonia (Argentina), the only Erethizontidae with a tendency to hypsodonty. Geobios, 35:153–161. Carbajal, E., R. Pascual, R. Pinedo, S.A. Salﬁty, and M.G. Vucetich, 1977. Un nuevo mamifero de la Formación Lumbrera (Grupo Salta) de la comarca de Carahuasi (Salta, Argentina), edad y correlaciones. Publicaciones del Museo Municipal de Ciencias Naturales de Mar del Plata “Lorenzo Scaglia”, 2:148–163. Carlini, A.A., R. Pascual, and F.J. Goin, 2007. A new argyrolagid marsupial from the Early Miocene of Patagonia (Argentina). Neues Jahrbuch für Geologie und Paläontologie – Abhandlungen, 245(3):323–330. Carlini, A.A. and G.J. Scillato-Yané, 1998. Nuevos xenarthra del Friasense (Mioceno medio) de Argentina. Studia Geologica Salmanticensia, 34:43–67. Carrapa, B., D. Adelmann, G.E. Hilley, et al., 2005. Oligocene range uplift and development of plateau morphology in the southern central Andes. Tectonics, 24:19 pp. Carroll, R.L., 1988. Vertebrate Paleontology and Evolution. New York, NY: Freeman and Co. Casadio, S., ed, 1998. Paleógeno de America del Sur y de la Península Antártica. Asociación Paleontológica Argentina, Publicación Especial 5, Buenos Aires. References 357

Case, J.A., 1988. Paleogene floras from Seymour Island, Antarctic Peninsula. Memoirs of the Geological Society of America, 169:523–540. Cashman, K., E. Nicholson, A. Rust, and S. Gislason, 2013. Breaking magma: controls on magma fragmentation and ash formation. [http://www.unige.ch/sciences/terre/mineral/CERG/ Workshop2/Program/P-25_Cashman.pdf]. Cattle, S.R., G.H. McTainsch, and S. Elias, 2009. Aeolian dust deposition rates, particle-sizes and contributions to soils along a transect in semi-arid New South Wales, Australia. Sedimentology, 56:765–783. Caughley, G., 1971. Season of births for northern-hemisphere ungulates in New Zealand. Mammalia, 35:204–219. Cerdà, A. 1998. Relationships between climate and soil hydrological and erosional characteristics along gradients in Mediterranean limestone areas. Geomorphology, 25:123–134. Cerdeño, E. and B. Vera, 2010. Mendozahippus fierensis, gen. et sp. nov., new Notohippidae (Notoungulata) from the late Oligocene of Mendoza (Argentina). Journal of Vertebrate Paleontology, 30:1805–1817. Cerling, T.E., 1986. A mass-balance approach to basin sedimentation: constraints on the recent history of the Turkana basin. Palaeogeography, Palaeoclimatology, Palaeoecology, 54:63–86. Cerling, T.E., K.L. Chritz, N.G. Jablonski, M.G. Leakey, and F.K. Manthi, 2013. Diet of Theropithecus from 4 to 1 Ma in Kenya. Proceedings of the National Academy of Sciences of the United States of America, 110:10 507–10 512. Cerling, T.E., E. Mbua, F.M. Kirera, et al., 2011a. Diet of Paranthropus boisei in the early Pleistocene of East Africa. Proceedings of the National Academy of Sciences of the United States of America, 108:9337–9341. Cerling, T.E., J.G. Wynn, S.A. Andanje, et al., 2011b. Woody cover and hominin environments in the past 6 million years. Nature, 476:51–56. Chapuis, J.-L., Y. Frenot, and M. Lebouvier, 2004. Recovery of native plant communities after eradication of rabbits from the subantarctic Kerguelen Islands, and influence of climate change. Biological Conservation, 117:167–179. Chapuis, J.-L., V. Le Roux, J. Asseline, L. Lefèvre, and F. Kerleau, 2001. Eradication of rabbits (Oryctolagus cuniculus) by poisoning on three islands of the subantarctic Kerguelen Archipelago. Wildlife Research,28:323–331. Chen, X.Y., 2001. The red clay mantle in the Wagga Wagga region, New South Wales: evaluation of an aeolian dust deposit (Yarabee Parna) using methods of soil landscape mapping. Australian Journal of Soil Research, 39:61–80. Chen, X.Y., N.A. Spooner, J.M. Olley, and D.G. Questiaux, 2002. Addition of aeolian dusts to soils in southeastern Australia: red silty clay trapped in dunes bordering Murrumbidgee River in the Wagga Wagga region. Catena, 47:1–27. Chernet, T., W.K. Hart, J.L. Aronson, and R.C. Walter, 1998. New age constraints on the timing of volcanism and tectonism in the northern Main Ethiopian Rift-southern Afar transition zone (Ethiopia). Journal of Volcanology and Geothermal Research, 80:267–280. Chiba, M., M. Tsuruta, and K. Eto, 1973. A photographic method of measuring eruption rates of rat mandibular incisors. Archives of Oral Biology, 18:1003–1010. Chorn, B., 2012. Tephrochronology of the Lake Malawi Drill Cores: a Feasibility Study.MS Thesis, University of Minnesota, MN. Chornogubsky, L., 2011. New remains of the dryolestoid mammal Leonardus cuspidatus from the Los Alamitos Formation (Late Cretaceous, Argentina). Paläontologisches Zeitscrift, 85:343–350. 358 References

Cifelli, R.L., 1985. Biostratigraphy of the Casamayoran, Early Eocene, of Patagonia. American Museum Novitates, 2820:1–26. Cifelli, R.L., 1993. The phylogeny of the native South American ungulates. In Szalay, F.S., M.J. Novacek, and M.C. McKenna, eds., Mammalian Phylogeny, New York, NY: Springer-Verlag, pp. 195–216. Ciochon, R., D. Piperno, and R.G. Thompson, 1990. Opal phytoliths found on the teeth of the extinct ape Gigantopithecus blacki: implications for paleodietary studies. Proceedings of the National Academy of Sciences of the United States of America, 87:8120–8124. Cladera, G., E. Ruigomez, E. Ortiz-Jaureguizar, M. Bond, and G. López, 2004. Tafonomía de la Gran Hondonada (Formación Sarmiento, edad-mamífero mustersense, Eoceno Medio), Chubut, Argentina. Ameghiniana, 41:315–330. Clark, P.U., D. Archer, D. Pollard, et al., 2006. The middle Pleistocene transition: characteristics, mechanisms, and implications for long-term changes in atmospheric pCO2. Quaternary Science Reviews, 25:3150–3184. Clark, R.L., 1986. Pollen as a chronometer and sediment tracer, Burrinjuck Reservoir, Australia. Hydrobiologia, 143:63–69. Cleaveland, L.C. and T.D. Herbert, 2007. Coherent obliquity band and heterogeneous precession band responses in early Pleistocene tropical sea surface temperatures. Paleoceanography, 22: PA2216. Clemens, S.C., 1998. Dust response to seasonal atmospheric forcing: proxy evaluation and calibration. Paleoceanography, 13:471–490. Clemens, S.C., D.W. Murray, and W.L. Prell, 1996. Nonstationary phase of the Plio-Pleistocene Asian Monsoon. Science, 274:943–948. Clemens, S.C. and W.L. Prell, 1990. Late Pleistocene variability of Arabian Sea summer monsoon winds and continental aridity: eolian records from the lithogenic component of deep-sea sediments. Paleoceanography,5:l09–145. Clemens, S.C. and W.L. Prell, 1991a. One million year record of summer monsoon winds and continental aridity from the Owen Ridge (Site 722), northwest Arabian Sea. In Prell, W.J. and N. Niitsuma,eds., Shipboard Scientific Party, Proceedings of the Ocean Drilling Program, Scientific Results, 117:365–388. Clemens, S.C. and W.L. Prell, 1991b. Late Quarternary forcing of Indian Ocean summer – monsoon winds: a comparison of Fourier model and general circulation model results. Journal of Geophysical Research Atmospheres 96(D12):22 683–22 700. Clutton-Brock, T. and J. Pemberton, eds., 2004. Soay Sheep: Dynamics and Selection in an Island Population. Cambridge UK: Cambridge University Press, 383 pp. Coale, K.H., K.S. Johnson, F.P. Chavez, et al., 2004. Southern Ocean iron enrichment experiment: carbon cycling in high- and low-Si waters. Science, 304: 408–414. Coltorti, M., L. Abbazzi, M.P. Ferretti, et al., 2007. Last glacial mammals in South America: a new scenario from the Tarija Basin (Bolivia). Naturwissenschaften, 94:288–299. Coman, B., 1999. Tooth and Nail: The story of the Rabbit in Australia. Melbourne, Australia: Text Publishing. Condon, R.W. and M.E. Stannard, 1956. Erosion in western New South Wales: I. General description of the Western Division. Journal of the Soil Conservation Service of NSW, 12:192–202. Conticelli, S., R.W. Carlson, E. Widom, and G. Serri, 2007. Chemical and isotopic composition (Os, Pb, Nd, and Sr) of Neogene to Quaternary calc-alkalic, shoshonitic, and ultrapotassic mafic rocks from the Italian peninsula: inferences on the nature of their mantle sources. In Beccaluva, L., G. Bianchini, and M. Wilson, eds., Cenozoic Volcanism in the Mediterreanean Area. Geological Society of America Special Paper, 418:171–202. References 359

Cook, B.I., R.L. Miller, and R. Seager, 2009. Amplification of the North American “Dust Bowl” drought through human-induced land degradation. Proceedings of the National Academy of Sciences of the United States of America, 106:4997–5001. Cooke, B.D., 1987. The effects of rabbit grazing on regeneration of Sheoaks, Allocasuarina verticillata, and Saltwater Ti-trees, Melaleuca halmaturorum, in the Coorong National Park, South Australia. Australian Journal of Ecology, 13:11–20. Cooper, J. and R.K. Brooke, 1982. Present and past distribution of the feral European rabbit (Oryctolagus cuniculus) on southern African offshore islands. Suid-Afrikaanse Tydskrif Natuurwetenskap en Tegnologie, 12:71–75. Copson, G. and J. Whinam, 1998. Response of vegetation on subantarctic Macquarie Island to reduced rabbit grazing. Australian Journal of Botany, 46:15–24. Cordy, J.-M. and S. Ginesu, 1994. Fiume Santo (Sassari, Sardaigne, Italie): un nouveau gisement à Oréopithèque (Oreopithecidae, Primates, Mammalia). Comptes rendus de l’Académie des sciences. Série 2. Sciences de la terre et des planètes, 318:697–703. Cortese, G. and R. Gersonde, 2008. Plio/Pleistocene changes in the main biogenic silica carrier in the Southern Ocean, Atlantic Sector. Marine Geology, 252:100–110. Costin, A.B. and D.M. Moore, 1960. The effects of rabbit grazing on the grasslands of Macquarie Island. Journal of Ecology, 48:729–732. Coxall, H.K., P.A. Wilson, H. Pälike, C.H. Lear, and J. Backman, 2005. Rapid stepwise onset of Antartic glaciation and deeper calcite compensation depth in the PacificOcean.Nature, 433:53–57. Coyne, P., 1981. An extreme example of the effects of feral animals. Australian Ranger Bulletin,1:28–29. Coyne, P., 2010. Ecological rebound on Phillip Island, South Pacific. Ecological Management and Restoration, 11:4–15. Crawley, M.J., 1983. Herbivory: the Dynamics of Animal–Plant Interactions. Oxford, UK: Blackwell Scientific Publications. Crawley, M.J., 1997. Plant–herbivore dynamics. In Crawley, M.J., ed., Plant Ecology, Oxford, UK: Blackwell Scientific Publications, pp. 401–474. Cremaschi, M. and F. Ferraro, 2007. The upper Pleistocene in the Paglicci cave (Gargano, southern Italy): loess and tephra in the anthropogenic sequence. Atti Societa Toscana di Scienze Naturali, Memoria, Serie A, 112:153–163. Cristini, L., K. Grosfeld, M. Butzin, and G. Lohmann, 2012. Influence of the opening of the Drake Passage on the Cenozoic Antarctic Ice Sheet: a modeling approach. Palaeogeography, Palaeoclimatology, Palaeoecology, 339:66–73. Crocker, R.L., 1946. Post-Miocene Climatic and Geologic History and its Significance in Rela- tion to the Genesis of the Major Soil Types of South Australia. Melbourne: CSIRO. Croft, D.A., 2007. The middle Miocene (Laventan) Quebrada Honda fauna, southern Bolivia and a description of its notoungulates. Paleontology, 50:277–303. Croft, D.A., F. Anaya, D. Auerbach, C. Garzione, and B.J. MacFadden, 2009. New data on Miocene Neotropical provinciality from Cerdas, Bolivia. Journal of Mammalian Evolution, 16:175–198. Croft, D.A., M. Bond, J.J. Flynn, M. Reguero, and A.R. Wyss, 2003. Large archaeohyracids (Typotheria, Notoungulata) from Central Chile and Patagonia, including a revision of Archae- otypotherium. Fieldiana, Geology, new series, 49, 38 pp. Cronin, S.J., V. Manoharan, M.J. Hedley, and P. Loganathan, 2000. Fluoride: a review of its fate, bioavailability, and risks of fluorosis in grazed-pasture systems in New Zealand. New Zealand Journal of Agricultural Research, 43:295–321. 360 References

Crossley, D.A., A. Jackson, J. Yates, and I.P. Boydell, 1998. Use of computed tomography to investigate cheek tooth abnormalities in chinchillas (Chinchilla laniger). Journal of Small Animal Practice, 39:385–389. Crozier, M.J., 2005. Multiple-occurrence regional landslide events in New Zealand: hazard management issues. Landslides, 2:247–256. Crozier, M.J., R.J. Eyles, S.L. Marx, J.A. McConchie, and R.C. Owen, 1980. Distribution of landslips in the Wairarapa hill country. New Zealand Journal of Geology and Geophysics, 23:575–586. Cumberland, K.B., 1944. High-country “run”: the geography of extensive pastoralism in New Zealand. Economic Geography, 20:204–220. Cumberland, K.B., 1947. Soil Erosion in New Zealand; A Geographic Reconnaissance, 2nd edn. Wellington, New Zealand: Whitcombe and Tombs. Cunningham, K.B., 1978. Erosion assessment in New Zealand mountains. Proceedings of the Conference of Erosion Assessment and Control, in New Zealand, Christchurch, New Zealand Association of Soil Conservators, pp. 272–284. Cunningham, K.B., 1979. A century of change in the forests of the Ruahine Range, North Island, New Zealand, 1879–1970. New Zealand Journal of Ecology, 2:11–20. Cutress, T.W. and W.B. Healy, 1965. Wear of sheep’s teeth. II. Effects of pasture juices on dentine. New Zealand Journal of Agricultural Research, 8:753–762. Dahl, A.L., 1986–2004. United Nations Environment Programme–Island Directory 1998 [http://islands.unep.ch/isldir.htm]. Dalldorf, G. and C. Zall, 1930. Tooth growth in experimental scurvy. Journal of Experimental Medicine, 52:57–64. Damuth, J., P. Andrews, C. Badgley, et al., 1998. Habitat and climate inference from the structure of mammal communities. National Center for Ecological Analysis and Synthesis, Santa Barbara, CA [http://www.nceas.ucsb.edu/fmt/doc?/nceas-web/results/projects/98DAMUT1]. Damuth, J.D. and B.J. MacFadden, eds., 1990. Body Size in Mammalian Paleobiology: Estima- tion and Biological Implications. Cambridge, UK: Cambridge University Press. Dangler, E.W. and S.A. El-Swaify, 1976. Erosion of selected Hawaii soils by simulated rainfall. Soil Science Society of America Journal, 40:769–773. Dare-Edwards, A.J., 1984. Aeolian clay deposits of south-eastern Australia: parna or loessic clay? Transactions of the Institute of British Geographers, new series, 9:337–344. Dart, R.C., K.M. Barovich, and D. Chittleborough, 2005. Pedogenic carbonates, strontium isotopes and their relationship with Australian dust processes. In Roach, I.C., ed., Regolith 2005: Ten Years of CRC LEME. Proceedings of the CRCLEME Regional Regolith Symposia, Cooperative Research Centre for Landscape Environments and Mineral Exploration (Australia) CRC LEME, pp. 64–66. Darwin, C.R., 1842. The Structure and Distribution of Coral Reefs. Being the First Part of the Geology of the Voyage of the Beagle, Under the Command of Capt. Fitzroy, R.N. During the Years 1832 to 1836. London, UK: Smith Elder and Co. Dávila, F.M. and R.A. Astini, 2007. Cenozoic provenance history of synorogenic conglomerates in western Argentina (Famatina belt): implications for Central Andean foreland development. Geological Society of America Bulletin, 119: 609–622. De Astis, G., P.D. Kempton, A. Peccerillo, and T.W. Wu, 2006. Trace element and isotopic variations from Mt. Vulture to Campanian volcanoes: constraints for slab detachment and mantle inﬂow beneath southern Italy. Contributions to Mineralogy and Petrology, 151:331–351. References 361

De Celles, P., B. Carrapa, and G. Gehrels, 2007. Detrital zircon U-Pb ages provide provenance and chronostratigraphic information from Eocene synorogenic deposits in northwestern Argentina. Geology,35(4):323–326. De Conto, R.M. and D. Pollard, 2003. Rapid Cenozoic glaciation of Antarctica induced by

declining atmospheric CO2. Nature, 421:245–249. De Iuliis, G., D. Brandoni, and G.J. Scillato-Yané, 2008. New remains of Megathericulus patagonicus Ameghino, 1904 (Xenarthra, Megatheriidae): information on primitive features of megatheriines. Journal of Vertebrate Paleontology, 28:181–196. De Kauwe, M.G., M.I. Disney, T. Quaife, P. Lewis, and M. Williams, 2011. An assessment of the MODIS collection 5 leaf area index product for a region of mixed coniferous forest. Remote Sensing of Environment, 115:767–780. De Lisle, J.F., 1965. The climate of the Auckland Islands, Campbell Island, and Macquarie Island. Proceedings of the New Zealand Ecological Society, 12:37–44. De Martonne, E., 1941. Nouvelle carte mondiale de l’indice s’aridité. Météorologie, 1941:3–26. Dean, M.C., 1995. The nature and periodicity of incremental lines in primate dentine and their relationship to periradicular bands in OH 16 (Homo habilis). In Moggi-Cecchi, J, ed., Struc- ture, Function and Evolution of Teeth. Ninth International Symposium on Dental Morphology. International Institute for the Study of Man, Florence, Italy, pp. 239–265. Dean, M.C., A.D. Beynon, D.J. Reid, and D.K. Whittaker, 1993. A longitudinal study of tooth growth in a single individual based on long- and short-period incremental markings in dentine and enamel. International Journal of Osteoarchaeology, 3:249–264. Del Grosso, S., W. Parton, T. Stohlgren, et al., 2008. Global potential net primary production predicted from vegetation class, precipitation, and temperature. Ecology, 89:2117–2126. Del Papa, C., A. Kirschbaum, J. Powell, et al., 2010. Sedimentological, geochemical and paleontological insights applied to continental omission surfaces: a new approach for reconstructing an Eocene foreland basin in NW Argentina. Journal of South American Earth Sciences, 29:327–345. Del Río, C.J., 2004. Tertiary marine molluscan assemblages of eastern Patagonia (Argentina): a biostratigraphic analysis. Journal of Paleontology, 78:1097–1122. Delmonte, B., I. Basile-Doelsch, J.-R. Petit, et al., 2004. Comparing the Epica and Vostok dust records during the last 220,000 years: stratigraphical correlation and provenance in glacial periods. Earth-Science Reviews, 66:63–87. Delsuc, F., S.F. Vizcaino, and E.J.P. Douzery, 2004. Influence of Tertiary paleoenvironmental changes on the diversification of South American mammals: a relaxed molecular clock study within xenarthrans. BMC Evolutionary Biology, 4:11. De Menocal, P.B., 1995. Plio-Pleistocene African climate. Science, 270:53–60. De Menocal, P.B., 2004. African climate change and faunal evolution during the Pliocene- Pleistocene. Earth and Planetary Science Letters, 220:3–24. De Menocal, P.B. and F.H. Brown, 1999. Pliocene tephra correlations between East African hominid localities, the Gulf of Aden, and the Arabian Sea. In Agusti, J., L. Rook, and P. Andrews, eds., Hominid Evolution and Climatic Change in Europe. Cambridge, UK: Cambridge University Press, pp. 23–54. De Menocal, P.B., J. Bloemendal, and J. King, 1991. A rock-magnetic record of monsoonal dust deposition in the Arabian Sea: evidence for a shift in the mode of deposition at 2.4 Ma. Proceedings of the Ocean Drilling Program, Scientific Results, 117:389–407. Deniz, E. and S. Payne, 1982. Eruption and wear in the mandibular dentition as a guide to ageing Turkish Angora goats. In Wilson, B., C. Grigson, and S. Payne, eds., Ageing and Sexing 362 References

Animal Bones from Archaeological Sites. British Archaeological Reports, British Series 109, Oxford, UK, pp. 155–205. Deschamps, C.M., A.I. Olivares, E.C. Vieytes, and M.G. Vucetich, 2007. Ontogeny and diversity of the oldest capybaras (Rodentia: Hydrochoeridae; late Miocene of Argentina). Journal of Vertebrate Paleontology, 27:683–692. Devendra, C., 1981. The utilization of forages from cassava, pigeon pea, leucaena and ground- nut by goats and sheep in Malaysia. In Morand-Fehr, I.P., A. Boutlouse, and M. de Simiane, eds., International Symposium on Nutrition and Systems of Goat Feeding,Tours,France, pp. 338–343. De Vos, J., 1979. The endemic Pleistocene deer of Crete. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series B, Palaeontology, Geology, Physics, Chemistry. Anthropology, 82:59–90. De Vos, J., 1984. The endemic Pleistocene deer of Crete. Verhandelingen der Koninklijke Nederlandse Akademie van Wetenschappen, Afd. Natuurkunde, 31:1–110. Dickau, R., B.S. Whitney, J. Iriarte, et al., 2013. Differentiation of neotropical ecosystems by modern soil phytolith assemblages and its implications for palaeoenvironmental and archaeological reconstructions. Review of Palaeobotany and Palynology, 193:15–37. Diekmann, B., D.K. Fütterer, H. Grobe, et al., 2003. Terrigenous sediment supply in the polar to temperate South Atlantic: land-ocean links of environmental changes during the Late Quaternary. In Wefer, G., S. Mulitza, and V. Ratimeyer, eds., The South Atlantic in the Late Quaternary: Reconstruction of Material Budgets and Current Systems. New York, NY: Springer-Verlag, pp. 375–399. Diekmann, B. and G. Kuhn, 2002. Sedimentary record of the mid-Pleistocene climate transition in the southeastern South Atlantic (ODP Site 1090). Palaeogeography, Palaeoclimatology, Palaeoecology, 182:241–258. Diester-Haass, L., K. Billups, D.R. Gröcke, et al., 2009. Mid-Miocene paleoproductivity in the Atlantic Ocean and implications for the global carbon cycle. Paleoceanography, 24: PA1209. Diester-Haass, L. and R. Zahn, 1996. Eocene-Oligocene transition in the southern ocean: history of water mass circulation and biological productivity. Geology, 24:163–166. Diester-Haass, L. and R. Zahn, 2001. Paleoproductivity increase at the Eocene-Oligocene climatic transition: ODP/DSDP sites 763 and 592. Palaeogeography, Palaeoclimatology, Palaeoecology, 172:153–170. Dingle, R.V., S.A. Marenssi, and M. Lavelle, 1998. High latitude Eocene climate deterioration: evidence from the northern Antarctic Peninsula. Journal of South American Earth Science, 11:571–579. Di Sarra, A., M. Cacciani, J. DeLuisi, et al., 2003. Desert aerosol in the Mediterranean. In Bolle, H.-J., ed., Mediterranean Climate: Variability and Trends. Heidelberg, Germany: Springer, pp. 309–315. Domingue, B.M.F., D.W. Dellow, and T.N. Barry, 1991. The efﬁciency of chewing during eating and ruminating in goats and sheep. British Journal of Nutrition, 65:355–363. Domingue, B.M.F., D.W. Dellow, P.R. Wilson, and T.N. Barry, 1990. Comparative nutrition of deer, goats and sheep. Proceedings of the New Zealand Society of Animal Production, 50:39–42. Duckworth, J., R. Hill, D. Benzie, et al., 1962. Studies of the dentition of sheep. I. Clinical observations from investigations into the shedding of permanent incisor teeth by hill sheep. Research in Veterinary Science, 3:1–17. References 363

Dunbar, R.I.M. and U. Bose 1991. Adaptation to grass-eating in gelada baboons. Primates,32:1–7. Duncan, P., T.J. Foose, I.J. Gordon, C.G. Gakahu, and M. Lloyd, 1990. Comparative nutrient extraction from forages by grazing bovids and equids: a test of the nutritional model of equid/ bovid competition and coexistence. Oecologia, 84:411–418. Dunn, R.E., 2013. From Cells to Canopies: Reconstructing Vegetation Structure and its Reponse to Climate Change in the Middle Cenozoic of Patagonia Using Phytolith Morphology. PhD Dissertation, University of Washington, Seattle, WA. Dunn, R.E., R.H. Madden, M.J. Kohn, et al., 2013. A new chronology for middle Eocene–early Miocene South American Land Mammal Ages. Geological Society of America Bulletin, 125:539–555. Dusen, P., 1899. Über die tertiäre Flora der Magellansländer In Wissenschaften Ergebnisse Schwedische Expedizion nach den Magellansländer, 1895–1897. Geologische und Paläonto- logische. Upsalla: Archiv für Botanik, 1:1–27. Eck, G.G., 1977. Morphometric Variability in the Dentitions and Teeth of Theropithecus and Papio. PhD Dissertation, University of California, Berkeley, CA. Eck, G.G., 1993. Theropithecus darti from the Hadar Formation, Ethiopia. In Jablonski, N., ed., Theropithecus: The Rise and Fall of a Primate Genus. Cambridge, UK: Cambridge University Press, pp. 15–84. Eden, D.N. and M.J. Page, 1998. Palaeoclimatic implications of a storm erosion record from late Holocene lake sediments, North Island, New Zealand. Palaeogeography, Palaeoclimatology, Palaeoecology, 139:37–58. Eger, A., P.C. Almond, and L.M. Condron, 2012. Upbuilding pedogenesis under active loess deposition in a super-humid, temperate climate–quantification of deposition rates, soil chemistry and pedogenic thresholds. Geoderma, 189–190:491–501. Ehrmann, W.U., 1991. Implications for sediment composition on the southern Kerguelen Plateau for paleoclimate and depositional environment. In Barron, J., B. Larsen, and J.G. Baldauf, eds. Proceedings of the Ocean Drilling Project, Scientific Results, 119:185–210. Ekanayake, J.C. and C.J. Phillips, 1999. A model for determining thresholds for initiation of shallow landslides under near-saturated conditions in the East Coast region, New Zealand. New Zealand Journal of Hydrology, 38:1–28. Ellis, B.A., 1996. Microhabitat Selection and Dietary Habits of Rodents in the Endemic Zone of Argentine Hemorrhagic Fever. PhD Dissertation, Johns Hopkins University, Baltimore, MD. Ellis, B.A., J.N. Mills, E.J.T. Kennedy, J.I. Maiztegui, and J.E. Childs. 1994. The relationship among diet, alimentary tract morphology, and life history for five species of rodents from the central Argentine pampa. Acta Theriologica, 39:345–355. Elton, C., 1942. Voles, Mice and Lemmings: Problems in Population Dynamics. Oxford, UK: Clarendon Press, 496 pp. Emry, R.J., 1992. Mammalian range zones in the Chadronian White River Formation at Flagstaff Rim, Wyoming. In Prothero, D.R. and W.A. Berggren, eds., Eocene–Oligocene Climatic and Biotic Evolution. Princeton, NJ: Princeton University Press, pp. 106–115. Engelstaedter, S., K.E. Kohfeld, I. Tegen & S.P. Harrison, 2003. Controls of dust emissions by vegetation and topographic depressions: an evaluation using dust storm frequency data. Geophysical Research Letters, 30:27.1–27.4. Engesser, B., 1989. The late Tertiary small mammals of the Maremma region (Tuscany, Italy): 2nd Part. Muridae and Cricetidae (Rodentia, Mammalia). Bollettino della Societa Paleontologica Italiana, 28:227–252. 364 References

Eronen, J.T., K. Puolamäki, L. Liu, et al., 2010a. Precipitation and large herbivorous mammals, I: estimates from present-day communities. Evolutionary Ecology Research, 12:217–233. Eronen, J.T., K. Puolamäki, L. Liu, et al., 2010b. Precipitation and large herbivorous mammals, II: application to fossil data. Evolutionary Ecology Research, 12:235–248. Eshed, V., A. Gopher, and I. Hershkovitz, 2006. Tooth wear and dental pathology at the advent of agriculture: new evidence from the Levant. American Journal of Physical Anthropology, 130:145–159. Estrada, A. and G. Halffter, 1993. Dung beetles attracted to mammalian herbivore (Alouatta palliata) and omnivore (Nasua narica) dung in the tropical rain forest of Los Tuxtlas, Mexico. Journal of Tropical Ecology, 9:45–54. Eswaran, H., N. Bliss, D. Lytle, and D. Lammers, 1992. Map of major soil regions of the world 1:30,000,000. Evans, R., 1998. The erosional impacts of grazing animals. Progress in Physical Geography, 22:251–268. Eyles, G.O., 1983. The distribution and severity of present solid erosion in New Zealand. New Zealand Geographer, 39:12–28. Falkner, T., 1774. A Description of Patagonia and the Adjoining Parts of South America; Containing an Account of the Soil, Produce, Animals, Vales, Mountains, Rivers, Lakes, etc. of Those Countries (1935 facsimile edition). London, UK: Hereford. Fanning, P. 1994. Long-term contemporary erosion rates in an arid rangelands environment in western New South Wales, Australia. Journal of Arid Environments, 28:173–187. FAO, 1997. The Digital Soil and Terrain Database of East Africa (SEA), Version 1.0. Food and Agriculture Organization of the United Nations, Rome, Italy. FAO, 2001. Andosols. In Driessen, P., J. Deckers, O. Spaargaren, and F. Nachtergaele, eds., Lecture Notes on the Major Soils of the World. World Soil Resources Report 94. Rome, Food and Agriculture Organization of the United Nations. FAO, 2003. Map of World Soil Resources, Food and Agriculture Organization of the United Nations, Rome, Italy. FAO, 2006. In Grieser, J., R. Gommes, S. Coﬁeld, and M. Bernardi, eds., Data Sources for FAO World Maps of Koeppen Climatologies and Climatic Net Primary Production, Food and Agriculture Organization of the United Nations, Rome, Italy [http://www.fao.org/nr/climpag/ globgrids/KC_commondata_en.asp]. Favila, M.E. and G. Halffter, 1997. The use of indicator groups for measuring biodiversity as related to community structure and function. Acta Zoológica Mexicana, nueva serie, 72:1–25. Feakins, S.J., F.H. Brown, and P.B. deMenocal, 2007a. Plio-Pleistocene microtephra in DSDP site 231, Gulf of Aden. Journal of African Earth Sciences, 48:341–352. Feakins, S.J., P.B. De Menocal, and T.I. Eglinton, 2005. Biomarker records of late Neogene changes in northeast African vegetation. Geology, 33:977–980. Feakins, S.J., T.I. Eglinton, and P.B. DeMenocal, 2007b. A comparison of biomarker records of northeast African vegetation from lacustrine and marine sediments (ca 3.40 Ma). Organic Geochemistry, 38:1607–1624. Feakins, S.J., N.E. Levin, H.M. Liddy, et al., 2013. Northeast African vegetation change over 12 m.y. Geology, 41:295–298. Feibel, C.S., 1999. Tephrostratigraphy and geological context in paleoanthropology. Evolutionary Anthropology, 8:87–100. Ferigolo, J., 1985. Evolutionary trends of the histological pattern in the teeth of edentata (Xenarthra). Archives of Oral Biology, 30:71–82. References 365

Fernicola, J.C., S.F. Vizcaino, and G. De Iuliius, 2009. The fossil mammals collected by Charles Darwin in South America during his travels on board the HMS Beagle. Revista de la Asociación Geológica Argentina, 64:147–159. Ferris, D.G., J. Cole-Dai, A.R. Reyes, and D.M. Budner, 2011. South Pole ice core record of explosive volcanic eruptions in the ﬁrst and second millennia A.D. and evidence of a large eruption in the tropics around 535 A.D. Journal of Geophysical Research, 116, D17308. Finger, K.L., A. Encinas, and S.N. Nielsen, 2013. Comment on “Evidence for an early-middle Miocene age of the Navidad Formation (central Chile): paleontological, paleoclimatic and tectonic implications” of Gutiérrez et al. (Andean Geology, 2013;40:66–78). Andean Geology, 40:571–579. Fiol, Ll.A., J.J. Fornós, B. Gelabert, and J.A. Guijarro, 2005. Dust rains in Mallorca (Western Mediterrenaen): their occurrence and role in some recent geological processes. Catena,63:64–84. Fisher, D.C., 1994. Stratocladistics: morphological and temporal patterns and their relation to phylogenetic process. In Grande, L. and O. Rieppel, eds., Interpreting the Hierarchy of Nature. San Diego, CA: Academic Press, pp. 133–171. Flux, J.E.C. and P.J. Fullagar, 1992. World distribution of the rabbit Oryctolagus cuniculus on islands. Mammal Review, 22:151–205. Flynn, J.J., J. Guerrero, and C.C. Swisher III, 1997. Geochronology of the Honda Group. In Kay, R.F., R.H. Madden, R.L. Cifelli, and J.J. Flynn, eds., Vertebrate Paleontology in the Neo- tropics: the Miocene Fauna of La Venta, Colombia. Washington DC: Smithsonian Institution Press, pp. 44–60. Flynn, J.J., M.J. Novacek, H.E. Dodson, et al., 2002. A new fossil mammal assemblage from the southern Chilean Andes: implications for geology, geochronology, and tectonics. Journal of South American Earth Sciences, 15:285–302. Flynn, J.J. and A.R. Wyss, 1998. Recent advances in South American mammalian paleontology. Trends in Ecology and Evolution, 13:449–454. Flynn, J.J., A.R. Wyss, D.A. Croft, and R. Charrier, 2003. The Tinguiririca Fauna, Chile: biochronology, paleoecology, biogeography, and a new earliest Oligocene South American Land Mammal Age. Palaeogeography, Palaeoclimatology, Palaeoecology, 195:229–259. Forman, S.L., R. Oglesby, and R.S. Webb, 2001. Temporal and spatial patterns of Holocene dune activity on the Great Plains of North America: megadroughts and climate links. Global and Planetary Change, 29:1–29. Fornós, J.J., R.G. Bromley, L.B. Clemmensen, and A. Rodríguez-Perea, 2002. Tracks and trackways of Myotragus belearicus Bate (Artiodactyla, Caprinae) in Pleistocene aeolianites from Mallorca (Balearic Islands, Western Mediterranean). Palaeogeography, Palaeoclimat- ology, Palaeoecology, 180:277–313. Forsyth, D.M., D.A. Coomes, G. Nugent, and G.M.J. Hall, 2002. Diet and diet preferences of introduced ungulates (Order: Artiodactyla) in New Zealand. New Zealand Journal of Zoology, 29:323–343. Fortelius, M., 1985. Ungulate cheek teeth: developmental, functional, and evolutionary interrela- tions. Acta Zoologica Fennica, 180:1–76. Fowler, W.B. and W. Lopushinsky, 1986. Wind-blown volcanic ash in forest and agricultural locations as related to meteorological conditions. Atmospheric Environment, 20:421–425. Frailey, C.D. and K.E. Campbell Jr., 2004. Paleogene rodents from Amazonian Peru: the Santa Rosa Local Fauna. Natural History Museum of Los Angeles County, Science Series, 40:71–130. Frei, E., 1978. Andepts in some high mountains of East Africa. Geoderma, 21:119–131. 366 References

Frenguelli, J., 1930. Particulas de silice organizada en el loess y en los limos pampeanos. Celulas silicificadas de gramineas. Anales de la Sociedad Cientifica de Santa Fe, 2:65–109. Frenguelli, J., 1955. Loess y limos pampeanos. Universidad Nacional de La Plata, Facultad de Ciencias Naturales y Museo. Serie Técnica y Didáctica, 7:1–88. Freudenberg, W., 1914. Die Säugetiere des älteren Quartärs von Milleleuropa mit besonderer Berücksichtigung der Fauna von Hundsheim und Deutschaltenburg in Niederösterreich: nebst Bemerkungen über verwandle Formen anderer Fundorte. Geologische und Palaontologische Abhandlungen, 12, 219 pp., Gustav Fischer, Jena. Freudenthal, M., 1971. Neogene vertebrates from the Gargano Peninsula, Italy. Scripta Geo- logica, Leiden, 3:1–10. Freudenthal, M. 1976. Rodent stratigraphy of some Miocene fissure fillings in Gargano (prov. Foggia, Italy). Scripta Geologica, Leiden, 37:1–23. Freudenthal, M. 1986. Cricetidae (Rodentia) from the Neogene of Gargano (Prov. of Foggia, Italy). Scripta Geologica, Leiden, 77:29–76. Fricke, H.C. and J.R. O’Neil, 1996. Inter- and intra-tooth variation in oxygen isotope composition of mammalian tooth enamel phosphate: implications for palaeolimatological and palaeobio- logical research. Palaeogeography, Palaeoclimatology, Palaeoecology, 126:91–99. Friedel, M.H., 1985. The population structure and density of central Australian trees and shrubs and relationships to range condition, rabbit abundance and soil. Australian Rangelands Journal, 7:130–139. Fritzsche, F., W. Zech, and G. Guggenberger, 2007. Soils of the Main Ethiopian Rift Valley escarpment: a transect study. Catena, 70:209–219. Frost, S.R., 2001. Fossil Cercopithecidae from the Afar Depression, Ethiopia; Species Systematics and Comparisions to the Turkana Basin. PhD Dissertation, City University of New York, New York, NY. Frost, S.R., 2010. African Pliocene and Pleistocene cercopithecid evolution and global climatic change. In Bobé, R., Z. Alemseged, and A.K. Behrensmeyer, eds,. Hominin Environments in the East African Pliocene: An Assessment of the Faunal Evidence. Dordrecht, the Netherlands: Springer, pp. 51–76. Fullagar, P.J., 1978. Report on the rabbits on Philip Island, Norfolk Island. CSIRO Division of Wildlife Research, Canberra, Australia. Fuller, I.C., 2005. February floods in the lower North Island, 2004: catastrophe – causes and consequences. New Zealand Geographer, 61:40–50. Gali-Muhtasib, H.U., C.C. Smith, and J.J. Higgins, 1992. The effect of silica in grasses on the feeding behavior of the prarie vole, Microtus ochrogaster. Ecology, 73:1724–1729. Gallagher, M.W., E. Nemitz, J.R. Dorsey, et al., 2002. Measurements and parameterizations of small aerosol deposition velocities to grassland, arable crops, and forest: influence of surface roughness length on deposition. Journal of Geophysical Research, Atmospheres, 107(D12): AAC8-1-AAC8–10. Garnier, E., B. Shipley, C. Roumet, and G. Laurent, 2001. A standardized protocol for the determination of specific leaf area and leaf dry matter content. Functional Ecology,15:688–695. Garzione, C.N., G.D. Hoke, J.C. Libarkin, et al., 2008. Rise of the Andes. Science, 320:1304– 1307. Garzione, C.N., P. Molnar, J.C. Libarkin, and B.J. MacFadden, 2006. Rapid late Miocene rise of the Bolivian Altiplano: evidence for removal of mantle lithosphere. Earth and Planetary Science Letters, 241:543–556. Gasparini, Z., 1981. Los Crocodylia fósiles de la Argentina. Ameghiniana, 18:177–205. References 367

Gaudry, A., 1902. Recherches Paléontologiques de M. André Tournouër en Patagonie. Bulletin de la Société d’histoire Naturelle d’Autun, t XV:117–123. Gaudry, A., 1903. Ajoute les remarques suivantes ‘Sur la marche de l’évolution en Patagonie’. Bulletin de la Société Géologique de France, 3:473–474. Genise, J.F., E.S. Bellosi, and M.G. Gonzalez, 2004. An approach to the description and interpretation of ichnofabrics in palaeosols. Geological Society of London, Special Publica- tions, 228:355–382. Genise, J.F., M.G. Mángano, L.A. Buatois, J.H. Laza, and M. Verde, 2000. Insect trace fossil associations in paleosols: the Coprinisphaera ichnofacies. Palaios, 15:49–64. Gibb, J.A. and J.M. Williams, 1990. European rabbit. In King, C.M. ed., The Handbook of New Zealand Mammals. Oxford, UK: Oxford University Press, pp. 138–160. Gibbs, H.S., 1968. Volcanic-Ash Soils in New Zealand. New Zealand Department of Scientiﬁc and Industrial Research, Information Series, No. 65, 28 pp. Gibson, D.J., 2009. Grasses and Grassland Ecology. Oxford, UK: Oxford University Press. Gihad, E.A., 1976. Intake, digestibility and nitrogen utilization of tropical natural grass hay by goats and sheep. Journal of Animal Science, 43:879–883. Gihad, E.A., T.M. El-Bedawy, and A.Z. Mehrez, 1980. Fiber digestibility by goats and sheep. Journal of Dairy Science, 63:1701–1706. Gingerich, P.D., 1979. The stratophenetic approach to phylogeny reconstruction in vertebrate paleontology. In Cracraft, J. and N. Eldredge, eds., Phylogenetic Analysis and Paleontology. New York, NY: Columbia University Press, pp. 41–77. Ginoux, P., J.M. Prospero, O. Torres, and M. Chin, 2004. Long-term simulation of global dust distribution with the COCART model: correlation with North Atlantic Oscillation. Environ- mental Modeling and Software, 19:113–128. Glade, T.W., 1996. The temporal and spatial occurrence of landslide-triggering rainstorms in New Zealand. In Mäusbacher, R. and S. Schulte, eds., Barsch Festschrift, Heidelberger Geographische Arbeiten, 104:237–250. Glade, T.W., 1997. The Temporal and Spatial Occurrence of Rainstorm-Triggered Landslide Events in New Zealand. PhD thesis, Research School of Earth Science, Department of Geography, Victoria University of Wellington, Wellington, New Zealand, 343 pp. Glade, T.W., 1998. Establishing the frequency and magnitude of landslide-triggering rainstorm events in New Zealand. Environmental Geology, 35:160–174. Gliozzi, E. and A. Malatesta, 1980. The Quaternary goat of Capo Figari (Northeastern Sardinia). Geologica Romana, 19:295–347. Goin, F.J., M.A. Abello, and L. Chornogubsky, 2010. Middle Tertiary marsupials from central Patagonia (early Oligocene of Gran Barranca): understanding South America’s Grande Cou- pure. In Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., The Paleontology of Gran Barranca. Cambridge, UK: Cambridge University Press, pp. 69–105. Goldasteh, I., G. Ahmadi, and A. Ferro, 2012. A model for removal of compact, rough, irregularly shaped particles from surfaces in turbulent ﬂows. Journal of Adhesion,88:766–786. Gomez, B., L. Carter, and N.A. Trustrum, 2007. A 2400 yr record of natural events and anthropogenic impacts in intercorrelated terrestrial and marine sediment cores: Waipaoa sedimentary system, New Zealand. Geological Society of America Bulletin, 119:1415–1432. Gong, Y., J. Hodgson, M.G. Lambert, and I.L. Gordon, 1996. Short-term ingestive behaviour of sheep and goats grazing grasses and legumes. 1. Comparison of bite weight, bite rate, and bite dimensions for forages at two stages of maturity. New Zealand Journal of Agricultural Research, 39:63–73. 368 References

Gordon, I.J. and A.W. Illius, 1989. Resource partitioning by ungulates on the Isle of Rhum. Oecologia 79:383–389. Goudie, A.S. and N.J. Middleton, 1992. The changing frequency of dust storms through time. Climatic Change, 20:197–225. Gradstein, F., J. Ogg, M. Schmitz, and G. Ogg, eds., 2012. The Geologic Time Scale 2012. Amsterdam, the Netherlands: Elsevier BV. Graham, A., K.M. Gregory-Wodzicki, and K.L. Wright, 2001. Mio-Pliocene palynoflora from the Eastern Cordillera, Bolivia: implications for the uplift history of the Central Andean Plateau. American Journal of Botany, 88:1545–1557. Grange, L.I. and H.S. Gibbs, 1949. Soil erosion in New Zealand. Part 1. Southern half of North Island. New Zealand Soil Bureau Bulletin, new series, 1, 28 pp. Grant, A., 1938–9. Hawke’s Bay Flood, April 1938. Proceedings of the New Zealand Institute of Engineers, 25:55–64. Grant, A. 1982. The use of tooth wear as a guide to the age of domestic ungulates. In Wilson, B.C., C. Grigson, and S. Payne, eds., Ageing and Sexing Animal Bones from Archaeological Sites. Oxford, British Archaeological Reports, 109:91–108. Grant, P.L.J., 1965. Major regime changes of the Tukituki River, Hawkes’ Bay, since about 1650 A.D. Journal of Hydrology (New Zealand), 4:17–30. Grant, P.L.J., 1977. Recorded Channel Changes of the Upper Waipawa River, Ruahine Range, New Zealand. Water and Soil Technical Publication No. 6, Wellington, Ministry of Works and Development. Gregory, W.K., 1910. The orders of mammals. Bulletin of the American Museum of Natural History, 27:1–524. Gregory-Wodzicki, K.M., 2000. Uplift history of the Central and Northern Andes: a review. Bulletin of the Geological Society of America, 112:1091–1105. Gregory-Wodzicki, K.M., W.C. McIntosh, and K. Velasquez, 1998. Climatic and tectonic implications of the late Miocene Jakokkota flora, Bolivian Altiplano. Journal of South American Earth Sciences, 11:533–560. Griffin, M., 1991. Eocene bivalves from the Río Turbio formation, southwestern Patagonia (Argentina). Journal of Paleontology, 65:119–146. Griffin, M. and M.A. Hünicken, 1994. Late Cretaceous–Early Tertiary gastropods from southwestern Patagonia, Argentina. Journal of Paleontology, 68:257–274. Grigera, D.E. and E.H. Rapoport, 1983. Status and distribution of the European hare in South America. Journal of Mammalogy, 64:163–166. Grine, F.E., D.W. Krause, G. Fosse, and W.L. Jungers, 1987. Analysis of individual, intraspecific and interspecific variability in quantitative parameters of caprine tooth enamel structure. Acta Odontologica Scandinavica, 45:1–23. Grine, F.E. and L.B. Martin, 1988. Enamel thickness and development in Australopithecus and Paranthropus. In Grine, F.E., ed., Evolutionary History of the “Robust” Australopithecines. New York, NY: Aldine de Gruyter, pp. 3–42. Gunn, B.M., N.D. Watkins, W.E. Trzcienski Jr., and J. Nougier, 1975. The Amsterdam– St. Paul volcanic province, and the formation of low Al tholeiitic andesites. Lithos, 8:137–149. Gunn, R.G., 1967. Life time performance of the breeding ewe. In Hill Farming Research Organization, 4th Annual Report, pp. 51–58. Gunn, R.G., 1970a. A note on the effect of Broken Mouth on the performance of Scottish Blackface hill ewes. Animal Production, 12:517–520. References 369

Gunn, R.G., 1970b. Some factors affecting reproductive rate in hill sheep. In Hill Farming Research Organization, 5th Annual Report, pp. 45–54. Guthrie-Smith, H., 1921. Tutira: the Story of a New Zealand Sheep Station. Edinburgh: William Blackwood and Sons. Hadley, D., G.L. Hufford, and J.J. Simpson, 2004. Resuspension of relic volcanic ash and dust from Katmai: still an aviation hazard. Weather and Forecasting, 9:829–840. Haileab, B., F.H. Brown, I. McDougall, and P.N. Gathogo, 2004. Gombe Group basalts and intitiation of Pliocene deposition in the Turkana depression, northern Kenya and southern Ethiopia. Geological Magazine, 141:41–53. Halffter, G., 1991. Historical and ecological factors determining the geographical distribution of beetles (Coleoptera: Scaraboidae: Scaraboeinae). Folia Entomológica Mexicana (Instituto de Ecologia, Veracruz, Mexico), 82:195–238. Hall, E.A., R.L. Specht, and C.M. Eardley, 1964. Regeneration of vegetation on the Koonamore Vegetation Reserve, 1926–1962. Australian Journal of Botany, 12:205–264. Halstead, P., P. Collins, and V. Isaakidou, 2002. Sorting the sheep from the goats: morphological distinctions between the mandibles and mandibular teeth of adult Ovis and Capra. Journal of Archaeological Science, 29:545–553. Hambrey, M.J., W.U. Ehrmann, and B. Larsen, 1991. Cenozoic glacial record of the Prydz Bay continental shelf, East Antarctica. In Barron, J., B. Larsen, and J.G. Baldauf, eds., Proceedings of the Ocean Drilling Project, Scientific Results, 119:77–132. Hancox, G.T. and K. Wright, 2005. Analysis of Terrain and Landsliding Caused by the 15–17 February 2004 Rainstorm in the Wanganui–Manawatu Hill Country, Southern North Island, New Zealand. Institute of Geological and Nuclear Sciences Science Report, 2005/11. Hanihara, T. and H. Ishida, 2005. Metric dental variation in major human populations. American Journal of Physical Anthropology, 128:287–298. Hansson, L. 1970. Methods of morphological diet micro-analysis in rodents. Oikos, 21:255–266. Hao, Q., Z. Guo, Y. Qiao, B. Xu, and F. Oldfield, 2010. Geochemical evidence for the provenance of middle Pleistocene loess deposits in southern China. Quaternary Science Reviews, 29:3317–3326. Harris, E.F. and L.R. Lease, 2005. Mesiodistal tooth crown dimensions of the primary dentition: a worldwide survey. American Journal of Physical Anthropology, 128:593–607. Harris, J.M. and T.E. Cerling, 2002. Dietary adaptations of extant and Neogene African suids. Journal of Zoology, 256:45–54. Harris, J.M. and T.D. White, 1979. Evolution of the Plio-Pleistocene African Suidae. Transac- tions of the American Philosophical Society, new series, 69:1–128. Hart, S.R., M. Coetzee, R.K. Workman, et al., 2004. Genesis of the Western Samoa seamount province: age, geochemical fingerprint and tectonics. Earth and Planetary Science Letters, 227:37–56. Hart, W.K., R.C. Walker, and G. WoldeGabriel, 1992. Tehpra sources and correlations in Ethiopia: application of elemental and neodymium isotope data. Quaternary International, 13–14:77–86. Hart, W.K., G. WoldeGabriel, R.C. Walter, and S.A. Mertzman, 1989. Basaltic volcanism in Ethiopia: constraints on continental rifting and mantle interactions. Journal of Geophysical Research, 94:7731–7748. Hasselbarth, L.M., B.H. Barnum, N.S. Winstead, and B.A. Toth, 2002. CARMA-dust user’s guide, 1.2 edition. UPOS-BC3-06, 20 pp. 370 References

Hawando, T., 1997. Desertification in Ethiopian highlands. Agricultural Research Institut, Agricultural University of Iceland, Reykjavik. RALA Report 200, pp. 75–86. Hay, W.W., J.L. Sloan and C.N. Wold, 1988. Mass/age distribution and composition of sediments on the ocean floor and the global rate of sediment subduction. Journal of Geophysical Research, 93:14 933–14 940. Healy, W.B., 1967. Ingestion of soil by sheep. Proceedings of the New Zealand Society of Animal Production, 27:109–120. Healy, W.B., 1968. The influence of soil type on ingestion of soil by grazing animals. International Society of Soil Science, Adelaide, 1968. Transactions of the 9th International Congress of Soil Science, 111:437–445. Healy, W.B. and T.G. Ludwig, 1965a. Ingestion of soil by sheep in New Zealand in relation to wear of teeth. Nature, 208:806–807. Healy, W.B. and T.G. Ludwig, 1965b. Wear of sheep’s teeth. I. The role of ingested soil. New Zealand Journal of Agricultural Research, 8:737–752. Healy, W.B. and T.G. Ludwig, 1966. Enamel solubility studies on New Zealand teeth. New Zealand Dental Journal, 62:276–278. Henderson, A., G. Galeano, and R. Bernal, 1997. Field Guide to Palms of the Americas. Princeton, NJ: Princeton University Press. Hershkovitz, P., 1962. Evolution of neotropical cricetine rodents (Muridae) with special reference to the phyllotine group. Fieldiana: Zoology, 46:1–524. Hershkovitz, P., 1969. The evolution of mammals on southern continents. VI. The recent mammals of the neotropical region: a zoogeographic and ecological review. Quarterly Review of Biology, 44:1–70. Herweijer, C., R. Seager, E.R. Cook, and J. Emile-Geay, 2007. North American droughts of the last millennium from a gridded network of tree-ring data. Journal of Climate, 20:1353–1376. Hesse, P.P., 1994. The record of continental dust from Australia in Tasman Sea sediments. Quaternary Science Reviews, 13:257–272. Hesse, P.P., 1997. Mineral magnetic ‘tracing’ of aeolian dust in Southwest Pacific sediments. Palaeogeography, Palaeoclimatology, Palaeoecology, 131:327–353. Hesse, P.P. and G.H. McTainsh, 2003. Australian dust deposits: modern processes and the Quaternary record. Quaternary Science Reviews, 22:2007–2035. Hewison, A.J.M., J.P. Vincent, J.M. Angibault, et al., 1999. Tests of estimation of age from tooth wear on Roe Deer of known age: Variation within and among populations. Canadian Journal of Zoology, 77:58–67. Hewitt, A.E., 1996. Estimating surface erosion using 137Cs at a semi-arid site in Central Otago, New Zealand. Journal of the Royal Society of New Zealand, 26:107–118. Hickey, F., 1960. Death and reproductive rates of sheep in relation to flock culling and selection. New Zealand Journal of Agricultural Research, 3:332–344. Hickey, F., 1963. Sheep mortality in New Zealand. New Zealand Agriculturist, Feilding, 15:1–3. Hicks, D.M., B. Gomez, and N.A. Trustrum, 2000. Erosion thresholds and suspended sediment yields: Waipaoa River basin, New Zealand. American Geophysical Union, Water Resources Research, Baltimore, MD, 36:1129–1142. Hillson, S., 1986. Teeth. Cambridge Manuals in Archaeology. Cambridge, UK: Cambridge University Press. Hinojosa, L.F., 2005. Cambios climáticos y vegetacionales inferidos a partir de paleofloras cenozoicas del sur de Sudamérica. Revista Geológica de Chile, 32:95–115. References 371

Hitz, R.B., 1997. Contributions to South American Mammalian Paleontology: New Interatheres (Notoungulata) from Chile and Bolivia, Typothere (Notoungulata) Phylogeny, and Paleosols from the Late Oligocene Salla Beds. PhD Dissertation, University of California at Santa Barbara. Hitz, R.B., J.J. Flynn, and A.R. Wyss, 2006. New basal Interatheriidae (Typotheria, Notoungulata, Mammalia) from the Paleogene of Central Chile. American Museum Novitates, 3520:1–32. Hitz, R.B., M.A. Reguero, A.R. Wyss, and J.J. Flynn, 2000. New Interatheriines (Interatheriidae, Notoungulata) from the Paleogene of Central Chile and Southern Argentina. Fieldiana: Geology, new series, 42:1–26. Hobbs, J.E., J.A. Lindesay, and H.A. Bridgman, eds., 1998. Climates of the Southern Continents: Past, Present, and Future. Amsterdam, the Netherlands: Springer. Hodson, M.J., P.J. White, A. Mead, and M.R. Broadley, 2005. Phylogenetic variation in the silicon composition of plants. Annals of Botany, 96:1027–1046. Hoffstetter, R. and R. Lavocat, 1970. Découverte dans le Déséadien de Bolivie des genres pentalophodontes appuyant les affinities africaines des rongeurs caviomorphes. Comptes Rendus Hebdomadaires des Séances de l’Académie des Sciences, Paris, Série D, 271:172–175. Holechek, J.L., 1982. Sample preparation techniques for microhistological analysis. Journal of Range Management, 35:267–268. Hollis, C.J., L. Handley, E.M. Crouch, et al., 2009. Tropical sea temperatures in the high-latitude South Pacific during the Eocene. Geology, 37:99–102. Holmgren, M., B.C. López, J.R. Gutiérrez, and F.A. Squeo, 2006. Herbivory and plant growth rate determine the success of El Niño Southern Oscillation-driven tree establishment in semiarid South America. Global Change Biology, 12:2263–2271. Hoorn, C., F.P. Wesselingh, H. ter Steege, et al., 2010. Amazonia through time: Andean uplift, climate change, landscape evolution, and biodiversity. Science 330:927–931. Horton, B.K., B.A. Hampton, B.N. LaReau, and E. Baldellon,. 2002. Tertiary provenance history of the Northern and Central Altiplano (Central Andes, Bolivia): a detrital record of Plateau- Margin Tectonics. Journal of Sedimentary Research, 72: 711–726. Houghton, P., 1996. People of the Great Ocean. Cambridge, UK: Cambridge University Press. Huber, M., 2001. Modeling Early Paleogene Climate: from the Top of the Atmosphere to the Bottom of the Ocean. PhD Dissertation, University of California at Santa Cruz, Santa Cruz, CA, 220 pp. Huber, M. and D. Nof, 2006. The ocean circulation in the southern hemisphere and its climatic impacts in the Eocene. Palaeogeography, Palaeoclimatology, Palaeoecology, 231:9–28. Huelsenbeck, J.P., 1994. Comparing the stratigraphic record to estimates of phylogeny. Paleo- biology, 20:470–483. Hungerbühler, D., M. Steinmann, W. Winkler, et al., 1995. An integrated study of fill and deformation in the Andean intermontane basin of Nabón (Late Miocene), southern Ecuador. Sedimentary Geology, 96:257–279. Hungerbühler, D., M. Steinmann, W. Winkler, et al., 2002. Neogene stratigraphy and Andean geodynamics of southern Ecuador. Earth Science Reviews, 57:75–124. Hünicken, M., 1955. Depositos neocretácicos y terciarios del extremo SSW de Santa Cruz (Cuenca carbonífera de Río Turbio). Revista del Instituto Nacional de Investigación de las Ciencias Naturales y Museo Argentino de Ciencias Naturales “Bernardino Rivadavia,” 4:1–161. Hünicken, M., 1966. Flora terciaria de los estratos de Río Turbio, Santa Cruz (niveles plantíferos del Arroyo Santa Flavia). Revista de la Facultad de Ciencias Exactas, Físicas y Naturales (Córdoba), Serie Ciencias Naturales, 27:139–262. 372 References

Hunt, A.M., 1959. A description of the molar teeth and investing tissues of normal guinea pigs. Journal of Dental Research, 38:216–231. Hurni, H., 1985. Soil Conservation Manual for Ethiopia, ﬁrst draft. Ministry of Agriculture, Addis Ababa, Ethiopia. Hurni, H., 1990. Degradation and conservation of soil resources in the Ethiopian highlands. In Messerli, B. and H. Hurni, eds., African Mountains and Highlands: Problems and Perspective. African Mountains Association, Marceline, MO: Walsworth Press. Hürzeler, J., 1983. Un alcélaphiné aberrant (Bovidae, Mammalia) des “Lignites de Grosseto” en Toscane. Comptes rendus [hebdomadaires] des séances de l’Académie des sciences. Série II. Mécanique, physique, chimie, sciences de la terre, sciences de l’univers, 296:497–503. Hürzeler, J. and B. Engesser, 1976. Les faunes de mammiferes néogenes du Bassin de Baccinello (Grosseto, Italie). Compts Rendues de l’Académie des Sciences de Paris, Sér. D, 283:333–336. Hutton, J.T. and K. Norrish, 1974. Silicon content of wheat husks in relation to water transpired. Australian Journal of Agricultural Research, 25:203–212. Illius, A.W. and I.J. Gordon, 1992. Modeling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions. Oecologia 89:428–434. Imber, M., M. Harrison, and J. Harrison, 2000. Interactions between petrels, rats and rabbits on Whale Island, and effects of rat and rabbit eradication. New Zealand Journal of Ecology, 24:153–160. Indeje, M., 2000. Prediction and Numerical Simulation of the Regional Climate of Equatorial Eastern Africa. PhD Dissertation, North Carolina State University, Raleigh, NC. Indeje, M., F.H.M. Semazzi, L. Xie, and L.J. Ogallo, 2001. Mechanistic model simulations of the East African climate using NCAR regional climate model: inﬂuence of large-scale orography on the Turkana Low-Level jet. Journal of Climate, 14:2710–2724. International Station Meteorological Climate Summary (ISMCS), 2002. World Dust Storm Frequency (days/year) Map [www.bridge.bris.ac.uk/.../dust_storm_ww.jpg at www.bridge. bris.ac.uk/projects/DIRTMAP]. Iriondo, M.H., 1997. Models of deposition of loess and loessoids in the upper Quaternary of South America. Journal of South American Earth Sciences, 10:71–79. Iriondo, M.H. and D.M. Kröhling, 2007. Non-classical types of loess. Sedimentary Geology, 202:352–368. Ivany, L.C., S. Van Simaeys, E.W. Domack, and S.D. Samson, 2006. Evidence for an earliest Oligocene ice sheet on the Antarctic Peninsula. Geology, 34:377–380. Jablonski, N.G. and S. Frost, 2010. Cercopithecoidea. In Werdelin, L. and W.J. Sanders, eds., Cenozoic Mammals of Africa. Berkeley, CA: University of California Press, pp. 393–428. Jablonski, N.G. and M.G. Leakey, 2008. Koobi Fora Research Project, Volume 6: The Monkeys. San Francisco, CA: California Academy of Sciences. Jackson, J.E., 1988. Terrestrial mammalian pests in Argentina, an overview. Proceedings of the Thirteenth Vertebrate Pest Conference, University of Nebraska, Lincoln, pp. 196–198. Jaksic, F.M., 1998. Vertebrate invaders and their ecological impacts in Chile. Biodiversity and Conservation, 7:1427–1445. Jaksic, F.M. and E.R. Fuentes, 1991. Ecology of a successful invader: the European rabbit in central Chile. In Groves, R.H. and F. Di Castri, eds., Biogeography of Mediterranean Invasions. Cambridge, UK: Cambridge University Press, pp. 273–283. Jaksic, F.M. and J.L. Yáñez, 1983. Rabbit and fox introductions in Tierra del Fuego: history and assessment of the attempts at biological control of the rabbit infestation. Biological Conser- vation, 26:367–374. References 373

James, I.L., 1973. Mass movements in the upper Pohangina catchment, Ruahine Range. Journal of Hydrology (New Zealand), 12:92–102. Janis, C.M., 1989. Why kangaroos (Marsupialia: Macropodidae) are not as hypsodont as ungulates (Eutheria). Australian Mammalogy, 13:49–53. Janis, C.M., 1995. Correlations between craniodental morphology and feeding behavior in ungulates: reciprocal illumination between living and fossil taxa. In Thomason, J.J., ed., Functional Morphology in Vertebrate Paleontology. Cambridge, UK: Cambridge University Press, pp. 76–98. Jensen, E.H., 1998. The Impact of Landslips on Contaminant Sources in Steep Pastoral Hill Country, Lake Tutira, North Island, New Zealand. Master’s thesis, Victoria University of Wellington, Wellington, New Zealand. Jewell, P.A., C. Milner, and J.M. Boyd, 1974. Island Survivors: The Ecology of the Soay Sheep of St Kilda. University of London, London, UK: The Athlone Press, 386 pp. Jicha, B.R., D.W. Scholl, and D.K. Rea, 2009. Circum-Paciﬁc arc ﬂare-ups and global cooling near the Eocene–Oligocene boundary. Geology, 37:303–306. Johansson, A., T. Haraldson, R. Omar, S. Kiliaridis, and G.E. Carlsson, 1993. A system for assessing the severity and progression of occlusal tooth wear. Journal of Oral Rehabilitation, 20:125–131. Jones, L.H.P. and A.A. Milne, 1963. Studies of silica in the oat plant. I. Chemical and physical properties of the silica. Plant and Soil, 18:207–220. Joordens, J.C.A., H.B. Vanhof, C.S. Feibel, et al., 2011. An astronomically tuned climate framework for hominins in the Turkana Basin. Earth and Planetary Science Letters, 307:1–8. Jordan, T.E., V. Tamm, G. Figueroa, et al., 1996. Development of the Miocene Manantiales foreland basin, Principal Cordillera, San Juan, Argentina. Andean Geology (formerly Revista Geológica de Chile), 23:43–79. Jordana, X. and M. Köhler, 2011. Enamel microstructure in the fossil bovid Myotragus balearicus (Majorca, Spain): implications for life-history evolution of dwarf mammals in insular ecosystems. Palaeogeography, Palaeoclimatology, Palaeoecology, 300:59–66. Jordana, X., N. Marín-Moratalla, D. DeMiguel, T.M. Kaiser, and M. Köhler, 2012. Evidence of correlated evolution of hypsodonty and exceptional longevity in endemic insular mammals. Proceedings of the Royal Society, London, B, Biological Sciences, 279:3339–3346. Justice, C.O., E. Vermote, J.R.G. Townshend, et al., 1998. The moderate resolution imaging spectroradiometer (MODIS): Land remote sensing for global research. IEEE Transactions on Geoscience and Remote Sensing, 36:1228–1249. Kaiser, T.M., D.W.H. Müller, M. Fortelius, et al., 2013. Hypsodonty and tooth facet development in relation to diet and habitat in herbivorous ungulates: implications for understanding tooth wear. Mammal Review, 43:34–46. Kane, D.W., 1984. The results of a Wairarapa survey of ovine incisor tooth anomalies, with particular respect to wear. Sheep and Beef Cattle Society of the New Zealand Veterinary Association, Proceedings of the Society’s 14th Seminar, Flock House, Bulls, New Zealand, pp. 19–32. Kanfoush, S.L., D.A. Hodell, C.D. Charles, T.R. Janecek, and F.R. Rack, 2002. Comparison of ice-rafted debris and physical properties in ODP Site 1094 (South Atlantic) with the Vostok ice core over the last four climatic cycles. Palaeogeography, Palaeoclimatology, Palaeoecology, 182:329–349. Katz, M.E., B.S. Cramer, J.R. Toggweiler, et al., 2011. Impact of Antarctic circumpolar current development on Late Paleogene ocean structure. Science, 332:1076–1079. 374 References

Kay, R.F., J.G. Fleagle, T.R.T. Mitchell, et al., 2008. The anatomy of Dolichocebus gaimanensis, a stem platyrrhine monkey from Argentina. Journal of Human Evolution, 54:323–382. Kay, R.F., B.J. MacFadden, R.H. Madden, H. Sandeman, and F. Anaya, 1998. Revised age of the Salla Beds, Bolivia, and its bearing on the age of the Deseadan South American Land Mammal “Age.” Journal of Vertebrate Paleontology, 18:189–199. Kay, R.F. and R.H. Madden, 1997. Paleogeography and paleoecology. In Kay, R.F., R.H. Madden, R.L. Cifelli, and J.J. Flynn, eds., Vertebrate Paleontology in the Neotropics: the Miocene Fauna of La Venta, Colombia. Washington DC: Smithsonian Institution Press, pp. 520–550. Kay, R.F., R.H. Madden, M.G. Vucetich, et al., 1999. Revised geochronology of the Casa- mayoran South American Land Mammal Age: climatic and biotic implications. Proceedings of the National Academy of Sciences of the United States of America, 96:13 235–13 240. Kemp, R.A., 2001. Pedogenic modification of loess: significance for palaeoclimatic reconstructions. Earth–Science Review, 54:145–156. Kennedy, N.M., 1980. Field recognition of tephric loess (c. 42,000–15,000 yr BP) in central North Island. New Zealand Soil News, 28:55–58. Kennett, J.P., 1977. Cenozoic evolution of Antarctic glaciation, the Circum-Antarctic Ocean, and their impact on global paleoceanography. Journal of Geophysical Research, 82:3843–3860. Kennett, J.P. and C.C. Von der Borch, 1986. Southwest Pacific Cenozoic paleoceanography. Initial Reports of the Deep Sea Drilling Project, 90:1493–1517. Kertesz, P., 1993. Veterinary Dentistry and Oral Surgery. London, UK: Wolfe Publishing. Kettner, A.J., B. Gomez, and J.P.M. Syvitski, 2007. Modeling suspended sediment discharge from the Waipaoa River system, New Zealand: the last 3000 years. Water Resources Research, 43(W07411):15 pp. Kieser, J.A., 1990. Human adult odontometrics: the study of variation in adult tooth size. In Cambridge Studies in Biological and Evolutionary Anthropology. Cambridge, UK: Cambridge University Press. Kieser, J.A., K.J. Dennison, J.A. Kaidonis, et al., 2001a. Patterns of dental wear in the early Maori dentition. International Journal of Osteoarchaeology, 11:206–217. Kieser, J.A., A. Kelsen, R. Love, P.G.P. Herbison, and K.J. Dennison, 2001b. Periapical lesions and dental wear in the early Maori. International Journal of Osteoarchaeology, 11:290–297. Kingdon, J., 1989. East African Mammals: An Atlas of Evolution in Africa. Chicago, IL: University of Chicago Press. Kingston, J.D., A.L. Deino, R.K. Edgar, and A. Hill, 2007. Astronomically forced climate change in the Kenyan Rift Valley 2.7–2.55 Ma: implications for the evolution of early hominin ecosystems. Journal of Human Evolution, 53:487–503. Kinuthia, J.H. 1992. Horizontal and vertical structure of the Lake Turkana Jet. Journal of Applied Meteorology, 31: 1248–1274. Kinuthia, J.H. and G.C. Asnani, 1982. A newly found jet in North Kenya (Turkana Channel). Monthly Weather Review, 110: 1722–1728. Klevezal, G.A., 1996. Recording Structures of Mammals: Determination of Age and Reconstruc- tion of Life History. Boca Raton, FL: CRC Press, 448 pp. Knights, M. and G.W. Garcia, 1997. The status and characteristics of the goat (Capra hircus) and its potential role as a significant milk producer in the tropics: a review. Small Ruminant Research, 26:203–215. Koenigswald, W.V., F.J. Goin, and R. Pascual, 1999. Hypsodonty and enamel microstructure in the Paleocene gondwanatherian mammal Sudamerica ameghinoi. Acta Palaeontologica Polo- nica, 44:263–300. References 375

Koford, C.B., 1957. The vicuña and the puna. Ecological Monographs, 27:153–219. Kohfeld, K.E. and S.P. Harrison, 2001. DIRTMAP: the geological record of dust. Earth-Science Reviews, 54:81–114. Köhler, M., 2010. Fast or slow? The evolution of life history traits associated with insular dwarfing. In Pérez-Mellado, V. and C. Ramon, eds., Islands and Evolution. Institut Menorquí d’Estudis, Recerca, 19:261–280. Köhler, M. and S. Moyà-Solà, 2001. Phalangeal adaptations in the fossil insular goat Myotragus. Journal of Vertebrate Paleontology, 21:621–624. Köhler, M. and S. Moyà-Solà, 2004. Reduction of brain and sense organs in the fossil insular bovid Myotragus. Brain Behavior and Evolution, 63:125–140. Köhler, M. and S. Moyà-Solà, 2009. Physiological and life history strategies of a fossil large mammal in a resource-limited environment. Proceedings of the National Academy of Sciences of the United States of America, 106:20 354–20 358. Kohn, M.J., 2010. Carbon isotope compositions of terrestrial C3 plants as indicators of (paleo) ecology and (paleo)climate. Proceedings of the National Academy of Sciences of the United States of America, 107:19 691–19 695. Kohn, M.J., J.A. Josef, R. Madden, et al., 2004. Climate stability across the Eocene–Oligocene transition, southern Argentina. Geology, 32:621–624. Kohn, M.J., C.A.E. Strömberg, R.H. Madden, R.E. Dunn, and A.A. Carlini, 2011. Stable isotope record of middle Eocene to early Miocene climate, Gran Barranca, southern Argentina. Journal of Vertebrate Paleontology, 31S:138. Kohn, M.J., A. Zanazzi, and J.A. Josef, 2010. Stable isotopes of fossil teeth and bones at Gran Barranca as monitors of climate change and tectonics. In Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., The Paleontology of Gran Barranca: Evolution and Environ- mental Change Through the Middle Cenozoic of Patagonia. Cambridge, UK: Cambridge University Press, pp. 341–361. Kojola, I., T. Helle, E. Huhta, and A. Niva, 1998. Foraging conditions, tooth wear and herbivore body reserves: a study of female reindeer. Oecologia, 117:26–30. Koppes, M.N. and D.R. Montgomery, 2009. The relative efficacy of fluvial and glacial erosion over modern to orogenic timescales. Nature, Geoscience, 2:644–647. Kosmas, C., N. Danalatos, LH Cammeraat, et al., 1997. The effect of land use on runoff and soil erosion rates under Mediterranean conditions. Catena, 29:45–59. Kowalski, E.A., 2001. Middle to Late Miocene Environments of Southern Ecuador: Temperature, Elevation, and Fossil Plants of the Nabón Basin. PhD Dissertation, University of Michigan, Ann Arbor, MI. Krajick, K., 2005. Winning the war against island invaders. Science, 310:1410–1413. Kramarz, A.G. and E.S. Bellosi, 2005. Hystricognath rodents from the Pinturas Formation, Early– Middle Miocene of Patagonia, biostratigraphic and paleoenvironmental implications. Journal of South American Earth Sciences, 18:199–212. Kramarz, A.G. and M. Bond, 2009. A new Oligocene astrapothere (Mammalia, Meridiungulata) from Patagonia and a new appraisal of astrapothere phylogeny. Journal of Systematic Palae- ontology, 7:117–128. Kramarz, A., M.G. Vucetich, A.A. Carlini, et al., 2010. A new mammal fauna at the top of the Gran Barranca sequence and its biochronological significance. In Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., The Paleontology of Gran Barranca: Evolution and Environmental Change Through the Middle Cenozoic of Patagonia. Cambridge, UK: Cambridge University Press, pp. 264–277. 376 References

Krause, D.W., 1993. Vucetichia (Gondwanatheria) is a junior synonym of Ferugliotherium (Multituberculata). Journal of Paleontology, 67:321–324. Krishtalka, L., R.M. West, C.G. Black, et al., 1987. Eocene (Wasatchian through Duchesnean) biochronology of North America. In Woodburne, M.O., ed., Cenozoic Mammals of North America: Geochronology and Biostratigraphy. Berkeley, CA: University of California Press, pp. 77–117. Krissek, L.A. and S.C. Clemens, 1991. Mineralogic variations in a Pleistocene high-resolution eolian record from the Owen Ridge, Western Arabian Sea (Site 722): implications for sediment source conditions and monsoon history. In Prell, W.L. and N. Niitsuma,eds., Proceedings of the Ocean Drilling Program, Scientiﬁc Results, 117:197–213. Krissek, L.A. and S.C. Clemens, 1992. Evidence for aridity-driven dust ﬂux to the northwest Arabian Sea and for decoupling of the dust and upwelling systems. In Summerhayse, C.P., W.L. Prell, and K.-C. Emeis, eds., Upwelling Systems, Evolution Since the Early Miocene. Geological Society, London: Special Publications, 64:359–378. Laden, G. and R. Wrangham, 2005. The rise of the hominids as an adaptive shift in fallback foods: plant underground storage organs (USOs) and australopith origins. Journal of Human Evolution, 49:482–498. Lal, R., 1993. Soil erosion and conservation in West Africa. In Pimentel, D., ed., World Soil Erosion and Conservation. Cambridge, UK: Cambridge University Press, pp. 7–25. Lalueza, C., J. Juan, and R.M. Albert, 1996. Phytolith analysis on dental calculus, enamel surface, and burial soil: information about diet and paleoenvironment. American Journal of Physical Anthropology, 101:101–113. Lalueza-Fox, C., C. Castresana, L. Sampietro, et al., 2005. Molecular dating of caprines using ancient DNA sequences of Myotragus balearicus, an extinct endemic Balearic mammal. BMC Evolutionary Biology, 5:70. Lalueza-Fox, C., B. Shapiro, P. Bover, J.A. Alcover, and J. Bertranpetit, 2002. Molecular phylogeny and evolution of the extinct bovid Myotragus balearicus. Molecular Phylogenetics and Evolution, 25:501–510. Lambert, M.G., N.A. Trustrum, and D.A. Costall, 1984. Effect of soil slip erosion on seasonally dry Wairarapa hill pastures. New Zealand Journal of Agricultural Research, 27:57–64. Lamont, N., 1939. Arresting deterioration of hill country. New Zealand Journal of Agriculture, 59:13–17. Lander, B., 1998. Oreodontoidea. In Janis, C.M., K.M. Scott, and L.L. Jacobs, eds., Evolution of Tertiary Mammals of North America, Cambridge, UK: Cambridge University Press, pp. 402–420. Landry, S.L., Jr., 1970. The Rodentia as omnivores. Quarterly Review of Biology, 45:351–372. Langer, P., 1987. Evolutionary patterns of Perissodactyla and Artiodactyla (Mammalia) with different types of digestion. Zeitschrift für Zoologische Systematik und Evolutionsforschung, 25:212–236. Lanigan, K., 2012. Characterisation and Paleoclimatic Signals within Tephric Loess Deposits Aged Between c. 33 to 9.5 cal ka in the Rotorua Area, Northern New Zealand. MS thesis, University of Waikato, Waikato, New Zealand. Larcher, W., 1995. Physiological Plant Ecology: Ecophysiology and Stress Physiology of Func- tional Groups. 3rd Edition. Berlin: Springer. Larrasoaña, J.C., A.P. Roberts, and E.J. Rohling, 2008. Magnetic susceptibility of eastern Mediterranean marine sediments as a proxy for Saharan dust supply? Marine Geology, 254:224–229. References 377

Latimer, J.C. and G.M. Filippelli, 2002. Eocene to Miocene terrigenous inputs and export production: geochemical evidence from ODP Leg 177, Site 1090. Palaeogeography, Palaeo- climatology, Palaeoecology 182:151–164. Latrubesse, E.M., M. Cozzuol, S.A.F. da Silva-Caminha, et al., 2010. The late Miocene paleogeography of the Amazon Basin and the evolution of the Amazon River system. Earth-Science Reviews, 99:99–124. Latrubesse, E.M., S.A.F. da Silva, M. Cozzuol, and M.L. Absy, 2007. Late Miocene continental sedimentation in southwestern Amazonia and its regional significance: biotic and geological evidence. Journal of South American Earth Sciences, 23:61–80. Lavenu, A., C. Noblet, G. Bonhomme, et al., 1992. New K-Ar age dates of Neogene to Quaternary volcanic rocks from the Ecuadorian Andes: implications for the relationship between sedimentation, volcanism and tectonics. Journal of South American Earth Sciences, 5:309–320. Law, K.T., C.K. Lee, N.M. King, and A.B. Rabie, 2003. The relationship between eruption and length of mandibular incisors in young rats. Medical Science Monitor: International Medical Journal of Experimental and Clinical Research, 9:47–53. Lawver, L.A. and L.M. Gahagan, 2003. Evolution of Cenozoic seaways in the circum-Antarctic region. Palaeogeography, Palaeoclimatology, Palaeoecology, 198:11–37. Leader-Williams, N., 1980. Dental abnormalities and mandibular swellings in South Georgia reindeer. Journal of Comparative Pathology, 90:315–330. Leader-Williams, N., 1982. Relationship between a disease, host density, and mortality in a free- living deer population. Journal of Animal Ecology, 51:235–240. Leader-Williams, N., 1988. Reindeer on South Georgia: The Ecology of an Introduced Popula- tion. Studies in Polar Research. Cambridge, UK: Cambridge University Press. Leakey, M.G., 1993. Evolution of Theropithecus in the Turkana Basin. In Jablonski, N., ed., Theropithecus: The Rise and Fall of a Primate Genus. Cambridge, UK: Cambridge University Press, pp. 85–123. Leamy, M.L., 1984. Andisols of the World. Congreso international de suelos volcanicos. Serie informes 13, Universidad de La Laguna, La Laguna, Spain: Secretariado de Publicaciones, pp. 368–387. Lear, C.H., T.R. Bailey, P.N. Pearson, H.K. Coxall, and Y. Rosenthal, 2008. Cooling and ice growth across the Eocene–Oligocene transition. Geology, 36:251–254. Lee, J.M. and J.G. Beeg, 2002. Geology of the Wairarapa Area, 1:250,000 geological map. Institute of Geological and Nuclear Sciences, Ltd., Lower Hutt, New Zealand. Leinders, J. 1984. Hoplitomerycidae fam. nov. (Ruminantia, Mammalia) from Neogene fissure fillings in Gargano (Italy). Part 1: The cranial osteology of Hoplitomeryx gen. nov. and a discussion on the classification of pecoran families. Scripta Geologica,70:1–68. Leps, J. and P. Smilauer, 2003. Multivariate Analysis of Ecological Data Using CANOCO. Cambridge UK: Cambridge University Press,. Leslie, C. and G.J. Hancock, 2008. Estimating the date corresponding to the horizon of the first detection of 137Cs and 239þ240Pu in sediment cores. Journal of Environmental Radioactivity, 99:483–490. Le Turdu, C., J.-J. Tiercelin, E. Gibert, et al., 1999. The Ziway-Shala lake basin system, Main Ethiopian Rift: influence of volcanism, tectonics, and climatic forcing on basin formation and sedimentation. Palaeogeography, Palaeoclimatology, Palaeoecology, 150:135–177. Leys, J., G. McTainsh, and Y. Shao, 2001. Wind erosion monitoring and modeling techniques in Australia. In Stott, D.E., R.H. Mohtar, and G.C. Steinhardt, eds., Sustaining the Global Farm. International Soil Conservation Organization, pp. 940–950. 378 References

Liang, Y., H. Hua, J. Zhang, C. Cheng, and V. Romheld, 2006. Importance of plant species and external silicon concentration to active silicon uptake and transport. New Phytologist, 172:63–72. Liu, Z., L.C. Cleaveland, and T.D. Herbert, 2008. Early onset and origin of 100-kyr cycles in Pleistocene tropical SST records. Earth and Planetary Science Letters, 265:703–715. Liu, Z., M. Pagani, D. Zinniker, et al., 2009. Global cooling during the Eocene-Oligocene climate transition. Science, 323:1187–1190. Livermore, R., C.-D. Hillenbrand, M. Meredith, and G. Eagles, 2007. Drake Passage and Cenozoic climate: an open and shut case? Geochemistry, Geophysics, Geosystems, 8:Q01005. Livermore, R., A. Nankivell, G. Eagles, and P. Morris, 2005. Paleogene opening of Drake Passage. Earth and Planetary Science Letters, 236:459–470. Lizarralde, M., J. Escobar, and G. Deferrari, 2004. Invader species in Argentina: a review about the beaver (Castor canadensis) population situation on Tierra del Fuego ecosystem. Interciencia, 29:352–356. Lloyd, E.F., S. Nathan, I.E.M. Smith, and R.B. Stewart, 1996. Volcanic history of Macauley Island, Kermedec Ridge, New Zealand. New Zealand Journal of Geology and Geophysics, 39:295–308. Lockwood, C.A., W.H. Kimbel, and D.C. Johanson, 2000. Temporal trends and metric variation in the mandibles and dentition of Australopithecus afarensis. Journal of Human Evolution,39:23–55. Longmore, M.E., 1982. The caesium-137 dating technique and associated applications in Australia–a review. In Ambrose, W. and P. Duerden, eds., Archaeometry: An Australian Perspective. Canberra, Australia: Australian National University Press, pp. 310–321. López, G.M., 1997. Paleogene faunal assemblage from Antofagasta de la Sierra (Catamarca Province, Argentina). Palaeovertebrata, Montpellier, 26:61–81. López, G.M., M.G. Vucetich, A.A. Carlini, et al., 2011. New Miocene mammal assemblages from Neogene Manantiales basin, Cordillera Frontal, San Juan, Argentina. In Salﬁty, J.A. and R.A. Marquillas, eds., Cenozoic Geology of the Central Andes of Argentina. Special Paper of the Geological Society of America, pp. 211–226. López-Martinez, N., 2008. The lagomorph fossil record and the origin of the European rabbit. In Alves, P.C., N. Ferrand, and K. Hackländer, eds., Lagomorph Biology: Evolution, Ecology, and Conservation. Berlin Heidelberg: Springer-Verlag, pp. 27–46. Louca, A., T. Antoniou, and M. Hatzipanayiotou, 1982. Comparative digestibility of feedstuffs by various ruminants, speciﬁcally goats. Proceedings of the Third International Conference on Goat Production and Disease. Tuscon, AZ: Dairy Goat Publishing Company, pp. 122–132. Loughran, R.J., B.L. Campbell, G.L. Elliott, and D.J. Shelly, 1990. Determination of the rate of sheet erosion on grazing land using caesium-137. Applied Geography, 10:125–133. Loughran, R.J., G.L. Elliott, B.L. Campbell, et al., 1993. Estimation of erosion using the radionuclide caesium-137 in three diverse areas in eastern Australia. Applied Geography, 13:169–188. Lowe, D.J. and D.J. Palmer, 2005. Andisols of New Zealand and Australia. Journal of Integrated Field Science, 2:39–65. Lowe, D.J., P.A.R. Shane, B.V. Alloway, and R.M. Newnham, 2008. Fingerprints and age models for widespread New Zealand tephra marker beds erupted since 30,000 years ago: a framework for NZ-INTIMATE. Quaternary Science Reviews, 27:95–126. Lucas, P.W., R.T. Corlett, and D.A. Luke, 1986. Postcanine tooth size and diet in anthropoid primates. Zeitschrift für Morphologie und Anthropologie, 76:253–276. References 379

Lucas, S.G. and R.M. Schoch, 1998. Tillodontia. In Janis, C.M., K.M. Scott, and L.L. Jacobs, eds., Evolution of Tertiary Mammals of North America, Cambridge, UK: Cambridge University Press, pp. 268–273. Lucas, S.G., R.M. Schoch, and T.E. Williamson, 1998. Taeniodonta. In Janis, C.M., K.M. Scott, and L.L. Jacobs, eds., Evolution of Tertiary Mammals of North America, Cambridge, UK: Cambridge University Press, pp. 260–267. Ludwig, T.G., W.B. Healy, and T.W. Cutress, 1966. Wear of sheep’s teeth. III. Seasonal variation in wear and ingested soil. New Zealand Journal of Agricultural Research, 9:157–164. Lustrino, M., L. Melluso, and V. Morra, 2007. The geochemical peculiarity of “Plio-Quaternary” volcanic rocks of Sardinia in the circum-Mediterranean area. In Beccaluva, L., G. Bianchini, and M. Wilson, eds., Cenozoic Volcanism in the Mediterreanean Area. Geological Society of America Special Paper, 418:277–301. Lüttge, U., 1997. Physiological Ecology of Tropical Plants. Berlin: Springer-Verlag. MacFadden, B.J., 1992. Fossil Horses: Systematics, Paleobiology, and Evolution of the Family Equidae. Cambridge, UK: Cambridge University Press. MacFadden, B.J., 2005. Diet and habitat of toxodont megaherbivores (Mammalia, Noto- ungulata) from the late Quaternary of South and Central America. Quaternary Research, 64:113–124. MacFadden,B.J.,F.Anaya,H.Perez,etal.,1990.LateCenozoicpaleomagnetismand chronology of Andean basins of Bolivia: evidence for possible oroclinal bending. Journal of Geology, 98:541–555. MacFadden, B.J., Y. Wang, T.E. Cerling, and F. Anaya, 1994. South American fossil mammals and carbon isotopes: a 25-million-year sequence from the Bolivian Andes. Palaeogeography, Palaeoclimatology, Palaeoecology, 107:257–268. MacKenzie, D., 1987. Can Ethiopia be saved? New Scientist, 115:54–58. Macklin, M.C., I.C. Fuller, J. Lewin, et al., 2002. Correlation of ﬂuvial sequences in the Mediterranean basin over the last 200 ka and their relationship to climate change. Quaternary Science Reviews, 21:1633–1641. MacLulich, D.A., 1937. Fluctuations in the Numbers of the Varying Hare (Lepus americanus). University of Toronto Studies, 43. Toronto, ON. MacLulich, D.A., 1957. The place of chance in population processes. Journal of Wildlife Management, 21:293–299. Madden, R.H., 1990. Miocene Toxodontidae (Notoungulata, Mammalia) from Colombia, Ecuador and Chile. PhD Dissertation, Duke University, Durham, North Carolina. Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., 2010. The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge, UK: Cambridge University Press. Madden, R.H., J. Guerrero, R.F. Kay, et al., 1997. The Laventan Stage and Age. In Kay, R.F., R.H. Madden, R.L. Cifelli and J.J. Flynn, eds., Vertebrate Paleontology in the Neotropics: the Miocene Fauna of La Venta, Colombia. Smithsonian Institution Press, Washington DC, pp. 499–519. Mahamed T.E.-A. and B.J. Ram, 1987. Sustaining Africa’s natural resources. Journal of Soil and Water Conservation, 42:224–227. Mahowald, N., K. Kohfeld, M. Hansson, et al., 1999. Dust sources and deposition during the last glacial maximum and current climate: a comparison of model results with paleodata from ice cores and marine sediments. Journal of Geophysical Research, Atmospheres, 104:15 895–15 916. 380 References

Mahowald, N.M., D.R. Muhs, S. Levis, et al., 2006. Change in atmospheric mineral aerosols in response to climate: last glacial period, preindustrial, modern, and doubled carbon dioxide climates. Journal of Geophysical Research, 111,D10202. Main, J.H.P. and D. Adams, 1965. Measurement of the rate of eruption of the rat incisor. Archives of Oral Biology, 10:999–1008. Mainland, I.L., 1998. Dental microwear and diet in domestic sheep (Ovis aries) and goats (Capra hircus): distinguishing grazing and fodder-fed ovicaprids using a quantitative analytical approach. Journal of Archaeological Science, 25:1259–1271. Mainland, I.L., 2003. Dental microwear in grazing and browsing Gotland sheep (Ovis aries) and its implications for dietary reconstruction. Journal of Archaeological Science, 30:1513–1527. Mallinson,D.J.,B.Flower,A.Hine,G.Brooks,andR.M.Garza,2003.Paleoclimateimplica- tions of high latitude precession-scale mineralogic ﬂuctuations during early Oligocene Antarctic glaciation: the Great Australian Bight record. Global and Planetary Change, 39:257–269. Manassero, M., P.E. Zalba, R.R. Andreis, and M. Morosi, 2000. Petrology of continental pyroclastic and epiclastic sequences in the Chubut Group (Cretaceous): Los Altares-Las Plumas area, Chubut, Patagonia. Andean Geology, 27:13–26. Mannion, A.M., 2008. The Tertiary–Quaternary environmental history of the Mediterranean Basin: the background to Mediterranean Island environments. In Vogiatzakis, I., G. Pungetti, and A.M. Mannion, eds., Mediterranean Island Landscapes: Natural and Cultural Approaches, Landscape Series, Volume 9. Amsterdam, the Netherlands: Springer, pp. 15–35. Mantua, N.J., S.R. Hare, Y. Zhang, J.M. Wallace, and R.C. Francis, 1997. A Paciﬁc interdecadal climate oscillation with impacts on salmon production. Bulletin of the American Meteoro- logical Society, 78:1069–1079. Markwick, P.J., 1998a. Crocodilian diversity in space and time: the role of climate in paleoecology and its implication for understanding K/T extinctions. Paleobiology,24:470–497. Markwick, P.J., 1998b. Fossil crocodilians as indicators of Late Cretaceous and Cenozoic climates: implications for using paleontological data in reconstructing palaeoclimate. Palaeo- geography, Palaeoclimatology, Palaeoecology, 137:205–271. Marocco, R., A. Lavenu, and R. Baudino, 1995. The Intermontane Late Paleogene/Neogene Basins of the Andes of Ecuador and Peru: Sedimentologic and Tectonic Implications. Ameri- can Association of Petroleum Geologists, Memoir, 62. Marra, A.C., 2005. Pleistocene mammals of Mediterranean islands. Quaternary International, 129:5–14. Marra, A.C., 2013. Evolution of endemic species, ecological interactions and geographical changes in an insular environment: a case study of Quaternary mammals of Sicily (Italy, EU). Geosciences, 3:114–139. Marsden, M. and D. Rowan, 1993. Protective value of vegetation on Tertiary terrain before and during Cyclone Bola, east coast, North Island, New Zealand. New Zealand Journal of Forestry Science, 23:255–263. Marshall, L.G. and B. Patterson, 1981. Geology and Geochronology of the Mammal-Bearing Tertiary of the Valle de Santa María and Río Corral Quemado, Catamarca Province, Argentina. Field Museum of Natural History, 80 pp. Marshall, L.G., C.C. Swisher III, A. Lavenu, R. Hoffstetter, and G.H. Curtis, 1992. Geochron- ology of the mammal-bearing late Cenozoic on the northern Altiplano, Bolivia. Journal of South American Earth Sciences, 5:1–19. References 381

Marshall, P., 1903. Dust storms in New Zealand. Nature, 68:233. Marshall, P., 1911. Oceania. In Steinmann, G. and O. Wilckens, eds., Handbuch der Regionalen Geologie, H. 7, no.2. Heidelberg, Germany. Marshall P., 1912. New Zealand and Adjacent Islands. Carl Winter’s Universitätsbuchhandlung, Heidelberg, Germany, 79 pp. Marshall, P. and E. Kidson, 1929. The dust storm of October 1928. New Zealand Journal of Science and Technology, 10:291–299. Marticorena, B. and G. Bergametti, 1995. Modeling the atmospheric dust cycle: 1. Design of a soil-derived dust emission scheme. Journal of Geophysical Research, 100:16 415–16 430. Martínez-Garcia, A., A. Rosell-Melé, S.L. Jaccard, et al., 2011. Southern Ocean dust-climate coupling over the past four million years. Nature, 476:312–316. Marx, R., D.E. Lee, K.M. Lloyd, and W.G. Lee, 2004. Phytolith morphology and biogenic silica concentrations and abundance in leaves of Chionochloa (Danthonieae) and Festuca (Poeae) in New Zealand. New Zealand Journal of Botany, 42:677–691. Marx, S.K. and B.S. Kamber, 2010. Trace-element systematics of sediments in the Murray– Darling Basin, Australia: sediment provenance and palaeoclimate implications of fine scale chemical heterogeneity. Applied Geochemistry, 25:1221–1237. Marx, S.K. and H.A. McGowan, 2005. A re-examination of the 1928 trans-Tasman dust transport event. Weather and Climate, 24:35–55. Marx, S.K., H.A. McGowan, and B.S. Kamber, 2009. Long-range dust transport from eastern Australia: a proxy for Holocene aridity and ENSO-type climate variability. Earth and Planetary Science Letters, 282:167–177. Masini, F., D. Petruso, L. Bonfiglio, and G. Mangano, 2008. Origination and extinction patterns of mammals in three central Western Mediterranean islands from the Late Miocene to Quater- nary. Quaternary International, 182:63–79. Masters, D.G., C.L. White, G.J. Judson, J. Lee, and N.D. Grace, 1999. Current issues in trace element nutrition of grazing livestock in Australia and New Zealand. Australian Journal of Agricultural Research, 50:1341–1364. Mather, A.S., 1982. The desertification of Central Otago, New Zealand. Environmental Conser- vation, 9:209–216. Matthew, W.D., 1901. Fossil mammals of the Tertiary of Northeastern Colorado. Memoirs of the American Museum of Natural History, 1:355–447. Matthews, B. and B.K.B. Berkovitz, 1972. Continuous recording of tooth eruption in the rabbit. Archives of Oral Biology, 17:817–820. Mayland, H.F., A.R. Florence, R.C. Rosenau, V.A. Lazar, and H.A. Turner, 1975. Soil ingestion by cattle on semiarid range as reflected by titanium analysis of feces. Journal of Range Management, 28:448–452. Mayland, H.F., G.E. Shewmaker, and R.C. Bull, 1977. Soil ingestion by cattle grazing crested wheatgrass. Journal of Range Management, 30:264–265. Mayland, H.F., J.L. Wright, and R.E. Sojka, 1991. Silicon accumulation and water uptake by wheat. Plant and Soil, 137:191–199. Mays, S., 2002. The relationship between molar wear and age in an early 19th Century AD archaeological human skeletal series of documented age at death. Journal of Archaeological Science, 29:861–871. Mazza, P., 1987a. Prolagus (Ochotonidae, Lagomorpha, Mammalia) from Neogene fissure fillings in Gargano (Southern Italy). Bollettino della Società Paleontologica Italiana, 25:159–185. 382 References

Mazza, P., 1987b. Further data on the Gargano (Southern Italy) Prolagus (Ochotonidae, Lagomorpha, Mammalia). Bollettino della Società Paleontologica Italiana, 25:203–211. Mazza, P., 1987c. Prolagus apricenicus and Prolagus imperialis: two new Ochotonids (Lago- morpha, Mammalia) of the Gargano (Southern Italy). Bollettino della Società Paleontologica Italiana, 26:233–243. Mazzoni, M.M., 1979. Contribución al conocimiento petrográfico de la Formación Sarmiento, barranca Sur del lago Colhue-Huapi, provincia del Chubut. Revista de la Asociacioń Argentina de Mineralogía. Petrología y Sedimentología, 10:33–54. Mazzoni, M.M., 1985. La Formación Sarmiento y el vulcanismo paleógeno. Revista de la Asociación Geológica Argentina, 40:60–68. McCann, W., 1852. Two Thousand Mile Ride Through the Argentine Provinces., London, UK: Smith, Elder, and Co. McCulloch, M., S. Fallon, T. Wyndham, et al., 2003. Coral record of increased sediment flux to the inner Great Barrier Reef since European settlement. Nature, 421:727–730. McDowell, R.E. and A. Woodward, 1982. Concepts in animal adaptation: comparative suitability of goat, sheep and cattle to tropical environments. Proceedings of the Third International Conference on Goat Production and Disease. Tuscon, AZ: Dairy Goat Publishing Company, pp. 387–394. McGlone, M.S., R.M. Newnham, and N.T. Moar, 2010. The vegetation cover of New Zealand during the Last Glacial Maximum: do pollen records under-represent woody vegetation? In Haberle, S., J. Stevenson, and M. Prebble, eds. Altered Ecologies (Terra Australis 32): Fire, Climate and Human Influence on Terrestrial Landscapes. Canberra, Australia: Australian National University Press, pp. 49–68. McGlone, M., J. Wilmshurst, and C. Meurk, 2007. Climate, fire, farming and the recent vegetation history of subantarctic Campbell Island. Earth and Environmental Science Transactions of the Royal Society of Edinburgh, 98:71–84. McGowan, H. and A. Clark, 2008. Identification of dust transport pathways from Lake Eyre Australia using Hysplit. Atmospheric Environment, 42:6915–6925. McGreevy, P.D., L.A. Hawson, T.C. Habermann, and S.R. Cattle, 2001. Geophagia in horses: a short note on 13 cases. Applied Animal Behaviour Science,71:119–125. McHenry, H.M., 1984a. Relative cheek-tooth size in Australopithecus. American Journal of Physical Anthropology, 64:297–306. McHenry, H.M., 1984b. New estimates of body weight in early hominids and their significance to encephalization and megadontia in robust australopithecines. In Grine, F.E. ed., Evolutionary History of the Robust Australopithecines. New York, NY: Aldine de Gruyter, pp. 133–147. McKenna, M.C., 1975. Toward a phylogenetic classification of the Mammalia. In Luckett, W.P. and F.S. Szalay, eds., Phylogeny of the Primates: A Multidisciplinary Approach. New York, NY: Plenum Press, pp. 21–46. McKenna, M.C. and S. Bell, 1997. Classification of Mammals above the Species Level. New York, NY: Columbia University Press. McKenna, M.C., A.R. Wyss, and J.J. Flynn, 2006. Paleogene pseudoglyptodont xenarthrans from central Chile and Argentine Patagonia. American Museum Novitates, 3536:1–18. McManus, W.R., 1966. Stocking rate and other grazing studies on the southern tablelands of New South Wales Wool Technology and Sheep Breeding, 13:97–102. McManus, W.R., G.W. Arnold, and M.L. Dudzinski, 1965. Studies in the wool production of grazing sheep. 4. Variation between sheep in intake, wool production, and efficiency. Australian Journal of Experimental Agriculture and Animal Husbandry,6:96–100. References 383

McManus, W.R., G.W. Arnold, and J.R. Paynter, 1964. Studies in the wool production of grazing sheep. 2. Variation in wool characteristics with season and stocking rate. Australian Journal of Experimental Agriculture and Animal Husbandry, 4:404–411. McNaughton, S.J., J.L. Tarrants, and M.M. McNaughton, 1985. Silica as a defense against herbivory and a growth promotor in African grasses. Ecology, 66:528–535. McSaveney, M.J. and I.E. Whitehouse, 1989. Anthropic erosion of mountain land in Canterbury. New Zealand Journal of Ecology, 12:151–163. McTainsh, G.H., 1989. Quaternary aeolian dust processes and sediments in the Australian region. Quaternary Science Reviews, 8:235–253. McTainsh, G.H., 1998. Dust storm index. In Sustainable Agriculture: Australia’s Recent Performance. A report of the National Collaborative Project on Indicators of Sustainable Agriculture. SCARM (Standing Committee on Agriculture and Resource Management) Tech- nical Report 70. Melbourne Australia: CSIRO Publishing, pp. 123–125. McTainsh, G.H. and W.C. Boughton, 1993. Land Degradation Processes in Australia. Melbourne, Australia: Longman Cheshire. McTainsh, G.H., J.F. Leys, and E.K. Tews, 2006. Wind erosion trends for the National State of the Enviornment Report 2006: Data and Methods. Australia: State of the Environment Annual Report, 2006:69–76. McTainsh, G.H. and A.W. Lynch, 1996. Quantitative estimates of the effect of climate change on dust storm activity in Australia during the Last Glacial Maximum. Geomorphology,17:263–271. McTainsh, G.H., A.W. Lynch, and R.C. Burgess, 1990. Wind erosion in eastern Australia. Australian Journal of Soil Research, 28:323–339. McTainsh, G.H., A.W. Lynch, and E.K. Tews, 1998. Climatic controls upon dust storm occurrence in eastern Australia. Journal of Arid Environments, 39:457–466. McTainsh, G.H. and J.R. Pitblado, 1987. Dust storms and related phenomena measured from meteorological records in Australia. Earth Surface Processes and Landforms, 12:415–424. McTainsh, G., K. Tews, J. Leys, and G. Bastin, 2008. Spatial and temporal trends in wind erosion of Australian rangelands during 1960 to 2005 using the Dust Storm Index (DSI): a report for the Australian Collaborative Rangeland Information System (ACRIS), Grifﬁth University, Brisbane, Australia. Mein, P. and R. Adrover, 1982. Une faunule de mammifères insulaires dans le Miocène moyen de Majorque (Iles Baléares). In Buffetaut, E., P. Janvier, J.-C. Rage, and P. Tassy, eds., Phylo- génie et Paléobiogéographie: Livre jubilaire en l’honneur de Robert Hoffstetter. Geobios, 15:451–463. Mein, P., E. Martín Suárez, and J. Agusti, 1993. Progonomys Schaub, 1938 and Huerzelerimys Gen. Nov., (Rodentia); their evolution in Western Europe. Scripta Geologica, 103:41–64. Meserve, P.L., B.K. Lang, and B.D. Patterson, 1988. Trophic relationships of small mammals in a Chilean temperate rainforest. Journal of Mammalogy, 69:721–730. Meserve, P. L., R. Murúa, O. Lopetegui, and J.R. Rau, 1982. Observations on the small mammal fauna of a primary temperate rain forest in southern Chile. Journal of Mammalogy, 1982:315–317. Mesﬁn, W.-M., 1972. An Introductory Geography of Ethiopia. Addis Ababa, Ethiopia: Berha- nena Selam H.S.I. Printing Press. Meurk, C.D., M.N. Foggo, and J.B. Wilson, 1994. The vegetation of subantarctic Campbell Island. New Zealand Journal of Ecology, 18:123–168. Meyer, H.H., W.M. Aitken, and J.E. Smeaton, 1983. Inheritance of wear rate in the teeth of sheep. Proceedings of the New Zealand Society of Animal Production, 43:189–191. 384 References

Michalk, D.L., 1980. Production systems on Australian sheep ranches. Rangelands, 2:11–14. Micol, T. and P. Jouventin, 2002. Eradication of rats and rabbits from Saint-Paul Island, French Southern Territories. In Veitch, C.R. and M.N. Clout, eds., Turning the Tide: the Eradication of Invasive Species, Cambridge, UK: IUCN, pp. 199–205. Mihlbachler, M.C., F. Rivals, N. Solounias, and G.M. Semprebon, 2011. Dietary change and evolution of horses in North America. Science, 331:1178–1181. Miles, A.E.W., 2001. The Miles method of assessing age from tooth wear revisited. Journal of Archaeological Science, 28:973–982. Miller, G.S. Jr., 1924. A second instance of the development of rodent-like incisors in an artiodactyl. Proceedings of the United States National Museum, 66:1–3. Miller, K.G., M.A. Kominz, J.V. Browning, J.D. Wright, and B.S. Cramer, 2005. The Phanero- zoic record of global sea-level change. Science 310:1293–1298. Millien, V., 2006. Morphological evolution is accelerated among island mammals. Public Library of Science, Biology, 4:1863–1868. Mills, A.J., A.V. Milewski, C. Sirami, et al., 2012. Aerosol capture by small trees in savannas marginal to treeless grassland in South Africa. Geoderma, 189–190:124–132. Milne, J.D.G. and I.J. Smalley, 1979. Loess deposits in the southern part of the North Island of New Zealand: an outline stratigraphy. Acta Geologica Academiae Scientiarum Hungaricae, 22:197–204. Mitchum, G.D., 1985. Tooth Deterioration in Sheep: a Study of Farms in Southern North Island of New Zealand. MSV Thesis, Massey University, Palmerston North, New Zealand. Mitchum, G.D. and A.N. Bruere, 1984. Solubilization of sheep’s teeth: a new look at a widespread New Zealand problem. Proceedings of the 14th Seminar of the Society of Sheep and Beef Cattle Veterinarians of the New Zealand Veterinary Association, pp. 44–56. Moe, H., 1979. Physiological cell death of secretory ameloblasts. Cell and Tissue Research, 197:443–451. Mohammed, M.U. and R. Bonneﬁlle, 1998. A late glacial/late Holocene pollen record from a highland peat at Tamsaa, Bale Mountains, south Ethiopia. Global and Planetary Change, 16–17:121–129. Mohr, P., 1983. Ethiopian ﬂood basalt province. Nature, 303:577–584. Molnar, P., 2004. Late Cenozoic increase in accumulation rates of terrestrial sediment: how might climate change have affected erosion rates? Annual Review of Earth and Planetary Science, 32:67–89. Molnar, S., J.K. McKee, I.M. Molnar, and T.R. Przybeck, 1983. Tooth wear rates among contemporary Australian aborigines. Journal of Dental Research, 62:562–565. Molnar, S., L. Richards, J. McKee, and I. Molnar, 1989. Tooth wear in Australian aboriginal populations from the river Murray valley. American Journal of Physical Anthropology, 79:185–196. Mones, A., 1981. Sinopsis sistemática preliminar de la familiar Dinomyidae (Mammalia: Roden- tia, Caviomorpha). Anais II Congresso Latino-Americano de Paleontologia, 2:605–619. Mones, A., 2002. Iconografía antigua y sinonímia objetiva del megaterio, Megatherium americanum Cuvier, 1796 (Mammalia: Bradypoda: Megatheriidae). Museo Nacional de Historia Natural y Antropología, Comunicaciones Paleontológicas, 2:161–191. Montgomery, D.R., G. Balco, and S.D. Willett, 2001. Climate, tectonics, and the morphology of the Andes. Geology, 29:579–582. Montgomery, D.R. and M.T. Brandon, 2002. Topographic controls on erosion rates in tectonically active mountain ranges. Earth and Planetary Science Letters, 201:481–489. References 385

Moreno, S., M. Delibes, and R.D. Villafuerte, 1996. Cover is safe during the day but dangerous at night: the use of vegetation by European wild rabbits. Canadian Journal of Zoology, 74:1656–1660. Moscatelli, G. and M.S. Pazos, 2000. Soils of Argentina: nature and use. In Kheoruenromne, I. and S. Theerawong, eds., Proceedings of International Symposium on Soil Science: Accom- plishments and Changing Paradigm towards the 21st Century and IUSS Extraordinary Council Meeting, pp. 81–92 [http://www.elsitioagricola.com/articulos/moscatelli/soils%20of %20argentina%20-%20nature%20and%20use.asp]. Moyà-Solà, S., J. Quintana, A. Alcover, and M. Köhler, 1999. Endemic island faunas of the Mediterranean Miocene. In Rössner, G.E. and K. Heissig, eds. The Miocene Land Mammals of Europe. München, Germany: Verlag Dr Friedrich Pfeil, pp. 435–442. Mullan, B., A. Porteous, D. Wratt, and M. Hollis, 2005. Changes in Drought Risk with Climate Change. Ministry for the Environment (NZ Climate Change Office) and Ministry of Agricul- ture and Forestry, National Institute of Water and Atmospheric Research NIWA Client Report: WLG2005-23 (May 2005), NIWA Project MFE05305, Wellington, New Zealand [www.niwa. co.nz]. Murai, S. and Y. Honda, 1990. World Vegetation Map. In Murai, S., Y. Honda, K. Asakura, and S. Goto, eds., An Analysis of Global Environment by Satellite Remote Sensing. Institute of Industrial Science, Tokyo, University of Tokyo [http://www-cger.nies.go.jp/grid-e/griddoc/vegetate.html]. Myneni, R.B., Y. Knyazikhin, J.L. Privette, et al., 2002. Global products of vegetation leaf area and fraction absorbed PAR from year one of MODIS data. Remote Sensing of Environment, 83:214–231. Nair, R.R., V. Ittekkot, S.J. Manganini, et al., 1989. Increased particle flux to the deep ocean related to monsoons. Nature, 228:749–751. Nammah, H., F.E. Larsen, D.K. McCool, R. Fritts Jr., and M. Molnau, 1986. Mt St Helens volcanic ash: effect of incorporated and unincorporated ash of two particle sizes on runoff and erosion. Agriculture, Ecosystems, and Environment, 15:63–72. Namwamba, F.L., 1993. Tephrostratigraphy of the Chemeron Formation, Baringo Basin, Kenya. MSc Thesis, University of Utah, Salt Lake City, UT. Náñez, C., ed, 1999. Paleogeno de América del Sur. Anales del Instituto de Geologia y Recursos Minerales, 33, Servicio Geologico Minero Argentino (SEGEMAR), Buenos Aires. NASA Earth Observtory 2005, Dust Storm in Australia. NASA Earth Observatory, 2009. EOS Project Science Office, NASA Goddard Space Flight Center. http://earthobservatory.nasa.gov/ NaturalHazards/view.php?id¼14580. Accessed 31 March 2009. Neave, H.M., 1999. Rabbit calicivirus disease program, report 1. Overview of Effects on Austra- lian Wild Rabbit Populations and Implications for Agriculture and Biodiversity. Rabbit Calicivirus Disease Monitoring and Surveillance Program and Epidemiology Research Program, Bureau of Rural Sciences, Canberra, Australia. Neil, D. and B. Yu, 1991. Rainfall extremes on the Southern Tablelands, NSW over the last century: implications for land degradation and land management. Proceedings of the Inter- national Hydrology and Water Resources Symposium, Perth, Australia, pp. 231–235. Ness, A.R., 1965. Eruption rates of impeded and unimpeded mandibular inciors of the adult laboratory mouse. Archives of Oral Biology, 10:439–451. Nichol, J.E. and D.W. Nichol, 2013. Pleistocene loess in the humid sub-tropical forest zone of East Asia. Geophysical Research Letters, 40:1978–1983. Nicholson, S.E., 1996. A review of climate dynamics and climate variability in Eastern Africa. In Johnson, T.C. and E. Onyango Odada, eds., The Limnology, Climatology and Paleoclimat- ology of the East African Lakes. Boca Raton, FL: CRC Press, pp. 25–56. 386 References

Nielsen, K.A., L.B. Clemmensen, and J.J. Fornós, 2004. Middle Pleistocene magnetostratigraphy and susceptibility stratigraphy: data from a carbonate aeolian system, Mallorca, Western Mediterranean. Quaternary Science Reviews, 23:1733–1756. Nong, G.T., R.G. Najjar, D. Seidov, and W.H. Peterson, 2000. Simulation of ocean temperature change due to the opening of Drake Passage. Geophysical Research Letters, 27:2689–2692. Norbury, D.C. and G.L. Norbury, 1996. Short-term effects of rabbit grazing on a degraded short- tussock grassland in central Otago. New Zealand Journal of Ecology, 20:285–288. North, S.G., D.J. Bullock, and M.E. Dulloo, 1994. Changes in the vegetation and reptile populations on Round Island, Mauritius, following eradication of rabbits. Biological Conser- vation, 67:21–28. Novillo, A. and R.A. Ojeda, 2008. The exotic mammals of Argentina. Biological Invasions, 10:1333–1344. Nyssen, J., J. Poesen, J. Moeyersons, et al., 2004. Human impact on the environment in the Ethiopian and Eritrean highlands–a state of the art. Earth-Science Reviews, 64:273–320. Ogle, C.C., 1990. Changes in the vegetation and vascular flora of Motuhora (Whale Island) 1970–1986. Tane, 32:19–48. Ohshima, H., N. Nakasone, E. Hashimoto, et al., 2005. The eternal tooth germ is formed at the apical end of continuously growing teeth. Archives of Oral Biology, 50:153–157. Ohtsuke, M. and H. Shinoda, 1995. Ontogeny of circadian dentinogenesis in the rat incisor. Archives of Oral Biology, 40:481–485. Olive, L.J., J.M. Olley, A.S. Murray, and P.J. Wallbrink, 1994. Spatial variation in suspended sediment transport in the Murrumbidgee River, New South Wales, Australia. In Variability in Stream Erosion and Sediment Transport. Proceedings of the Canberra Symposium,, IAHS Publication 224, pp. 241–249. Oliver, R. and J.H. Sorensen, 1951. Botanical investigations on Campbell Island. New Zealand Department of Science and Industry (DSIR), Research Cape Expedition Series Bulletin,7. Oliver, R.B., 1910. The vegetation of the Kermadec Islands. Transactions of the Royal Society of New Zealand, 42:118–175. Olley, J.M. and P. Wallbrink, 2004. Recent trends in turbidity and suspended sediment loads in the Murrumbidgee River, NSW, Australia. Sediment transfer through the fluvial system. Proceedings of a Symposium of the IAHS, Moscow, IAHS Publication 288:125–129. Olley, J.M. and R.J. Wasson, 2003. Changes in the flux of sediment in the Upper Murrumbidgee catchment, southeastern Australia, since European settlement. Hydrological Processes, 17:3307–3320. Orpin, A.R., L. Carter, M.J. Page, et al., 2010. Holocene sedimentary record from Lake Tutira: a template for upland watershed erosion proximal to the Waipaoa Sedimentary System, northeastern New Zealand. Marine Geology, 270:11–29. Orr, M.B., 1983. Incisor wear and acute periodontitis in ewes. Surveillance, 10:19–20. Orr, M.B., M.W. O’Callaghan, D.M. West, and A.N. Bruere, 1979. A syndrome of dental abnormalities of sheep. II. The pathology and radiology. New Zealand Veterinary Journal, 27:276–278. Ortiz, P.E., D.A. García López, M.J. Babot, et al., 2012. Exceptional Late Pliocene microvertebrate diversity in northwestern Argentina reveals a marked small mammal turnover. Palaeogeography, Palaeoclimatology, Palaeoecology,361–362:21–37. Page, M.J. and N.A. Trustrum, 1997. A late Holocene lake sediment record of the erosion response to land use change in a steepland catchment; New Zealand. Zeitschrift Fur Geomor- phologie, 41:369–392. References 387

Page. M.J., N.A. Trustrum, and R.C. DeRose, 1994a. A high resolution record of storm-induced erosion from lake sediments, New Zealand. Journal of Paleolimnology, 11:333–348. Page, M.J., N.A. Trustrum, and J.R. Dymond, 1994b. Sediment budget to assess the geomorphic effect of a cyclonic storm, New Zealand. Geomorphology, 9:169–188. Palazzesi, L. and V.D. Barreda, 2012. Fossil pollen records reveal a late rise of open-habitat ecosystems in Patagonia. Nature Communications 3: Article 1294. Palmer, A.S., 1982. The Stratigraphy and Selected Properties of Loess in Wairarapa, New Zealand. PhD thesis, Victoria University of Wellington, Wellington, New Zealand. Pardiñas, U.FJ. and E.P. Tonni, 1998. Procedencia estratigráfica y edad de los más antiguos Muroideos (Mammalia, Rodentia) de América del Sur. Ameghiniana, 35:473–475. Pardoe, C., 2003. The Menindee Lakes: a regional archaeology. Australian Archaeology, 57:42–53. Paredes, J.M., F. Colombo, N. Foix, et al., 2008. Basaltic explosive volcanism in a tuff-dominated intraplate setting, Sarmiento Formation (Middle Eocene–Lower Miocene), Patagonia, Argen- tina. Latin American Journal of Sedimentology and Basin Analysis, 15:77–92. Parkes, J.P., 1984a. Feral goats on Raoul Island. I. Effect of control methods on their density, distribution and productivity. New Zealand Journal of Ecology, 7:85–93. Parkes, J.P., 1984b. Feral goats on Raoul Island. II. Diet and notes on the flora. New Zealand Journal of Ecology, 7:95–101. Parkes, J.P., 1993. Feral goats: designing solutions for a designer pest. New Zealand Journal of Ecology, 17:71–83. Parkes, J.P., 1995. Rabbits as Pests in New Zealand: A Summary of the Issues and Critical Information. Landcare Research, Hamilton, New Zealand. Parkes, J.P., 2001. Advances in New Zealand mammalogy 1990–2000: feral livestock. Journal of the Royal Society of New Zealand, 31:233–241. Parkes, J.P., 2005. Feral sheep. In King, C.M., ed., The Handbook of New Zealand Mammals, 2nd Edition, Melbourne, Australia: Oxford University Press, pp. 392–398. Parkin, D.W., 1974. Trade-winds during the glacial cycles. Proceedings of the Royal Society, London, A, Mathematical, Physical and Engineering Sciences, 337:73–100. Parra, V., J.-J. Jaeger and H. Bocherens, 1999. The skull of Microtia, an extinct burrowing murine rodent of the late Neogene Gargano paleoisland. Lethaia, 32:89–100. Parras, A., M. Griffin, R. Feldmann, et al., 2008. Correlation of marine beds based on Sr- and Ar-date determinations and faunal affinities across the Paleogene/Neogene boundary in southern Patagonia, Argentina. Journal of South American Earth Sciences, 26:204–216. Pascual, R. and A.A. Carlini, 1987. A new superfamily in the extensive radiation of South American Paleogene marsupials. Fieldiana: Zoology, 39:99–110. Pascual, R., F.J. Goin, D.W. Krause, E. Ortiz-Jaureguizar, and A.A. Carlini, 1999. The first gnathic remains of Sudamerica: implications for gondwanathere relationships. Journal of Vertebrate Palaeontology, 19:373–382. Pascual, R. and O. Odremán Rivas, 1971. Evolución de las comunidades de los vertebrados del Terciario argentino; los aspectos paleozoogeograficos y paleoclimaticos relacionados. Ameghiniana, 7:372–412. Pascual, R. and O. Odremán Rivas, 1973. Las unidades estratigráficas del terciario portadoras de mamíferos: su distribución y sus relaciones con los acontecimientos diastróficos. Actas del Quinto Congreso Geológico Argentino, 3:293–335. Pascual, R. and E. Ortiz-Jaureguizar, 1990. Evolving climates and mammal faunas in Cenozoic South America. Journal of Human Evolution, 19:23–60. 388 References

Pascual, R. and E. Ortiz-Jaureguizar, 2007. The Gondwanan and South American episodes: two major and unrelated moments in the history of the South American mammals. Journal of Mammalian Evolution, 14:75–137. Pascual, R., M. G. Vucetich, G. J. Scillato-Yané and M. Bond, 1985. Main pathways of mammalian diversiﬁcation in South America. In F. G. Stehli and S. D. Webb, eds., The Great American Biotic Interchange. New York, Plenum Press, pp. 219–247. Passey, B.H., N.E. Levin, T.E. Cerling, F.H. Brown, and J.M. Eiler, 2010. High-temperature environments of human evolution in East Africa based on bond ordering in paleosol carbonates. Proceedings of the National Academy of Sciences of the United States of America, 107:11 245–11 249. Patterson, B., 1936. The internal structure of the ear in some notoungulates. Fieldiana, Geological Series, 6:199–227. Patterson, B., 1958. A new genus of erethizontid rodent from the Colhuehuapian of Patagonia. Breviora, 92:1–4. Patterson, B. and R. Pascual, 1968. The fossil mammal fauna of South America. Quarterly Review of Biology, 43: 409–451. Patterson, B. and A.E. Wood, 1982. Rodents from the Deseadan Oligocene of Bolivia and the relationships of the Caviomorpha. Bulletin of the Museum of Comparative Zoology, 149:371–543. Patterson, B.D., P.L. Meserve, and B.K. Lang, 1990. Quantitative habitat associations of small mammals along an elevational transect in temperate rainforests of Chile. Journal of Mammal- ogy, 71:620–633. Payne, S., 1973. Kill-off patterns in sheep and goats: The mandibles from Asvan Kale. Anatolian Studies, 23:281–303. Payne, S., 1985. Morphological distinctions between the mandibular teeth of young sheep (Ovis) and goats (Capra). Journal of Archaeological Science, 12:139–147. Payne, S., 1987. Reference codes for wear states in the mandibular cheek teeth of sheep and goats. Journal of Archaeological Science, 14:609–614. Pearsall, D.M., 2000. Paleoethnobotany: A Handbook of Procedures. San Diego, CA: Academic Press. Pearson, O.P., 1951. Mammals in the highlands of southern Peru. Bulletin of the Museum of Comparative Zoology, 106:117–174. Pease, P.P., V.P. Tchakerian, and N.W. Tindale, 1998. Aerosols over the Arabian Sea: geochemistry and source areas for aeolian desert dust. Journal of Arid Environments, 39:477–496. Peden, R., 2012. The spread of rabbits in New Zealand. Te Ara–The Encyclopedia of New Zealand [http://www.teara.govt.nz/en/rabbits/1]. Pedersen, E.O. and E.B. Roche, 1973. End of a rabbit infestation. New Zealand Journal of Agriculture, 158:45–47. Peizhen, Z., P. Molnar, and W.R. Downs, 2001. Increased sedimentation rates and grain sizes 2–4 myr ago due to the inﬂuence of climate change on erosion rates. Nature, 410:891–897. Pekar, S.F., N. Christie-Blick, M.A. Kominz, and K.G. Miller, 2002. Calibration between eustatic estimates from back-stripping and oxygen isotopic records for the Oligocene. Geology, 30:903–906. Pekar, S.F., A. Hucks, M. Fuller, and S. Li, 2005. Glacioeustatic changes in the early and middle Eocene (51–42 Ma): shallow-water stratigraphy from ODP Leg 189 Site 1171 (South Tasman Rise) and deep-sea d18O records. Geological Society of America Bulletin, 117:1081–1093. References 389

Pendergast, A.L., J.M. Bowler, and M.L. Cupper, 2009. Late Quaternary environments and human occupation in the Murray River Valley of northwestern Victoria. In Fairbaim A.S., S. O’Connor, and B. Marwick, eds., New Directions in Archaeological Science. Canberra, Australia: Australian National University Press, Terra Australis, 28:55–74. Pérez-Barbería, F.J. and I.J. Gordon, 2001. Relationships between oral morphology and feeding style in the Ungulata: a phylogenetically controlled evaluation. Proceedings of the Royal Society, London, B, Biological Sciences, 268:1023–1032. Pfuhl, H.A. and I.N. McCave, 2005. Evidence for late Oligocene establishment of the Antarctic Circumpolar Current. Earth and Planetary Science Letters, 235:715–728. Phillips, C.J. and B. Oxberry, 1972. Comparative histology of molar dentitions of Microtus and Clethrionomys, with comments on dental evolution in microtine rodents. Journal of Mammalogy, 53:1–20. Pick, J.H., 1942. Australia’s Dying Heart: Soil Erosion in the Inland. Melbourne, Australia: Melbourne University Press, 90 pp. Pick, J.H. and V.L.R. Alldis, 1944. Australia’s Dying Heart: Soil Erosion and Station Manage- ment in the Inland. Melbourne, Australia: Melbourne University Press, 119 pp. Pickford, M. 2001. The status of Sus giganeus Falconer and Cautley, 1847 (Mammalia, Suinae) from the Indian subcontinent. Transactions of the Royal Society of Edinburgh, Earth Sciences, 92:39–42. Pickford, M., B. Senut, G. Poupeau, F.H. Brown, and B. Haileab, 1991. Correlation of tephra layers from the Western Rift Valley (Uganda) to the Turkana Basin (Ethiopia/Kenya) and the Gulf of Aden. Compte Rendus de l’Académie des Sciences, Paris, Série II, 313:223–229. Pik, R. 2011. East Africa on the rise. Nature Geoscience, 4:660–661. Pillans, B.J., 1988. Loess chronology in Wanganui Basin, New Zealand. In Eden, D.N. and R.J. Furkert, eds. Loess, its Distribution, Geology and Soils. Rotterdam, the Netherlands: Balkema, pp. 175–191. Pillans, B.J., 1991. New Zealand Quaternary stratigraphy: an overview. Quaternary Science Reviews, 10:405–418. Pillans, B.J., W.A. Pullar, M.J. Selby, and J.M. Soons, 1992. The age and development of the New Zealand landscape. In Soons, J.M. and M.J. Selby, eds., Landforms of New Zealand, 2nd Edition, Auckland, New Zealand: Longman Paul, pp. 31–62. Piperno, D.R., 1988. Phytolith Analysis: An Archaeological and Geological Perspective. London, UK: Academic Press. Piperno, D.R., 2006. Phytoliths. Altamira Press, Lanham, Maryland, 238 pp. Piperno D.R. and Pearsall, D.M., 1998. The silica bodies of tropical American grasses: morphology, taxonomy, and implications for grass systematics and fossil phytolith identiﬁcation. Smithsonian Contributions to Botany 85, Washington, DC: Smithsonian Institution Press. Pizzimenti, J.J. and R. De Salle, 1980. Dietary and morphometric variation in some Peruvian rodent communities: the effect of feeding strategy on evolution. Biological Journal of the Linnean Society, 13:263–285. Podbury, T., T.C. Sheales, I. Hussain, and B.S. Fisher, 1998. Use of El Niño climate forecasts in Australia. American Journal of Agricultural Economics, 80:1096–1101. Podwojewski P., J. Poulenard, T. Zambrana, and R. Hofstede, 2002. Overgrazing effects on vegetation cover and properties of volcanic ash soil in the páramo of Llangahua and La Esperanza (Tungurahua, Ecuador). Soil Use and Management, 18:45–55. Pohlen, I.J., 1971. Soils of Hawke’s Bay Region, New Zealand. Soil Bureau Publication 495, DSIR. 390 References

Pons-Moyà, J., S. Moyà-Solà, J. Agusti, and J.A. Alcover, 1981. La fauna de mamíferos de los yacimientos menorquines con Geochelone gymnesica (Bate, 1914), nota preliminar. Acta Geológica Hispánica, 16:129–130. Poorter, H., K.J. Niklas, P.B. Reich, et al., 2012. Biomass allocation to leaves, stems and roots: meta-analyses of interspecific variation and environmental control. New Phytologist, 193:30–50. Porter W.L., R.S. Scott, and B.W. Manktelow, 1970. The occurrence of paradontal disease in sheep in relation to superphosphate topdressing, stocking rate and other related factors. New Zealand Veterinary Journal, 18:21–27. Poux, C., P. Chevret, D. Huchon, W.W. de Jong, and E.J.P. Douzery, 2006. Arrival and diversification of caviomorph rodents and platyrrhine primates in South America. Systematic Biology, 55: 228–244. Powell, J.E., M.J. Babot, D.A. García López, M.V. Deraco, and C. Herrera, 2011. Eocene vertebrates of northwestern Argentina: annotated list. In Salfity, J.A. and R.A. Marquillas, eds., Cenozoic Geology of the Central Andes of Argentina. Special Paper of the Geological Society of America, pp. 349–370. Prell, W.L. and Niitsuma, N., eds., 1989. Site 722. Shipboard Scientific Party, Proceedings of the Ocean Drilling Program, Initial Reports, 117, College Station, TX. Preston, N.J. and M.J. Crozier, 1999. Resistance to shallow landslide failure through root-derived cohesion in East Coast hill country soils, North Island, New Zealand. Earth Surface Processes and Landforms, 24:665–675. Proffit, W.R. and K.T. Sellers, 1986. The effect of intermittent forces on eruption of the rabbit incisor. Journal of Dental Research, 65:118–122. Prospero, J.M., 1996. Saharan dust transport over the North Atlantic Ocean and Mediterranean: an overview. In Guerzoni, S. and R. Chester, eds., The Impact of Desert Dust Across the Mediterranean. New York, NY: Kluwer Academic Publishers, pp. 133–151. Prospero, J.M., P. Ginoux, O. Torres, S.E. Nicholson, and T.E. Gill, 2002. Environmental characterization of global sources of atmospheric soil dust identified with the Nimbus 7 total ozone mapping spectrometer (TOMS) absorbing aerosol product. Review of Geophysics, 40:1–30. Prothero, D.R. and C.C. Swisher III, 1992. Magnetostratigraphy and geochronology of the terrestrial Eocene–Oligocene transition in North America. In Berggren, W.A. and D.R. Prothero, eds., Eocene–Oligocene Climatic and Biotic Evolution. Princeton, NJ: Princeton University Press, pp. 46–73. Pye, K., 1987. Eolian Dust and Dust Deposits. New York, NY: Academic Press. Pye, K., 1995. The nature, origin and accumulation of loess. Quaternary Science Review, 14:653–667. Pyle, D.M., 1999. Widely dispersed Quaternary tephra in Africa. Global and Planetary Change, 21:95–112. Qian, H., C. Badgley, and D.L. Fox, 2009. The latitudinal gradient of beta diversity in relation to climate and topography for mammals in North America. Global Ecology and Biogeography, 18:111–122. Quinn, W.H., V.T. Neal, and S.E. Antunez de Mayolo, 1987. El Niño occurrences over the past four and a half centuries. Journal of Geophysical Research, 92:14 449–14 461. Quintana, J., P. Bover, J.A. Alcover, J. Agusti, and S. Ballon, 2010. Presence of Hypolagus Dice, 1917 (Mammalia, Lagomorpha) in the Neogene of the Balearic Islands (Western Mediterra- nean): description of Hypolagus balearicus nov. sp. Geobios, 43:555–567. Quintana, J., M. Köhler, and S. Moyà-Solà, 2011. Nuralagus rex, gen et sp nov, an endemic insular giant rabbit from the Neogene of Minorca (Badlearic Islands, Spain). Journal of Vertebrate Paleontology, 31:231–240. References 391

Rabinovics, J., A. Capurro, M. Hernandez, and J.L. Cajal, 1991. Vicuña and the bioeconomics of Andean peasant community in Catamarca, Argentina. In Robinson, J. and K. Redford, eds., Neotropical Wildlife Use and Conservation. Chicago, IL: University of Chicago Press, pp. 337–358. Raigemborn, M.S., M. Brea, A.F. Zucol, and S.D. Matheos, 2009. Early Paleogene climate at mid latitude in South America: mineralogical and paleobotanical proxies from continental sequences in Golfo San Jorge basin (Patagonia, Argentina). Geologica Acta, 7:125–145. Ramaswamy, V. and R.R. Nair, 1994. Fluxes of material in the Arabian Sea and Bay of Bengal; sediment trap studies. Journal of Earth-System Science, 103:189–210. Ramis, D. and P. Bover, 2001. A review of the evidence for domestication of Myotragus balearicus Bate 1909 (Artiodactyla, Caprinae) in the Balearic Islands. Journal of Archaeo- logical Science, 28:265–282. Ramos, V.A., 2005. Seismic ridge subduction and topography: foreland deformation in the Patagonian Andes. Tectonophysics, 399:73–86. Ratcliffe, F.N., 1959. The rabbit in Australia. In Keast, A., R.L. Crocker, and C.S. Christian, eds., Biogeography and Ecology in Australia. The Hague: Junk, pp. 545–564. Raymond, B., J. McInnes, J.M. Dambacher, S. Way, and D.M. Bergstrom, 2011. Qualitative modeling of invasive species eradications on subantarctic Macquarie Island. Journal of Applied Ecology, 48:181–191. Ré, G.H., E. Bellosi, M. Heizler, et al., 2010. A geochronology for the Sarmiento Formation at Gran Barranca. In Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge, UK: Cambridge University Press, pp. 46–58. Réale, D., P. Boussès, B. Pisanu, and J.-L. Chapuis, 2000. Biannual reproductive cycle in the Kerguelen feral sheep population. Journal of Mammalogy, 81:169–178. Reguero, M.A. 1998. El problema de las relaciones sistemáticas y filogenéticas de los Typotheria y Hegetotheria (Mammalia, Notoungulata): Análisis de los taxones de Patagonia de la Edad- Mamífero Deseadense (Oligoceno). Doctoral thesis, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, 301 pp. Reguero, M.A., A.M. Candela, and R.N. Alonso, 2007. Biochronology and biostratigraphy of the Uquía Formation (Pliocene-early Pleistocene, NW Argentina) and its significance in the Great American Biotic Interchange. Journal of South American Earth Sciences, 23:1–16. Reguero, M.A., A.M. Candela, and G.H. Cassini, 2010. Hypsodonty and body size in rodent-like notoungulates. In Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., The Palaeontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. New York, NY: Cambridge University Press, pp. 362–368. Reguero, M.A. and E. Cerdeño, 2005. New late Oligocene Hegetotheriidae (Mammalia, Noto- ungulata) from Salla, Bolivia. Journal of Vertebrate Paleontology, 25:674–684. Reguero, M.A., D.A. Croft, J.J. Flynn, and A.R. Wyss, 2003b. Small archaeohyracids from Chubut, Argentina and central Chile; implications for trans-Andean temporal correlation. Fieldiana, Geology, new series, 48:1–17. Reguero, M.A., D.C. Croft, G.M. López, and R.N. Alonso, 2008. Eocene archaeohyracids (Mammalia; Notoungulata; Hegetotheria) from the Puna, northwest Argentina. Journal of South American Earth Sciences, 26:225–233. Reguero, M., F.J. Goin, C. Acosta Hospitaleche, T. Dutra, and S. Marenssi, 2013. Late Cretaceous/Paleogene West Antarctica Terrestrial Biota and its Intercontinental Affinities. SpringerBriefs in Earth Systems Sciences, Springer, DOI: 10.1007/978-94-007-5491-1. 392 References

Reguero, M.A. and F.J. Prevosti, 2010. Rodent-like notoungulates (Typotheria) from Gran Barranca, Chubut Province, Argentina: phylogeny and systematics. In Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., The Paleontology of Gran Barranca: Evolution and Environmental Change Through the Middle Cenozoic of Patagonia. Cambridge, UK: Cambridge University Press, pp. 152–169. Reguero, M.A., M. Ubilla, and D. Perea, 2003a. A new species of Eopachyrucos (Mammalia, Notoungulata, Interatheriidae) from the late Oligocene of Uruguay. Journal of Vertebrate Paleontology, 23:445–457. Reid, L.M. and M.J. Page, 2002. Magnitude and frequency of landsliding in a large New Zealand catchment. Geomorphology, 49:71–88. Reig, O.A., 1987. An assessment of the systematics and evolution of the Akodontini, with the description of new fossil species of Akodon (Cricetidae: Sigmodontinae). Fieldiana, Zoology, new series, 39:347–399. Reumer, J. and I. Robert, 2005. Two interesting taphonomical phenomena in remains of Artiodactyla (Mammalia: Cervidae, Bovidae). Darmstädter Beitráge zur Naturgeschichte, Heft 14:53–57. Riddle, E.E. and K.H. Cook, 2008. Abrupt rainfall transitions over the Greater Horn of Africa: observations and regional model simulations. Journal of Geophysical Research: Atmospheres, 113:14 pp. Rife, D.L., J.O. Pinto, A.J. Monaghan, C.A. Davis, and J.R. Hannan, 2010. Global distribution and characteristics of diurnally varying low-level jets. Journal of Climate 23:5041– 5064. Rimmington, G.M. and N. Nicholls, 1993. Forecasting wheat yields in Australia with the Southern Oscillation Index. Australian Journal of Agricultural Research, 44:625–632. Rinaldi, C., 1995. A new technique for assessing the incremental growth of rodent incisors. In Radlanski, R.J. and H. Renz, eds., Proceedings of the 10th International Symposium on Dental Morphology, Berlin, Germany, pp. 190–194. Rinaldi, C., 1999. Dentin Growth Increments: Insights into Rodent Paleobiology. PhD Thesis, University of Kansas, Lawrence, KS. Rinaldi, C. and T.M. Cole III, 2004. Environmental seasonality and incremental growth rates of beaver (Castor canadensis) incisors: implications for palaeobiology. Palaeogeography, Palaeoclimatology, Palaeoecology, 206:289–301. Risnes, S., 1986. Enamel apposition rate and the prism periodicity in human teeth. European Journal of Oral Sciences, 94:394–404. Robinson, C., J. Kirkham, and C.A. Nutman, 1988. Relationship between enamel formation and eruption rate in rat mandibular incisors. Cell and Tissue Research, 254:655–658. Rochette, P., E. Tamrat, G. Féraud, et al., 1998. Magnetostratigraphy and timing of the Oligocene Ethiopian traps. Earth and Planetary Science Letters, 164:497–510. Roelofsen, H.D., P.M. van Bodegom, L. Kooistra, and J.-P.M. White, 2013. Trait estimation in herbaceous plant assemblages from in situ canopy spectra. Remote Sensing, 5:6323– 6345. Rolett, B. and J. Diamond, 2004. Environmental predictors of pre-European deforestation on Paciﬁc islands. Nature, 431:443–446. Romero, E.J., 1986a. Fossil evidence regarding the evolution of Nothofagus Blume. Annals of the Missouri Botanical Garden, 73:276–283. Romero, E.J., 1986b. Paleogene phytogeography and climatology of South America. Annals of the Missouri Botanical Garden, 73:449–461. References 393

Rook, L., G. Gallai, and D. Torre, 2006. Lands and endemic mammals in the late Miocene of Italy: Constrains for paleogeographic outlines of Tyrrhenian area. Palaeogeography, Palaeo- climatology, Palaeoecology, 238:263–269. Rook, L., T. Harrison, and B. Engesser, 1996. The taxonomic status and biochronological implications of new finds of Oreopithecus from Baccinello (Tuscany, Italy). Journal of Human Evolution, 30:3–27. Rook, L., P. Renne, and M. Benvenuti, 2000. Geochronology of Oreopithecus-bearing succession at Baccinello (Italy) and the extinction pattern of European Miocene hominoids. Journal of Human Evolution, 39:577–582. Rose, J., X. Meng, and C. Watson, 1999. Palaeoclimate and palaeoenvironmental responses in the western Mediterranean over the last 140 ka; evidence from Mallorca, Spain. Journal of the Geological Society, 156:435–448. Rosenberg, G.D. and D.J. Simmons, 1980. Rhythmic dentinogenesis in the rabbit incisor: circadian, ultradian, and infradian periods. Calcified Tissue International, 32:29–44. Rosenberg, K.V. and R.J. Cooper, 1990. Approaches to avian diet analysis. Studies in Avian Biology, 51:408–418. Roth, S., 1903. Los ungulados sudamericanos. Anales del Museo de La Plata, Sección Paleonto- lógica, 5:1–36. Royle, S.A., 2001. A Geography of Islands: Small Island Insularity. London, UK: Routledge. Rudge, M.R., 1969. Reproduction of feral goats Capra hircus L. near Wellington, New Zealand. New Zealand Journal of Science, 12:817–827. Rudge, M.R., 1970. Dental and periodontal abnormalities in two populations of feral goats (Capra hircus L.) in New Zealand. New Zealand Journal of Science, 13:260–267. Rudge, M.R., 1976. Ageing domestic sheep (Ovis aries L.) from growth lines in the cementum of the first incisor. New Zealand Journal of Zoology, 3:421–424. Rudge, M.R., 1986. The decline and increase of feral sheep (Ovis aries L.) on Campbell Island. New Zealand Journal of Ecology, 9:89–100. Rudge, M.R. and J.M. Clark, 1978. The feral goats of Raoul Island, and some effects of hunting on their body size and population density. New Zealand Journal of Zoology, 5:582–589. Ruskin, B.G., F.M. Dávila, G.D. Hoke, et al., 2011. Stable isotope composition of middle Miocene carbonates of the Frontal Cordillera and Sierras Pampeanas: did the Paranaense seaway flood western and central Argentina? Palaeogeography, Palaeoclimatology, Palaeo- ecology, 308:293–303. Saint-Andre, P.-A., 1994. Contribution a l’etude des grands mammiferes du Neogene de l’altiplano bolivien. These doctoral, Museum National d’Histoire Naturelle, Paris. Salamy, K.A. and J.C. Zachos, 1999. Latest Eocene–Early Oligocene climate change and Southern Ocean fertility: inferences from sediment accumulation and stable isotope data. Palaeogeography, Palaeoclimatology, Palaeoecology, 145:61–77. Salinger, M.J., J.A. Renwick, and A.B. Mullan, 2001. Interdecadal Pacific Oscillation and South Pacific Climate. International Journal of Climatology, 21:1705–1721. Sánchez, M.V., M.G. González, and J.F. Genise, 2010b. Phytolith analysis of Coprinisphaera, unlocking dung beetle behaviour, herbivore diets and palaeoenvironments along the Middle Eocene–Early Miocene of Patagonia. Palaeogeography, Palaeoclimatology, Palaeoecology, 285:224–236. Sánchez, M.V., J.H. Laza, E.S. Bellosi, and J.F. Genise, 2010[a]. Ichnostratigraphy of middle Cenozoic Coprinisphaera from central Patagonia: insights into the evolution of dung 394 References

beetles, herbivores and grass-dominated habitats. Palaeogeography, Palaeoclimatology, Palaeoecology, 297:633–648. Sander, P.M., M.B. Leite, T.H. Mors, and W. Santel, 1994. Functional symmetries in the schmelzmuster and morphology of rootless rodent molars. Zoological Journal of the Linnean Society, 110:141–179. Sangster, A.G., M.J. Hodson, and H.J. Tubb, 2001. Silicon deposition in higher plants. In Datnoff, L.E., G.H. Snyder, and G.H. Korndörfer, eds., Silicon in Agriculture. Studies in Plant Science, 8:85–113. Sanson, G.D., 1980. The morphology and occlusion of the molariform cheek teeth in some Macropodinae (Marsupialia: Macropodidae). Australian Journal of Zoology, 28:341–365. Sanson, G.D., S.A. Kerr, and K.A. Gross, 2007. Do silica phytoliths really wear mammalian teeth? Journal of Archaeological Science, 34:526–531. Sarna-Wojcicki, A.M., C.E. Meyer, P.H. Roth, and F.H. Brown, 1985. Ages of tuff beds at East African early hominid sites and sediments in the Gulf of Aden. Nature, 313:306–308. Sarnthein, M., G. Tetzlaff, B. Koopmann, K. Wolter, and U. Pﬂaumann, 1981. Glacial and interglacial wind regimes over the eastern subtropical Atlantic and North-West Africa. Nature, 293:193–196. Savelli, C., 2002. Time-space distribution of magmatic activity in the western Mediterranean and peripheral orogens during the past 30 Ma (a stimulus to geodynamic considerations). Journal Geodynamique, 34:99–126. Scarano, A.C., 2009. El proceso de desarrollo de la hipsodoncia durante la transición Eoceno- Oligoceno: El caso de los ungulados autoctonos del orden Notoungulata (Mammalia). Tesis de Doctorado, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, Argentina. Scarano, A.C., A.A. Carlini, and A.W. Illius, 2011. Interatheriidae (Typotheria; Notoungulata), body size and paleoecology characterization. Mammalian Biology–Zeitschrift für Säugetier- kunde, 76:109–114. Schatz, W., 1994. Analyse des nördlichen Nabónbeckens (Ob. Miozän; Südecuador), Diplomar- beit an der Universität Zürich, Philosophische Fakultät, 213 pp. Scher, H.D. and E.E. Martin, 2004. Circulation in the Southern Ocean during the Paleo- gene inferred from neodymium isotopes. Earth and Planetary Science Letters, 228:391– 405. Scher, H.D. and E.E. Martin, 2006. Timing and climatic consequences of the opening of Drake Passage. Science, 312:428–430. Schmitt, D.N., D.B. Madsen, and K.D. Lupo, 2002. Small-mammal data on early and middle Holocene climates and biotic communities in the Bonneville Basin, USA. Quaternary Research, 58:255–260. Schubert, S.D., M.J. Suarez, P.J. Pegion, R.D. Koster, and J.T. Bacmeister, 2004. On the cause of the 1930s Dust Bowl. Science, 303:1855–1859. Schultz, J.E. and R.J. French, 1976. Silicon uptake by wheat and its relation to grain yield and water use. Australian Journal of Experimental Agriculture and Animal Husbandry, 16:123–128. Schumacher, S. and D. Lazarus, 2004. Regional differences in pelagic productivity in the late Eocene to early Oligocene–a comparison of southern high latitudes and lower latitudes. Palaeogeography, Palaeoclimatology, Palaeoecology, 214:243–263. Schuor, I. and S. Stedman, 1935. The growth pattern and daily rhythm of the incisor of the rat. Anatomical Record, 63:325–333. References 395

Scott, J.J. and J.B. Kirkpatrick, 2008. Rabbits, landslips and vegetation change on the coastal slopes of subantarctic Macquarie Island, 1980–2007: implications for mangement. Polar Biology, 31:409–419. Scott, W.B., 1913. A History of Land Mammals in the Western Hemisphere. New York, NY: MacMillan. Scott, W.B., 1937a. A History of Land Mammals in the Western Hemisphere, 2nd Edition. New York, NY: MacMillan. Scott, W.B., 1937b. The Astrapotheria. Proceedings of the American Philosophical Society, 77:309–393. Shadle, A.R., 1936. The attrition and extrusive growth of the four major incisor teeth of domestic rabbits. Journal of Mammalogy, 17:15–21. Shao, Y. and H. Lu, 2000. A simple expression for wind erosion threshold friction velocity. Journal of Geophysical Research, 105(D17):22 437–22 443. Shao, Y., G.N. Taff, and R.S. Lunetta, 2009. A Review of Selected MODIS Algorithms, Data Products, and Applications. Washington DC: Environmental Protection Agency. Sheets, P.D. and D.K. Grayson, 1979. Volcanic Activity and Human Ecology. New York, NY: Academic Press. Sheldon, N.D., G.J. Retallack, and S. Tanaka, 2002. Geochemical climofunctions from North American soils and application to paleosols across the Eocene–Oligocene boundary in Oregon. Journal of Geology, 110:687–696. Shockey, B.J., 1997a. Toxodontia of Salla, Bolivia (Late Oligocene): Taxonomy, Systematics, and Functional Morphology. PhD Dissertation, University of Florida, Gainesville. Shockey, B.J., 1997b. Two new notoungulates (Family Notohippidae) from the Salla beds of Bolivia (Deseadan, Late Oligocene): systematics and functional morphology. Journal of Vertebrate Paleontology, 17:584–599. Shockey, B.J. and F. Anaya, 2008. Postcranial osteology of mammals from Salla, Bolivia (Late Oligocene): form, function, and phylogenetic implications. In Sargis, E.J. and M. D’agosto, eds. Mammallian Evolutionary Morphology: A Tribute to Frederick S. Szalay. Dordrecht, the Netherlands: Springer, pp. 135–157. Shockey, B.J. and J.J. Flynn, 2007. Morphological diversity in the postcranial skeleton of Casamayoran (?Middle to Late Eocene) Notoungulata and foot posture in notoungulates. American Museum Novitates, 3601:1–26. Shoji, S., M. Nanzyo, and R. Dahlgren, eds., 1993. Volcanic Ash Soils; Genesis, Properties and Utilization. Amsterdam: Elsevier, Developments in Soil Science 21. Sicher, H., 1942. Tooth eruption: the axial movement of continuously growing teeth. Journal of Dental Research, 21:201–210. Sijp, W.P. and M.H. England, 2004. Effect of the Drake Passage throughflow on global climate. Journal of Physical Oceanography, 34:1254–1266. Silva, C.A. and B. Saavedra, 2008. Knowing for controlling: ecological effects of invasive vertebrates in Tierra del Fuego. Revista Chilena de Historia Natural, 81:123–136. Silver, I.A., 1969. The ageing of domestic animals. Science in Archaeology, 26:283–302. Simpson, G.G., 1932. Enamel on the teeth of an Eocene edentate. American Museum Novitates, 567:1–4. Simpson, G.G., 1933. A new crocodilian from the Notostylops beds of Patagonia. American Museum Novitates, 623:1–9. Simpson, G.G., 1945. The principles of classification and a classification of mammals. Bulletin of the American Museum of Natural History, 85:1–350. 396 References

Simpson, G.G., 1948. The beginning of the age of mammals in South America. 1. Introduction, Systematics; Marsupialia, Edentata, Condylarthra, Litopterna and Notioprogonia. Bulletin of the American Museum of Natural History, 91:1–232. Simpson, G.G., 1967. The beginning of the age of mammals in South America. 2. Systematics: Notoungulata, concluded (Typotheria, Hegetotheria, Toxodonta, Notoungulata incertae sedis); Astrapotheria; Trigonostylopoidea; Pyrotheria; Xenungulata; Mammalia incertae sedis. Bul- letin of the American Museum of Natural History, 137:1–259. Sinclair, M.R., 2002. Extratropical transition of southwest Pacific tropical cyclones: Part 1. Climatology and mean structure changes. Monthly Weather Review, 130:590–609. Sirocko, F., D. Garbe-Schönberg, and C. Devey, 2000. Processes controlling trace element geochemistry of Arabian Sea sediments during the last 25,000 years. Global and Planetary Change, 26:217–303. Sirocko, F., M. Sarnthein, H. Lange, and H. Erlenkeuser, 1991. Atmospheric summer circulation and coastal upwelling in the Arabian Sea during the Holocene and the Last Glaciation. Quaternary Research, 36:72–93. Skogland, T., 1988. Tooth wear by food limitation and its life history consequences in wild reindeer. Oikos, 51:238–242. Sloan, L.C. and E.J. Barron, 1992. Paleogene climatic evolution: a climate model investigation of the influence of continental elevation and sea-surface temperature upon continental climate. In Prothero, D.R. and W.A. Berggren, eds., Eocene-Oligocene Climatic and Biotic Evolution. Princeton, NJ: Princeton University Press, pp. 202–217. Smith, B.H., 1984. Patterns of molar wear in hunter–gatherers and agriculturalists. American Journal of Physical Anthropology, 63:39–56. Smith, B.H., 2000. ‘Schultz’sRule’ and the evolution of tooth emergence and replacement patterns in primates and ungulates. In Teaford, M.F., M.M. Smith, and W.J. Ferguson, eds., Development, Function and Evolution of Teeth. Cambridge, UK: Cambridge University Press, pp. 212–227. Smith, J., D. Vance, R.A. Kemp, et al., 2003. Isotopic constraints on the source of Argentinian loess, with implications for atmospheric circulation and the provenance of Antarctic dust during recent glacial maxima. Earth and Planetary Science Letters, 212:181–196. Smith, J.D., H.H. Genoways, and J.K. Jones, Jr., 1977. Cranial and dental anomalies in three species of platyrrhine monkeys from Nicaragua. Folia Primatologia, 28:1–42. Smith, S.P., 1887. Geological notes on the Kermadec Group. Transactions of the New Zealand Institute, 20:333–344. Sondaar, P.Y. and A.A.E. Van der Geer, 2005. Evolution and extinction of Plio-Pleistocene island ungulates. In Crégut-Bonnoure, E., ed., Les ongulés holarctiques du Pliocéne. Quaternaire, 2:241–256. Song, Z., J.F. Parr, and F. Guo, 2013. Potential of global cropland phytolith carbon sink from optimization of cropping system and fertilization. PLoS ONE, 8(9):73747. Spalletti, L.A. and M.M. Mazzoni, 1977. Sedimentologia del Grupo Sarmiento en un perfil ubicado al sudeste del Lago Colhue-Huapi, Provincia del Chubut. Revista del Museo de La Plata. Obra del Centenario, 4:261–283. Sparks, D.R. and J.C. Malechek, 1968. Estimating percentage dry weight in diet using a microscope technique. Journal of Range Management, 21:264–265. Spence, J.A., and G.U. Aitchison, 1985. Early tooth loss in sheep: a review. Veterinary Annuals, 25:125–133. Sponheimer, M., B.H. Passey, D.J. de Ruiter, et al., 2006. Isotopic evidence for dietary variability in the early hominin Paranthropus robustus. Science, 314:980–982. References 397

Spoor, C.F. and P.Y. Sondaar, 1986. Human fossils from the endemic island fauna of Sardinia. Journal of Human Evolution, 15:399–408. Springer, K., 2006. Macquarie Island–mammalian pests, past, present and future. Newsletter of the Invasive Species Specialist Group of the IUCN Species Survival Commission, 23:14–17. Spurgin, A.M., 1904. Enamel in the teeth of an embryo edentate (Dasypus novemcinctus Linn.). American Journal of Anatomy, 3:75–84. Steinmann, M., 1997. The Cuenca Basin of Southern Ecuador: Tectono-Sedimentary History and the Tertiary Andean Evolution. Doctoral Dissertation, Swiss Federal Institute of Technology, Zurich, ETH No. 12297. Steinmann, M., D. Hungerbühler, D. Seward, and W. Winkler, 1999. Neogene tectonic evolution and exhumation of the southern Ecuadorian Andes: a combined stratigraphy and ﬁssion-track approach. Tectonophysics, 307:255–276. Stephens, P.R., N.A. Trustrum, and D.L. Hicks, 1983. Experimental aerial photographic survey of erosion and catchment condition, Gladstone district, Wairarapa. In Stephens, P.R., ed., Remote Sensing for Soil Conservation. Water and Soil Miscellaneous Publication No. 52, Soil Conservation Center, Ministry of Works and Development, Palmerston North, NZ, pp.129–154. Steppan, S. 1995. Revision of the tribe Phyllotini (Rodentia, Sigmodontinae), with a phylogenetic hypothesis for the Sigmodontinae. Fieldiana Zoology, new series, 80:120 pp (Division of Mammals, USNM). Steppan, S.J., R.M. Adkins, and J. Anderson, 2004. Phylogeny and divergence-date estimates of rapid radiations in muroid rodents based on multiple nuclear genes. Systematic Biology, 53:533–553. Stirton, R.A., 1935. A review of the Tertiary beavers. University of California Publications in Geological Sciences, 23:391–458. Stirton, R.A., 1940. Phylogeny of North American Equidae. University of California Publications in Geological Sciences, 25:165–198. Stirton, R.A., 1947. Observations on evolutionary rates in hypsodonty. Evolution, 1:32–41. Stoddart, D.R. and R.P.D. Walsh, 1992. Environmental variability and environmental extremes as factors in the island ecosystem. Atoll Research Bulletin, 356:1–71. Stone, T. and M.L. Cupper, 2003. Last glacial maximum ages for robust humans at Kow Swamp, southern Australia. Journal of Human Evolution, 45:99–111. Storer, J.E., 1984. Mammals of the Swift Current Creek local fauna (Eocene: Uintan), Saskatch- ewan. Natural History Contributions, Saskatchewan Museum of Natural History, 7:1–158. Strömberg, C.A.E., 2006. Evolution of hypsodonty in equids: testing a hypothesis of adaptation. Paleobiology, 32:236–258. Strömberg, C.A.E., R.E. Dunn, R.H. Madden, M.J. Kohn and A.A. Carlini, 2013. Decoupling the spread of grasslands from the evolution of grazer-type herbivores in South America. Nature Communications, 4:1–8. Stromer, E., 1926. Reste land- und süsswasser bewohnender wirbeltiere aus den diamantenfel- dern Deutsch-Südwestafrikas. In Kaiser, E., ed., Die Diamantenwüste Sudwestafrikas. Berlin: Verlag von Dietrich Reimer, 2:107–153. Stuut, J.-B., I. Smalley, K. and O’Hara-Dhand, 2009. Aeolian dust in Europe: African sources and European deposits. Quaternary International, 198:234–245. Suckling, F.E.T., 1950. Te Awa Soil Conservation Experimental Station. Report on Three Years’ Experimental Work 1945–48. Manawatu Catchment Board and Soil Conservation Council, Wellington, New Zealand, 116 pp. 398 References

Suckling, F.E.T., 1954. Pasture management trials on unploughable hill country at Te Awa. I. Establishment of experimental area and results for 1949–51. New Zealand Journal of Science and Technology, A36:237–273. Suckling, F.E.T., 1959. Pasture management trials on unploughable hill country at Te Awa. II. Results for 1951–57. New Zealand Journal of Agricultural Research, 2:488–543. Suckling, F.E.T., 1964. Stocking rate trials at Te Awa. Sheepfarming Annual (Massey Agricul- tural College), 1964:18–32. Suckling, F.E.T., 1975. Pasture management trials on unploughable hill country at Te Awa. III. Results for 1959–69. New Zealand Journal of Experimental Agriculture, 3:351–436. Suckling, G.W. and M.R. Rudge, 1977. Changes with age in the length of central incisor teeth and their clinical crowns in sheep. New Zealand Journal of Agricultural Research, 20:145–149. Summerell, G.K., T.I. Dowling, D.P. Richardson, J. Walker, and B. Lees, 2000. Modelling current parna distribution in a local area. Australian Journal of Soil Research, 38:867–878. Sun, Y. and Z. An, 2005. Late Pliocene-Pleistocene changes in mass accumulation rates of eolian deposits on the central Chinese Loess Plateau. Journal of Geophysical Research, Atmospheres, 110:8 pp. Sundquist, B., 2011. The Earth’s Carrying Capacity: Some Related Reviews and Analyses. Topsoil Loss and Degradation: Causes, Effects and Implications: A Global Perspective [http://home. windstream.net/bsundquist1/]. Sutcliffe, A.J., 1973. Similarity of bones and antlers gnawed by deer to human artifacts. Nature, 246:428–430. Sykes, W.R., 1965. Notes on the 1964 eruption and the vegetation of Raoul Island. Proceedings of the New Zealand Ecological Society, 12:20–23. Szalay, F.S., 1977. Phylogenetic relationships and a classiﬁcation of the eutherian Mammalia. In Hecht, M.K., P.C. Goody, and B.M. Hecht, eds., Major Patterns in Vertebrate Evolution. New York, NY: Plenum Press, pp. 315–374. Tamene, L. and P.L.G. Vlek, 2008. Soil erosion studies in northern Ethiopia. Wind erosion in northern Ethiopia. In Braimoh, A.K. and P.L.G. Vlek, eds., Land Use and Soil Resources. Amsterdam, the Netherlands: Springer, pp. 73–100. Taylor, A.C. and E.O. Butcher, 1951. The regulation of eruption rate in the incisor teeth of the white rat. Journal of Experimental Zoology, 117:165–188. Taylor, B.W., 1955. The Flora, Vegetation and Soils of Macquarie Island. Australian Antarctic Division, Melbourne, Australia. Teaford, M.F. and P.S. Ungar, 2000. Diet and the evolution of the earliest human ancestors. Proceedings of the National Academy of Sciences of the United States of America, 97:13 506– 13 511. Tegen, I., S.P. Harrison, K. Kohfeld, et al. 2002. The impact of vegetation and preferential source areas on global dust aerosol: results from a model study. Journal of Geophysical Research, 107:AAC 14-11-AAC 14–27. Tegen, I., M. Werner, S.P. Harrison, and K.E. Kohfeld, 2004. Relative importance of climate and land use in determining present and future global soil dust emission. Geophysical Research Letters, 31:L05105. Ter Braak, C.J.F., 1995. Ordination. In Jongman, R.H.G., C.J.F. Ter Braak, and O.F.R. Van Tongeren, eds., Data Analysis in Community and Landscape Ecology. Cambridge, UK: Cambridge University Press, pp. 91–173. Ter Braak, C.J.F., 1996. Unimodal Models to Relate Species to Environment. DLO-Agricultural Mathematics Group, Wageningen, the Netherlands. References 399

Ter Braak, C.J.F. and P. Smilauer, 1998. CANOCO Reference Manual and User’s Guide to CANOCO for Windows: Software for Canonical Community Ordination (v.4). Center for Biometry, Wageningen, the Netherlands. Terry, R.C., 2008. Modeling the effects of predation, prey cycling, and time averaging on relative abundance in raptor-generated small mammal death assemblages. Palaios, 23:402–410. Terry, R.C., 2010a. On raptors and rodents: testing the ecological fidelity and spatio-temporal resolution of cave death assemblages. Paleobiology, 36:137–160. Terry, R.C., 2010b. The dead don’t lie: using skeletal remains for rapid assessment of historical small-mammal community baselines. Proceedings of the Royal Society, London, B, Biological Sciences, 277:1193–1201. Teruggi, M.E., 1955. Algunas observaciones microscopicas sobre vidrio volcánico y ópalo organógeno en sedientos pampianos. Notas del Museo de La Plata. Geología, 18:17–26. Teruggi, M.E., 1957. The nature and origin of Argentine loess. Journal of Sedimentary Petrology, 27:322–332. Tetley, J.H. and B.M. Langford, 1965. A study of nematode parasitism in hill-country breeding ewes. New Zealand Journal of Agricultural Research, 8:573–584. Thomas, H., 1984. Les origines africaines des Bovidae (Artiodactyla, Mammalia) miocenes des lignites de Grosseto (Toscane, Italie). Bulletin du Muséum national d’histoire naturelle. Section C., Sciences de la terre, paléontologie, géologie, minéralogie, 6:81–101. Thorn, V.C., 2004. Phytoliths from subantarctic Campbell Island: plant production and soil surface spectra. Review of Palaeobotany and Palynology, 132:37–59. Thorn, V.C., 2006. Vegetation reconstruction from soil phytoliths, Tongariro National Park, New Zealand. New Zealand Journal of Botany, 44:397–413. Thornton, O.G., 1938–9. Extraordinary flood discharges in some streams near Gisborne on 19th February 1938. Proceedings of the New Zealand Society of Civil Engineers, 25:65–72. Thurley, D.C., 1983. Studies of high tooth wear in Wairarapa. In. Orr, M., ed., Proceedings of a Scientists’ Meeting on Dental Abnormalities in Sheep, Wellington, New Zealand, pp. 31–33. Thurley, D.C., 1984. The pathogenesis of excessive wear in the deciduous teeth of sheep. New Zealand Veterinary Journal, 32:25–29. Thurley, D.C., 1985a. The pathogenesis of excessive wear in the permanent teeth of sheep. New Zealand Veterinary Journal, 33:24–26. Thurley, D.C., 1985b. Erosion of the non-occlusal surfaces of sheep’s deciduous teeth. New Zealand Veterinary Journal, 33:157–158. Toggweiler, J.R. and H. Bjornsson, 2000. Drake Passage and palaeoclimate. Journal of Quater- nary Science, 15:319–328. Tournouër, A., 1903a. Note sur la géologie et la paléontologie de la Patagonie. Bulletin de la Société Géologique de France Quatrième Série (Tome Troisième), 463–473. Tournouër, A., 1903b. Coupes des terrains tertiaires de la Patagonie. Compte Rendu Académie des Sciences, 137:348–349. Trauth, M.H., J.C. Larrasoaña, and M. Mudelsee, 2009. Trends, rhythms and events in Plio-Pleistocene African climate. Quaternary Science Reviews, 28:399–411. Trauth, M.H., M.A. Maslin, A. Deino, and M.R. Strecker, 2005. Late Cenozoic moisture history of East Africa. Science, 309:2051–2053. Tripati, A.K., J. Backman, H. Elderfiel, and P. Ferretti, 2005. Eocene bipolar glaciation associated with global carbon cycle changes. Nature, 436:341–346. Trumbull, R.B., U. Riller, O. Oncken, et al., 2006. The time-space distribution of Cenozoic volcanism in the South-Central Andes: a new data compilation and some tectonic 400 References

implications. In Oncken, O., G. Chong, G. Franz, et al., eds., The Andes, Springer Berlin, pp. 29–43. Trustrum, N.A., M.G. Lambert, and V.J. Thomas, 1983. The impact of soil slip erosion on hill country pasture production in New Zealand. Proceedings of the 2nd International Conference on Soil Erosion and Conservation, Honolulu, Hawaii. Soil Conservation Society of America. Trustrum, N.A. and P.R. Stephens, 1981. Selection of hill-country pasture measurement sites by interpretation of sequential aerial photographs. New Zealand Journal of Experimental Agriculture, 9:31–34. Tryon, C.A. and S. McBrearty, 2002. Tephrostratigraphy and the Acheulian to Middle Stone Age transition in the Kapthurin Formation, Kenya. Journal of Human Evolution, 42:211–235. Tsoar, H. and K. Pye, 1987. Dust transport and the question of desert loess formation. Sediment- ology, 34:139–153. Tudhope, A.W., C.P. Chilcott, M.T. McCulloch, et al., 2001. Variability in the El Niño-Southern Oscillation through a Glacial-Interglacial cycle. Science, 291:1511–1517. Tummers, M. and I. Thesleff, 2003. Root or crown: a developmental choice orchestrated by the differential regulation of the epithelial stem cell niche in the tooth of two rodent species. Development, 130:1049–1057. Ugolini, F.C. and R.J. Zasoski, 1979. Soils derived from tephra. In Sheets, P.D. and D.K. Grayson, eds., Volcanic Activity and Human Ecology. New York, NY: Academic Press, pp. 83–124. Umazano, A.M., E.S. Bellosi, G. Visconti, G.A. Jalfin, and R.N. Melchor, 2009. Sedimentary record of a late Cretaceous volcanic arc in central Patagonia: petrography, geochemistry and provenance of fluvial volcaniclastic deposits of the Bajo Barreal Formation, San Jorge Basin, Argentina. Cretaceous Research, 30:749–766. Umer, M., H.F. Lamb, R. Bonnefille, et al., 2007. Late Pleistocene and Holocene vegetation history of the Bale Mountains. Ethiopia Quaternary Science Reviews, 26:2229–2246. Uno, K.T., T.E. Cerling, J.M. Harris, et al., 2011. Late Miocene to Pliocene carbon isotope record of differential diet change among East African herbivores. Proceedings of the National Academy of Sciences of the United States of America, 108:6509–6514. Van der Geer, A.A.E., 2005. Island ruminants and the evolution of parallel functional structures. In: Cregut, E., ed., Les ongulés holarctiques du Pliocène et du Pléistocène. Actes Colloque International Quaternair (hors-série) 2:231–240. Van der Geer, A.A.E., 2008. The effect of insularity on the Eastern Mediterranean early cervoid Hoplitomeryx: the study of the forelimb. Quaternary International, 182:145–159. Van der Geer, A., G. Lyras, J. de Vos, and M. Dermitzakis, 2010. Evolution of Island Mammals: Adaptation and Extinction of Placental Mammals on Islands. Hoboken, NJ: Wiley-Blackwell. Van der Made, J., 1988. Sus nanus, nov. sp., a Pliocene dwarf pig from Capo Figari (Northeastern Sardinia). Bolletimo della Societe Paleontologica Italiana, 27:367–378. Van der Made, J., 1999. Biogeography and stratigraphy of the Mio-Pleistocene mammals of Sardinia and the description of some fossils. In Reumer, J.W.F. and J. de Vos, eds., Elephants Have a Snorkel! Papers in Honour of Paul Y. Sondaar. Deinsea, Jaarbericht van het Natuur- historisch Museum Rotterdam, 7:337–360. Van der Made, J., 2004. The status of Conohyus giganteus (Nyanzachoerini, Tetraconodontinae, Suidae)–Reply to Pickford (2001). Transactions of the Royal Society of Edinburgh, Earth Sciences, 94:157–167. Van der Made, J., 2005. The fossil endemic goat Nesogoral cenisae n.sp. from Campidano, Sardinia–cursorial adaptations in insular environment. In Alcover, J.A. and P. Bover, eds., References 401

Proceedings of the International Symposium “Insular Vertebrate Evolution: The Palaeonto- logical Approach.” Monografías de la Societat d’Historia Natural de les Balears, 12:347–368. Van der Made, J., 2008. New endemic large mammals from the Lower Miocene of Oschiri (Sardinia): observations on evolution in insular environment. Quaternary International, 182:116–134. Van der Made, J. and M.R. Palombo, 2004. Megaloceros sardus n. sp., a large deer from the Pleistocene of Sardinia. Hellenic Journal of Geosciences, 41:163–176. Van der Made, J. and J. Rodriguez, 2003. Increased molar enamel thickness as an adaptation to insular environment. In Alcover, J.A. and P. Bover, eds., Insular Vertebrate Evolution, the Paleontological Approach. Proceedings of the International Symposium, Palma de Mallorca, September 16–19, 2003, Monografies de la Societat d’Història Natural de les Balears, 12: Abstract pp. 74–75. Van Roosmalen, M.G.M., 1980. Habitat Preferences, Diet, Feeding Strategy, and Social Organ- ization of the Black Spider Monkey (Ateles paniscus paniscus) in Surinam. PhD Thesis at the Agricultural University of Wageningen, Holland and published as Report 80/13, Rijksinstituut voor Natuurbeheer, Leersum, Holland, 175 pp. Van Roosmalen, M.G.M., 1985. A Guide to the Fruits of the Guianan Flora. Wageningen, Holland: University of Utrecht Press/Veenman, 517 pp. Van Vuren, D. and B.E. Coblentz, 1988. Dental anomalies of feral goats (Capra hircus)on Aldabra Atoll. Journal of Zoology, London, 216:503–505. Vella, P., W. Kaewyana, and C.G. Vucetich, 1988. Late Quaternary terraces and their cover beds, north-western Wairarapa, New Zealand, and provisional correlations with oxygen isotope stages. Journal of the Royal Society of New Zealand, 18:309–324. Ventura, E. Jr. and L.D. Norton, 2001. Controlling Interrill and Rill Erosion in a Highly Erodible Volcanic Soil. 2001 Annual Meeting of the American Society of Agricultural and Biological Engineers, St. Joseph, MI, Paper 012074. Verdú, J.R. and E. Galante, 2002. Climatic stress, food availability and human activity as determinants of endemism patterns in the Mediterranean region: the case of dung beetles (Coleoptera, Scarabaeoidea) in the Iberian Peninsula. Diversity and Distributions, 8:259–274. Verzi, D.H., 2001. Phylogenetic position of Abalosia and the evolution of the extant Octodontinae (Rodentia, Caviomorpha, Octodontidae). Acta Theriologica, 46:243–268. Verzi, D.H., 2002. Patrones de evolución morfológica en Ctenomyinae (Rodentia, Octodontidae). Mastozoología Neotropical, 9:309–328. Verzi, D.H. and C.I. Montalvo, 2008. The oldest South American Cricetidae (Rodentia) and Muste- lidae (Carnivora): late Miocene faunal turnover in central Argentina and the Great American Biotic Interchange. Palaeogeography, Palaeoclimatology, Palaeoecology, 267: 284–291. Verzi, D.H., C.I. Montalvo, and C.M. Deschamps, 2008. Biostratigraphy and biochronology of the Late Miocene of central Argentina: evidence from rodents and taphonomy. Geobios, 41:145–155. Verzi, D.H. and A.I. Olivares, 2006. Craniodental joint in South American burrowing rodents (Ctenomyidae): adaptations and constraints related to a specialized mandibular position in digging. Journal of Zoology, 270:488–501. Verzi, D.H., E.C. Vieytes, and C.I. Montalvo, 2011. Dental evolution in Neophanomys (Rodentia, Octodontidae) from the late Miocene of central Argentina. Geobios 44:621–633. Vieytes, E.C., 2003. Microestructura del esmalte de roedores Hystricognathi sudamericanos fósiles y vivientes. Significado morfofuncional y filogenético. Doctoral Thesis, Universidad Nacional de La Plata, Argentina, 200 pp. 402 References

Vigne, J.-D., 1992. Zooarchaeology and the biogeographical history of the mammals of Corsica and Sardinia since the last ice age. Mammal Review, 22:87–96. Vila, G., C. Fioroni, L. Pea, S. Bohaty, and D. Persico, 2008. Middle Eocene–late Oligocene climate variability: calcareous nannofossil response at Kerguelen Plateau, Site 748. Marine Micropaleontology, 69:173–192. Vile, D., E. Garnier, B. Shipley, et al., 2005. Speciﬁc leaf area and dry matter content estimate thickness in laminar leaves. Annals of Botany, 96:1129–1136. Virgo, K.J. and R.N. Munro, 1978. Soil and erosion features of the Central Plateau region of Tigrai, Ethiopia. Geoderma, 20:131–157. Viste, E. and A. Sorteberg, 2013. Moisture transport into the Ethiopian highlands. International Journal of Climatology, 33:249–263. Voorhies, M.R., 1985. A Miocene rhinoceros herd buried in volcanic ash. National Geographic Society Research Reports, 19:671–688. Vrba, E.S., E Vrba, G Denton, T Partridge, and L Burckle, eds., 1995. Paleoclimate and Evolution, with Emphasis on Human Origins. New Haven, CT: Yale University Press, pp. 262–288. Vucetich, M.G., 1989. Rodents (Mammalia) of the Lacayani fauna revisited (Deseadan, Bolivia): comparison with New Chinchillidae and Cephalomyidae from Argentina. Bulletin Museum National de Histoire Naturelle, Paris, Series 4, 11:233–247. Vucetich, M.G., C.M. Deschamps, A.I. Olivares, and M.T. Dozo. 2005. Capybaras, size, shape, and time: a model kit. Acta Palaeontologica Polonica, 50:259–272. Vucetich, M.G., M.M. Mazzoni, and U.F.J. Pardiñas, 1993. Los roedores de la Formación Collon Cura (Mioceno medio), y la ignimbrita Pilcaniyeu, Cañadon del Tordillo, Neuquen. Ameghini- ana, 30:361–381. Vucetich, M.G. and A.M. Ribeiro, 2003. A new and primitive rodent from the Tremembé Formation (late Oligocene) of Brazil, with comments on the morphology of the lower premolars of caviomorph rodents. Revista Brasileira de Paleontologia, 5:73–82. Vucetich, M.G., D.H. Verzi, and J.-L. Hartenberger, 1999. Review and analysis of the radiation of the South American Hystricognathi (Mammalia, Rodentia). Compte Rendus de l’Academie des Sciences, Paris, Sciences de la Terre et des Planetes, 329:763–769. Vucetich, M.G., E.C. Vieytes, M.E. Pérez, and A.A. Carlini, 2010. The rodents from La Cantera and the early evolution of caviomorphs in South America. In Madden, R.H., A.A. Carlini, M.G. Vucetich, and R.F. Kay, eds., The Paleontology of Gran Barranca: Evolution and Environ- mental Change Through the Middle Cenozoic of Patagonia. Cambridge, UK: Cambridge University Press, pp.193–205. Wade, M.H. and P.C. de F. Carvalho, 2000. Defoliation patterns and herbage intake on pastures. In Lemaire, G., J. Hodgson, A. de Moraes, C. Nabinger and P.C. de F. Carvalho, eds., Grassland Ecophysiology and Grazing Ecology. Wallingford, UK: CABI Publishing, pp. 233–248. Walker, P.H. and A.B. Costin, 1971. Atmospheric dust accession in south-eastern Australia. Australian Journal of Soil Research, 9:1–5. Walker, S., A.F. Mark, and J.B. Wilson, 1995. The vegetation of Flat Top Hill: an area of semiarid grassland/shrubland in central Otago, New Zealand. New Zealand Journal of Ecology, 19:175–194. Warkentin, B.P. and T. Maeda, 1980. Physical and mechanical characteristics of andisols: soils with variable charge. New Zealand Society of Soil Science, 1980:303–323. Washington, R., M. Todd, N.J. Middleton, and A.S. Goudie, 2003. Dust-storm source areas determined by the Total Ozone Monitoring Spectrometer and surface observations. Annals of the Association of American Geographers, 93:297–313. References 403

Wasson, R.J., 1994. Annual and decadal variation in sediment yield in Australia, and some global comparisons. In Variability in Stream Erosion and Sediment Transport. Proceedings of the Canberra Symposium, IAHS Publication 224, pp. 269–279. Wasson, R.J. and R.W. Galloway, 1986. Sediment yield in the Barrier Range before and after European settlement. Rangelands Journal, 8:79–90. Wasson, R.J., R.K, Mazari, B. Starr, and G. Clifton, 1998. The recent history of erosion and sedimentation on the Southern Tablelands of southeastern Australia: sediment flux dominated by channel incision. Geomorphology, 24:291–308. Watson, J.S., 1961. Feral rabbit populations on Pacific islands. Pacific Science, 15:591–593. Wegner, A., P. Gabrielli, D. Wilhelms-Dick, et al., 2011. Rare earth elements from an ice core in the Atlantic sector of Antarctica indicate a dust provenance change at the end of the last deglaciation. Climate of the Past Discussions, 7:601–633. Weinreb, M.M. and Y. Sharav. 1964. Tooth development in sheep. American Journal of Veterinary Research, 25:891–908. Weldeab, S., W. Siebel, R. Wehausen, et al., 2003. Late Pleistocene sedimentation in the Western Mediterranean Sea: implications for productivity changes and climatic conditions in the catchment areas. Palaeogeography, Palaeoclimattology, Palaeoecology, 190:121–137. Wen, D., 1993. Soil erosion and conservation in China. In Pimentel, D., ed., World Soil Erosion and Conservation. Cambridge, UK: Cambridge University Press, pp.63–86. West, D.M., 2002. Dental disease of sheep. New Zealand Veterinary Journal, 50:102–104. Western, D., 1979. Size, life history and ecology in mammals. African Journal of Ecology, 17:185–204. White, T.D., G. Suwa, and B. Asfaw, 2000. Jaws and teeth of Australopithecus afarensis from Make, Middle Awash, Ethiopia. American Journal of Physical Anthropology, 111:45–68. Whitehouse, I.E., 1984. Erosion in the eastern South Island high country–a changing perspective. Journal of the Tussock Grasslands and Mountainlands Institute, 42:3–23. Wilf, P., N.R. Cúneo, K.R. Johnson, et al., 2003. High plant diversity in Eocene South America: evidence from Patagonia. Science, 300:122–125. Wilf, P., K.R. Johnson, N.R. Cúneo, et al., 2005. Eocene plant diversity at Laguna del Hunco and Río Pichileufú, Patagonia, Argentina. American Naturalist, 165:634–650. Wilkinson, M.J., L.G. Marshall, J.G. Lundberg, and M.H. Kreslavsky, 2010. Megafan environments in northern South America and their impact on Amazon Neogene aquatic ecosystems. In Hoorn, C. and F. Wesselingh, eds., Amazonia: Landscape and Species Evolution: A Look into the Past. Hoboken, NJ: Wiley-Blackwell, pp. 162–184. Williams, G.R. and M.R. Rudge, 1969. A population study of feral goats (Capra hircus L.) from Macauley Island, New Zealand. Proceedings of the New Zealand Ecological Society, 16:17–28. Williams, K., I. Parer, B. Coman, J. Burley, and M. Braysher, 1995. Managing Vertebrate Pests: Rabbits. Bureau of Resource Sciences and CSIRO, Victoria, Australia. Wilmshurst, J.M. 1997. The impact of human settlement on vegetation and soil stability in Hawke’s Bay, New Zealand. New Zealand Journal of Botany, 35:97–111. Wilmshurst, J.M., A.J. Anderson, T.F.G. Higham, and T.H. Worthy, 2008. Dating the late prehistoric dispersal of Polynesians to New Zealand using the commensal Pacific rat. Proceed- ings of the National Academy of Sciences of the United States of America, 105:7676–7680. Wilmshurst, J.M., K.L. Bestic, C.D. Meurk, and M.S. McGlone, 2004. Recent spread of Draco- phyllum scrub on subantarctic Campbell Island, New Zealand: climatic or anthrogenic origins? Journal of Biogeography, 31:401–413. 404 References

Wilson, P.R. and D.F.G. Orwin, 1964. The sheep population of Campbell Island. New Zealand Journal of Science, 7:460–490. Wilson, R.W., 1951. Evolution of the early Tertiary rodents. Evolution, 5:207–215. Wise, S.W. Jr., J.R. Breza, D.M. Harwood, W. Wei, and J.C. Zachos, 1992. Paleogene glacial history of Antarctica in light of Leg 120 drilling results. Proceedings of the Ocean Drilling Program, Scientific Results, 120:1001–1030. WoldeGabriel, G., W.K. Hart, S. Katoh, Y. Beyene, and G. Suwa, 2005. Correlation of Plio- Pleistocene tephra in Ethiopian and Kenyan rift basins: temporal calibration of geological features and hominid fossil records. Journal of Volcanology and Geothermal Research, 147:81–108. WoldeGabriel, G., G. Heiken, T.D. White, et al., 2000. Volcanism, tectonism, sedimentation, and the paleoanthropological record in the Ethiopian Rift System. In McCoy, F.W. and G. Heiken, eds., Volcanic Hazards and Disasters in Human Antiquity. Geological Society of America Special Paper 345:83–99. Wood, A.E. and B. Patterson, 1959. The rodents of the Deseadan Oligocene of Patagonia and the beginnings of South American rodent evolution. Bulletin of the Museum of Comparative Zoology, 120:282–428. Wood, B. and P. Constantino, 2007. Paranthropus boisei: fifty years of evidence and analysis. Yearbook of Physical Anthropology, 50:106–132. Wood, B. and M. Leakey, 2011. The Omo–Turkana Basin fossil hominins and their contribution to our understanding of human evolution in Africa. Evolutionary Anthropology, 20:264–292. Wood, B. and D. Strait, 2004. Patterns of resource use in early Homo and Paranthropus. Journal of Human Evolution, 46:119–162. World Resources Institute, 1992. World Resources 1992–93: A report by the WRI in collabor- ation with the United Nations Environmental Programme and the United Nations Development Programme. New York, NY: Oxford University Press. World Resources Institute, 2002. Drylands, People, and Ecosystem Goods and Services: a Web- based Geospatial Analysis. [Retrieved January 10, 2011 from http://www.wri.org.] Worster, D., 1982. Dust Bowl: the Southern Plains in the 1930s. Oxford, UK: Oxford University Press. Wright, A.C.S., and A.J. Metson, 1959. Soils of Raoul (Sunday) Island, Kermadec Group. New Zealand Department of Scientific and Industrial Research, Soil Bureau Bulletin, 10, 49 pp. Wyss, A.R., J.J. Flynn, M.A. Norell, et al., 1993. South America’s earliest rodent and recognition of a new interval of mammalian evolution. Nature, 365:434–437. Wyss, A.R., J.J. Flynn, M.A. Norell, et al., 1994. Paleogene mammals from the Andes of Central Chile: a preliminary taxonomic, biostratigraphic, and geochronologic assessment. American Museum Novitates, 3098:449–454. Yamada, F. and F.A. Cervantes, 2005. Pentalagus furnessi. Mammalian Species, 782:1–5. Yang, W., B. Tan, D. Huang, et al., 2006. MODIS Leaf Area Index products: from validation to algorithm improvement. IEEE Transactions on Geoscience and Remote Sensing, 44:1885–1898. Yll, R., R. Perez-Obiol, and J.A. Alcover, 2002. Palynological analysis of Myotragus balearicus coprolites, the extinction of animal and vegetal species during the Holocene in the Balearic Islands (Spain). Abstracts of the Proceedings of the Thirty-Fifth Annual Meeting of the American Association of Stratigraphic Palynologists, p.251. Yu, B. and D. Neil, 1994. Temporal and spatial variation of sediment yield in the Snowy Mountains region, Australia. In Variability in Stream Erosion and Sediment Transport. Pro- ceedings of the Canberra Symposium, IAHS Publication 224, pp. 281–289. References 405

Yuretich, R.F., 1979. Modern sediments and sedimentary processes in Lake Rudolf (Lake Turkana) eastern Rift Valley, Kenya. Sedimentology, 26:313–331. Zachos, J.C., T.M. Quinn, and K.A. Salamy, 1996. High-resolution (104 years) deep-sea foraminiferal stable isotope records of the Eocene–Oligocene climate transition. Paleocean- ography, 11:251–266. Zajicek, G., 1976. The rodent incisor tooth proliferon. Cell Proliferation, 9:207–214. Zecchetto, S. and F. De Biasio, 2007. Sea surface winds over the Mediterranean basin from satellite data (2000–04): meso- and local-scale features on annual and seasonal time scales. Journal of Applied Meteorology and Climatology, 46:814–827. Zeder, M.A., 2002. Reconciling rates of long bone fusion and tooth eruption and wear in sheep (Ovis) and goats (Capra). In Ruscillo, D., ed., Recent Advances in Ageing and Sexing Animal Bones. Proceedings of the 9th Conference of the International Council of Archaeozoology, Oxford, UK: Oxbow Books, pp. 87–118. Zeleke, T., F. Giorgi, G. Mengistu Tsidu, and G.T. Diro, 2013. Spatial and temporal variability of summer rainfall over Ethiopia from observations and a regional climate model experiment. Theoretical and Applied Climatology, 111:665–681. Zhang, X., N. Drake, and J. Wainwright, 1998. Downscaling Land Surface Parameters for Global Soil Erosion Estimation Using no Ancillary Data. Department of Geography, King’s College London [http://www.geocomputation.org/1998/55/gc_55.htm]. Zinsmeister, W.J., 1981. Middle to late Eocene invertebrate fauna from the San Julian Formation at Punta Casamayor, Santa Cruz Province, southern Argentina. Journal of Paleontology, 55:1083–1102. Zucol, A., M. Brea, and E.S. Bellosi, 2010. Phytolith analysis in Gran Barranca (central Patagonia): the middle-late Eocene. In Madden, R.H., A.A. Carlini, M.G. Vucetich and R.F. Kay, eds., The Paleontology of Gran Barranca. Cambridge, UK: Cambridge University Press, pp. 317–340. Zucol, A.F., M.M. Mazzoni, R.H. Madden, 1999. Análisis ﬁtolítico de la secuencia sedimen- taria de Gran Barranca, Chubut. Primer Encuentro Argentino de Investigaciones Fitolíticos (Diamante, Entre Rios), pp. 11–12. Index

?Acoelodus, 49 Alcideorbignya, 51, 52 ?Acoelohyrax, 43 Alfredton, 97 ?Paginula, 49 Allia Bay, 214 “Megaceroides cretensis”, 160 alligator. See Alligatoridae “Pseudostylops subquadratus”, 47 Alligatoridae, 248 % terrigenous, 200, 215 Alouatta palliata, 145 Alpine–Himalayan volcanic belt, 257 Aboriginal tooth size, 147 altiplano, 61, 66, 154, 280, 283, 313, 317 aboriginals, 330, 341 altiplano and puna plateaus, 209 Abothrix, 60 alveolar bone, 297–298 Acacia-savanna, 209 Amazonian Peru, 284 Acaena magellanica, 308 Amblypoda, 52 Acantholippia, 316 Ameghino, Carlos, 2 acid-insoluble residue, 98, 132 Ameghino, Florentino, 2, 51 acid-insoluble residue in fecal material (AIRf), 122, Amsterdam Island, 308 126, 150, 326, 329 Ancylocoelus, 271 acid-insoluble residue in pasture grasses (AIRp), Andean batholith complex, 78 318 Andean mountain building, 70 Acoelohyrax, 43 Andes, 57, 61, 77, 241, 262, 280, 283, 297, 313, Acropithecus, 27, 270 315 Acropithecus rigidus, 271 andesite lava, 179 Adelaide, 147 Andesite Line, 145, 165, 257, 330, 341 Adianthidae, 52 andesitic volcanism, 77, 146, 165, 308 Adinotherium, 23–24 Andinodus, 52 Adobe Photoshop (v5.0), 293 andisol, 60, 71, 76, 153, 176, 209, 255, 257, 280 aerial top-dressing, 89 andisol erodibility, 257 aerosol dust composition, 134–135 Andreis, Renato, 6 aerosol optical depth (AOD), 140 Andrews, Charles W., 156 Afar Basin, 231 animalivory, 62 Afar Plateau, 332 Anisotemnus, 42, 272 Afrotheria, 52 annual amplitude of mean monthly temperature, 73 age mark birth cohorts, 87 annual frequency of dust storms, 303 Agrostis, 179 annual tooth wear, 114–115 Agrostis magellanica, 180 Antarctic Circumpolar Current, 242–244 AIRf. See acid-insoluble residue Antarctic Peninsula, 243 Akodon, 60 Antarctica, 40, 237, 342 Akodon azarae, 67 Antepithecus brachystephanus, 46 Akodontini, 60, 63 Antepithecus innexus, 46 Alaska, 338 Anthracomys majori, 158 Alaska Peninsula, 209 Antilocapra, 1 Albertine Graben, 207 Antofagasta de la Sierra, 313, 316 Albertogaudrya, 50 Anzac rains, 85, 113 Albertogaudryidae, 50 AOD. See aerosol optical depth (AOD) Alcelaphinae, 155 Aorangi Mountains, 92

406 Index 407

Apodemus, 160 ENSO drought conditions, 135 Arabian Sea, 193, 198, 234, 332, 338 environmental variables, 136 Archaeohyracidae, 27, 36, 39, 41, 44, 236, 284 fluvial-eolian interaction, 142 Archaeohyrax, 27, 34, 44 time series analysis, 137 Archaeohyrax patagonicus, 44 wet climate processes, 141 Archaeolaginae, 311 studies of sheep tooth wear, 121 Archaeophylus patrius, 46 dust flux and soil ingestion, 132 Archaeopithecidae, 271 fecal silica, 124 Archaeotypotherium, 27, 41, 44 methods, 124 Archaeotypotherium propheticus, 44 phytolith counts, 124 Arctocyonia, 52 questions unanswered, 130 Arctostylopidae, 52 scientific impact, 122 Ardipithecus, 193 study site, 124 Ardipithecus ramidus, 198, 219 tooth wear, 124 Arequipa Department, Peru, 66 Australian aboriginals, 145 Argentina, 13, 257 australopithecine(s), 193, 334 Argentine Basin, 277, 338 Australopithecus, 193, 197–198, 233 Argyrohippus, 271, 299 Australopithecus (=Paranthropus) boisei, 193, Argyrohippus fraterculus, 27, 47 219 Argyrolagidae, 13, 286, 323 Australopithecus aethiopicus, 193 Argyrolagoidea, 18, 38, 236 Australopithecus afarensis, 193, 198 arid-adapted plants, 252 Australopithecus anamensis, 198 aridisols, 61 Avena, 58 aridlands, 82, 284 Avena sativa, 132 armadillo(s), 272, 286, 298, 312 Awash Valley, 228 Arnold, G.W., 123 Artiodactyla, 53, 154 B-Tulu Bor Tuff, 207 Asmodeus, 271 Bajo Barreal Formation, 256 Asteraceae, 180 Baker, George, 122, 131 Astraponotus, 50, 271 Bale Mountains, 209 Astraponotus beds. See Mustersan SALMA Balearic archipelago, 154 Astrapotheria, 37, 51–52, 236 Balearic Promontory, 157 Astrapotheriidae, 50 Baluchistan, 210 Astrapotheriidae, 37, 50, 236, 271 bamboos, 264 Astrapotherium, 50 Bare Island, 305 Astrapotherium? ruderarium, 37 Baringo Basin, 207 Atacama Desert, 316 Barnicoat, C.R., 86 Ateles, 145 Barrancan. See Barrancan SALMA atmospheric paleotemperatures, 248 Barrancan SALMA, 7, 277, 313 Auckland, New Zealand, 260 Barreda, Viviana, 5 Auricularia, 177 Barytheria, 52 Austral Basin, 241 Bay of Plenty, 114, 307 Australia, 120, 133, 141, 146, 234, 258, 284, 301, Beadle, Noel, 131 328, 338–339 beaver. See Castor canadensis desert and grasslands, 120 benchmarks of eruption and onset of wear, 173 driest, lowest, flattest, 120 Berry, Edward W., 5 Dust Storm Index, 133 Bertoldi de Pomar, Hety, 6, 263 kangaroos and wallabies (Macropodidae), 120 BEW. See benchmark of eruption and onset of modern humans wear high-wear environments, 145 Bifidipes aeolis ichnospecies, 157 in Oceania, 145–147 binning the data, 227 tooth size, 144 Black Pumice tuff, 207 tooth size variation, 147 Black-tailed jackrabbits. See Lepus californicus tooth wear gradients, 148 Blechnum, 177 southeast dust path body size, 226–227 dry climate processes, 138 Bolivia, 252, 257, 280 dust composition, 134 Bolomys, 60 408 Index

Bolomys obscurus, 67 forward selection, 77 Bos, 288 ranked interset correlations, 76 Bos indicus, 302 Cape Gargano, 154 Bosque Petriﬁcado, 61 Cape Verde Islands, 163 Bougainville, 146 Capra aegagrus, 308 bovid. See Bovidae Capra hircus, 164, 331 Bovidae, 154, 156, 158, 298 Capraia Islands, 158 Bowman, Isaiah, 66 Caprinae, 154 brachiolite, 264 Carnac Island, 306 Brachylagus idahoensis, 321 carnivory, 62 Brandt, Johann Friedrich von, 1 Carodnia, 52 Braun, Janet K., 59 Carolozittelia, 52 Brazil, 266 Carterton, 91 Brazil Current, 240–241 Carumbium, 179 Brioli, Ferdinand, 4 Casamayoran SALMA, 4, 43 Broadbeach, 151 Cascade range, 209 Broken Hill, 136 Castor canadensis, 7, 42, 289, 314 Bruere, A. Neil, 90 Castoridae, 57 Brule Formation, 310 Catamarca Province, Argentina, 315 Buenos Aires, 57 cattle, 50, 57, 89, 302, 308. See Bos Buenos Aires Province, 67, 266 Cavia aperea, 313 bulliform phytoliths, 264 caviid. See Caviidae Burdekin river, 302 Caviidae, 18 Burrinjuck Reservoir, 302 Caviomorpha, 13, 40, 57, 236, 284, 314 Buxaceae, 157 ceja, 66 Buxus balearica, 157 cementum, 296–297 Centinela Formation, 278

C23-C33 n-alkanes MAR, 228 Central Andean Volcanic Zone, 61, 79, 209, 315 C3 woodland, 229 Central Andes, 13, 19, 27, 284, 313 C30 n-alkanoic acid, 227 central Arabia, 202 C4 diet, 233 Central Volcanic Plateau, 91, 100 C4 feeding, 228 Cephalomyidae, 13 caatingas, 266 Cephalomys, 13 Cabeza Blanca, 40, 48–49 Cerdas, 313 Cailloma, 66 Cerling, Thure E., 203 Caiman, 248 cerrado savannas, 263 Caiman jacare, 248 Cerro Barcino Formation, 256 Caiman latirostris, 249 Cerro Galan, 320 Calomys, 63 Cervidae, 159, 330 Calomys laucha, 67 Cervus, 160 Calomys musculinus, 67 Chaco Province, 249 Camargo Formation, 283 Chadron Formation, 310 Camarones, 277 Chadronian. See Chadronian NALMA Camelidae, 19, 154, 315, 323 Chadronian NALMA, 310 Campanorco, 45 Chamaerops humilis, 250 Campbell Island, 166, 171, 180, 186, 189–190 Chari Tuff, 207 Campbell Plateau, 247 Chatham Islands, 250 Cañadon Blanco, 45, 48, 277 Chelemys, 60 Cañadon Hondo, 39 Chemeron Formation, 207 Cañadon Vaca, 34, 41, 49 Chiguata, 66 Canary Islands, 163, 257, 258 Chile, 64, 250, 252, 257, 283 Canberra, 123, 303, 329 China, 260 Candiacervis, 160 Chinchilla laniger, 297 cangagua aeolica, 61 chinchillid. See Chinchillidae canonical community ordination (CANOCO), Chinchillidae, 13 73–74 Chinchilulla, 63 CCA biplot, 74–76 Chionochloa, 189 Index 409

Chionochloa antarctica, 180, 189 Crete, 154, 159–160, 258 Chionochloa rubra, 189 Cricetidae, 160 Chivay, 66 crocodilians, 244 Chloris barbata, 305 Croft, Darin, 27 Chrysobactron rossi, 189 cross-striations, 291 Chubut Group, 256 crown lagomorphs, 309 Chubut Province, Argentina, 278 crown simplification, 296 Cifelli, Richard L., 25 Ctenomyidae, 19 Cingulata, 13, 323 Ctenomys, 313 circadian incremental lines, 294 culling, 93 circadian structures in dentine, 289–291 Cumberland, Kenneth Brailey, 85, 113 circadian structures in enamel, 291–294 Cumbria, 118 CLAMP3 dataset, 252 Cuniculus, 1 climate intimacy, 238–242 Cuvier, Georges, 2 clover, 86 Cuzco Department, Peru, 66 CMMT. See coldest month mean temperature Cyclone Bola, 112–113 (CMMT) Cynodon, 58 cobalt deficiency, 144 Cyperus, 306 Cochilius, 271 Cyperus ustulatus, 177 Cochilius fumensis, 46 Cohuna, 147 Daouitherium, 52 coldest month mean temperature (CMMT), 73 Darling River, 138 Coley’s Quarry, 50 Darwin, Charles, 2 Colhue-Huapi Member, 244–245, 252, 258, 265. Dasypodidae, 272, 286, 312 See Sarmiento Formation Dasypodoidea, 13 Colhuehuapian. See Colhuehuapian SALMA Dasyproctidae, 13 Colhuehuapian SALMA, 278, 299, 313 De Salle, Robert, 66 Collon-Cura Formation, 19 decadal variation, 108–111 Colloncuran. See Colloncuran SALMA deep time climate variability, 244 Colloncuran SALMA, 23, 313 deer. See Cervidae Colombia, 79, 257, 293 deFinetti diagram, 66 Colorado state, 7, 145 DEM. See Digital Elevation Model (DEM) Colpodon, 271 DeMenocal website, 212 Columbia Plateau, 209 DeMenocal, Peter B., 201 Commonwealth Scientific and Industrial Research Department of Scientific and Industrial Research, 90, (CSIRO), 123 171 Comodoro Rivadavia, 240 Deseadan SALMA, 23, 278, 284, 299, 312 comparable stages of wear and eruption, 172–173 Deseado stage. See Deseadan SALMA comparable wear stages, 173–174 desert, 120 Condobolin, 136 Desmarest, Anselme Gaëtan, 1 Condylarthra, 52 Desmostylia, 52 consequences of elodonty, 299 Desmostyliformes, 52 Contour Plot command. See JMP v3.1 Dickson Experimental Station, Canberra, Australian Cook glacier, 302 Capital Territory, 123, 329, 338 Coorong, 147 Didolodontidae, 51 Coprinisphaera ichnofacies, 265 diet, xiii, 18, 63, 70, 194 Córdoba Province, Argentina, 250, 317 aboriginal, 147 Coriaria arborea, 177 Australopithecus, 193 Coromandel volcanic center, 114 C4 grass, 195 Corsica, 158 dung beetle, 265 cortaderales, 58 feral goat and sheep, 168 Cortaderia argentea, 58 grass, 297 Coryphodontidae, 52 hard objects, 235 Costin, Alec, 131 hypsodonty, 70, 73 Cova de Ca Na Reia, 160 large teeth, 144 Cowra, 136 Maori, 146 Cretaceous, 256 Myotragus, 157 410 Index

diet (cont.) terrigenous sediment, 200 surface processes, 145 volcanism and surface processes, 209 Theropithecus, 196 temporal resolution, 227 Vicugna, 315 terrestrial fossil record diet classification, 59–60, 62–64, 324 Australopithecinae, 197–198 in Argentina, 67 Australopithecus, 197 in Chile, 64–66 Suidae, 195 in Peru, 66 Theropithecus, 195–196 diet gradient, 70 time series analysis, 216 diet quality, 54, 298 Australopithecus, 219 dietary intake, 115 Metridiochoerus, 216 dietary pressure, 306 Nyanzachoerus-Notochoerus, 216 Digital Elevation Model (DEM), 149 Theropithecus, 219 Digitaria pruriens, 177 East African rift system, 192 Dikika, 214 East African volcanic highlands, 198 Dinocerata, 52 Echimyidae, 63 Distichlis, 319 Ecuador, 79, 257 domestic sheep, 324, 326 Eduardo Abaroa, 61 Drake Passage, 237, 241–242, 256 Egmont (Taranaki), 114 driest continent, 120 Eivissa. See Ibiza dry climate processes, 138–141 El Maitán Belt, 256 dry country grasslands, 120 El Niño events, 107 Dryolestida, 13, 323 El Niño Southern Oscillation (ENSO), 101 DSDP Site 231, 193, 198, 229 El Nuevo, 49 DSDP Site 277, 245 elephants. See Proboscidea DSDP Site 511, 245, 276 Elephas, 228 DSDP Site 512, 277 Ellis, Barbara, 67 DSDP Site 513, 277 elodonty, 1, 294–295 DSI. See Dust Storm Index EI Rosado, 50, 265, 276, 282 dung-beetle brood balls, 265 Elymus, 306 Dusen, Per, 5 Embrithopoda, 52 Dust Bowl, 321 Emile Baudot Seamount, 157 Dust Bowl drought, 321 endemic excess tooth wear, 100 dust storm, 82, 120, 133, 138, 148, 194 ENSO, 107, 119, 135, 339. See El Niño Southern conditions, 136, 138, 266, 329 Oscillation source area, 144, 320 ENSO erosion, 111–112 dust storm frequency, 79, 82, 129, 267, 315, 321, 325 ENSO in New South Wales, 135 Dust Storm Index (DSI), 133–134 Entre Rios Province, Argentina, 250 dwarf ngaio, 179 Eoastrapostylops, 51–52 Eocaiman, 248 earlier-erupting teeth that are shed, 120 Eocaiman cavernensis, 248 early interest, 85–89 Eocardiidae, 18 earth surface processes, 91–92 Eocene, 4 East Africa, 332, 340 Eocene–Oligocene Transition (EOT), 28–29, 243 East African (or Somali or Findlater) low-level jet, Eohyrax, 27, 38, 40, 44 205 Eohyrax rusticus, 29, 36, 39 East African Plio-Pleistocene Eolian archipelagos, 158 body size evolution, 226 Eomorphippus, 39, 42 erosion rates, 211 Eomorphippus obscurus, 27, 34, 39, 47–48 evolutionary rates, 213 Eomorphippus pascuali, 39, 46 fluvial-eolian interaction, 231 Eopachyrucos, 27, 34, 39–40 grass and grasslands, 228 Eopachyrucos pliciferus, 34, 41 source to sink sediment cascade, 198 Eopachyrucos pliciformis, 27 lithogenic flux, 204 EOT. See Eocene–Oligocene Transition spatial (geographic) complexity, 202 Eparctocyona, 52 surface winds, 204 Epica Dome C ice core, 267 temporal complexity, 201 Epiklohnia verticalis, 38 Index 411

Equidae, 1, 4, 7, 25, 228, 379, 397 earth surface processes, 92 Equidé. See Equidae ENSO erosion, 112 Erica shrub-dominated vegetation, 210 geographic patterns, 93 erosion of the Sarmiento Formation, 257–258 endemic area, 100 erosion rates, 211–212 regional survey, 101 eruption frequency, 274–276 six farms, 98 especially coarse grasses, 58 Te Awa versus Feilding, 93 espinal, 266 Wallaceville versus the Wairarapa, 97 esteros del Iberá, 248 soil ingestion, 90 Etayoia, 52 temporal patterns, 101 Ethiopia, 192, 231, 257, 332 decadal timescales, 108 Ethiopian plateau, 210 interannual variation, 104 Ethiopian Rift, 193, 228 seasonal variation, 102 Ethiopian Rift System, 198 volcanic ash and erosion, 114 Eumaiochoerus, 158 Wairarapa syndrome, 91 Eumegamyinae, 312 wet climate erosion, 112 Europe, 310 extrinsic (or exogenous or adventitious) abrasives. European arrival, 304 See soil European perennial pasture grass, 88 Eyles, Garth O., 113 European settlement, 302 Europeans, 251 Fabiana densa, 316 Eurystomus stehlini, 48 Fabiana spp., 316 Euston, 148 Falkner, Thomas, 1, 8 ever-growing teeth, 285–288 fan-shaped phytoliths, 264 alveolar bone, 297 faunal hypsodonty, 29, 38–39 cementum, 297 February 2004 rainstorm event, 94 circadian structures in dentine, 289 Feilding, 93 circadian structures in enamel, 294 feral goats and sheep on islands, 164–166 consequences of elodonty, 299 fern, 189 crown simplification, 296 fern-scrubland, 304 engines of erosion?, 321 Feruglio, Egidio, 47 environmental impact in South America, 313–315 Ferugliotherium, 55 fossil record of rabbits, 309 Festuca, 316 measurement of crown height, 288 Festuca rubra, 180 periodontal ligaments, 295 field protocol, 155–320 persistent enamel-forming organ, 295 Fiji, 306 rabbit introductions and eradications, 299 Fischer von Waldheim, Gotthelf, 1 in Australia, 301 flood basalt, 208 in New Zealand, 304 fluvial-eolian interaction, 142, 231–233 on Carnac Ialand, 307 Foggia Province, Italy, 160 on Ile Saint-Paul, 308 folivory, 63 on Kerguelen Islands, 308 foregut-fermenting, 50 on Macquarie Island, 309 forest, 260 on Phillip Island, 306 forest versus grassland, 262–263 on Round Island, 168 formation of ice, 243–244 on Whale Island (Moutohora), 307 Formosa Province, Argentina, 73 rabbit-like notoungulates, 312 Fortelius, Mikael, 54 Vicugna, 315 fraction of absorbed photosynthetically active field protocol, 318 radiation (fAPAR), 261 Laguna Blanca dust sources, 316 Fremantle, 306 Laguna Blanca Reserve, 316 French Southern Territories, 307 mineral particle consumption, 317 Frenguelli, Joaquin, 6 why elodonty?, 298 Freudenberg, Wilhelm, 157 evolutionary rates, 213–214 excess tooth wear, 86, 117 Gaiman, 278 excess tooth wear in New Zealand Galapagos Archipelago, 165 early interest, 86 Galea, 313 412 Index

Gargano, 160–161 Guilielmoscottia, 39 Gaudry, Albert, 2 Guilielmoscottia plicifera, 46 gazelles, 156 guinea pig. See Caviidae GBV-3 El Rosado, 14, 43, 47, 49, 156, 272 Gulf of Aden, 192, 198, 207 GBV-4 La Cancha. See La Cancha Gulf of Alaska, 234 GBV-60 El Nuevo. See El Nuevo Gulf of San Jorge, 3 gelada baboon, 195, 233 gulley erosion, 112 Gele Tuff, 207 Guthrie-Smith, William Herbert, 85, 112 Geoffroy Saint Hilaire, Étienne, 1 Gymnesic Islands, 156 geographic area, 277–278 geographic patterns, 93 Hacienda Pairumani, 66 geometry and history, 242–243 Hadar, 200, 207 Geomyidae, 57 Hadar Formation, 195 geophagia, 144 Haszard Formation, 179 Geoxus, 60 Hattomys, 160 girafﬁd, 158 Hawaii, 165 Girbilidae, 160 Hawke’s Bay, 92 glacial erosion, 78 Hawke’s Bay Flood, 85, 113 Glade, Thomas, 113 Healy, W. Bernard, 90, 190, 341 glass shards, 202 Hebrides Islands, 166 glirid, 330 Hegetotheriidae, 13, 36, 40, 284–285 Gliridae, 157, 160 Hegetotherium, 27 Glyptodontidae, 312 Henricosborniidae, 51 Glyptodontoidea, 13 herbivore clades, 58 glyptodonts (Glyptodontidae), 312 herbivore dung, 265 goat. See Capra herbivore fauna, 53 Gobiolagus, 310 herbivore reproduction, 101 Goin, Francisco J., 39 herbivores, 1, 28, 53, 80, 324 Golfe du Morbihan, 308 dust, 228 Gondwanatheria, 323 East Africa, 192 Goodradigbee River, 302 elodonty, 284, 312 Gramineae, 330 erosion, 314 Gran Barranca, 29, 237, 283, 335 hypsodonty, 268 Gran Barranca Member, 244, 265. See Sarmiento marsupial(s), 120, 153 Formation Mediterranean, 155 Gran Hondonada, 272 mountain, 71 Grant, Peter Raymond and Rosemary, 331 South America, 236 GraphClick v3.0, 135 tooth shape, 300 grass and grasslands, 228–229 tooth wear, 122 grass phytoliths, 263–264 herbivorous diet, 70, 79 grass-dominated ecosystems, 262 herbivory, 43, 63, 115 grasslands, 82, 262 hypsodonty, 70 grazers, 324 phytoliths, 121 grazing, 63 soil ingestion, 92, 118, 192 grazing morphology, 270–273 volcanic ash, 71 Great American Biotic Interchange (GABI), 19, Hershkovitz, Philip, 63 323 Hertwig’s root sheath, 91 Great Australian Bight, 270 Hertwig’s solution, 65 Great Barrier Reef, 302 Heteromyidae, 57 Great Basin, 144 Hickey, F., 93 Great Dividing Range, Australia, 82 high montane dwarf forests, 266 Great Plains, 320–321 high-wear environments, 145 Groeberia, 285 Hillston, 136 Groeberiidae, 286, 323 hindgut-fermenting, 50 Grossetto Province, Italy, 158 Hitz, Ralph, 27 ground sloths, 312 Holocene, 321 guanaco, 57 Homalodotheria, 52 Index 413

Homalostylops, 39 Inter-decadal Paciﬁc Oscillation (IPO), 101, 108 Homalostylops parvus, 271 intrinsic (or endogenous) abrasives. See phytoliths Homo, 193 introductions and eradications, 299–301 Homo erectus, 147 Iran, 202 Homo habilis, 198 island evolution, 154 Homo sapiens, 145, 198 feral goats and sheep, 164 Honda Group, 293 Campbell Island, 180, 189 Hoplitomericidae, 160 Macauley Island, 179, 184 Hoplitomeryx, 160 Raoul Island, 175, 184 Hordeum, 58 Mediterranean islands, 154 Horn of Africa, 192 convergent evolution, 155 horse. See Equidae Crete, 159 horse latitudes, 120, 328 eolian processes, 162 Huajara, 61 Gargano, 160 Huayquerian SALMA, 19, 45 Mallorca, 156 Huerzelerimys oreopitheci, 158 Maremma region, 158 Huila Department, Colombia, 293 Mediterranean volcanism, 161 human tooth size, 144–145 Sardenia, 159 humid pampas, 266 Isotemnidae, 43, 272 Hünicken, Mario Alfredo, 5 Itaborai, 51 Hutt River Valley, 98 Itaboraian SALMA, 45 Huxley, Thomas Henry, 57 Italy, 257 Hydrochoerinae, 312 Hydrochoerus, 285 jackrabbit, 320–321 Hyophorbe, 306 Janis, Christine, 53, 120 Hyopsodontidae, 51–52 JMP v3.1, 77 Hyopsodus, 41 JMP v5.0.1.2, 77, 80 Hyperoxotodon, 24 Johnbell, 40 Hypnomys, 157 Jubaea, 250 Hypolagus, 311 Jubaea chilensis, 250 hypsodont, 2 Juli, 66 hypsodonty Juniper–Podocarpus-dominated forest, 210 dust storm frequency, 268 Hypsodonty Event #1, 274 Kaharoa Tephra, 147 Hypsodonty Event #2, 274 Kaitoke, 97 hypsodonty index (HI), 28–29 Kale Tuff, 207 Hyraces. See Hyracoidea Kanapoi, 213–214 Hyracoidea, 52 kangaroos (Macropodidae), 53–54, 120, 328 hyracoids. See Hyracoidea Kanjera Tuff, 207 Kansas state, 289 Iberian Peninsula, 160 Kapthurin Formation Bedded Tuff complex, 207 Ibiza, 154, 160 Karl von Linne, 1 Ignigena, 40 Karpathos, 159 Ihering, Hermann von, 2 Katmai Peninsula, 338 Ile Guillou, 308 Kaurite, 145 Île Saint-Paul. See Saint Paul Island Kayampanga Tuff, 207 Ile Verte, 308 KBS Tuff, 207 Imperata aundinacea, 177 Kedong–Olorgesailie, 207 Incamys, 13 Kenya, 145, 192, 207, 257 Indian Ocean, 245, 307 Kerguelen archipelago, 308 Indian Ocean dipole, 210 Kerguelen Island, 166 Indo-Australian Plate, 146 Kerguelen Plateau, 243 insect trace fossils, 262 Kermadec Archipelago, 114, 165–166 insectivory, 62 Kibenikhoria, 39, 49 interannual variation, 103–108 Kikuyu, 145 Interatheriidae, 27, 34, 39, 45, 236, 270, 285 Kiwitea, 94 Interatheriinae, 27, 45–46, 298 Koken, Ernst, 4 414 Index

Kokiselei Tuff, 207 Leporinae, 311 Kolhue-Kaike Formation, 256 Leptictis, 52 Konso, 214 Leptocheniinae, 57 Konso basin, 202 Lepus, 321 Koobi Fora, 213–214 Lepus americanus, 321 Koobi Fora Formation, 207 Lepus californicus, 321 Kovalevsky, Vladimir Onufrievich, 57 Lepus europaeus, 314 Kow Swamp. See Cohuna Lepus townsendii, 321 kumara, 146 Letrero Formation, 280 Kunzea, 307 linear sedimentation rates (LSR), 203, 215 lithogenic flux, 200, 203–204, 215 La Cancha, 29 Litopterna, 51–52 La Cancha level, 258 llanos, 266 La Cantera, 29 Llanos de la Rioja, 316–317 La Flecha, 40 Loess Plateau of China, 205, 258 La Niña events, 107 Lokochot Tuff, 207 La Pampa Province, Argentina, 266 Lolium, 58 La Rioja Province, Argentina, 317 Lolium rigidum, 132 La Venta, 280 Lomogol Tuff, 207 La Victoria Formation, 293 long cell phytoliths, 264 Lachlan River, 136 Los Alerces, 61 Lack, David Lambert, 331 Los Arrayanes, 61 Laetoli, 214 Los Glaciares, 61 Lago Puelo, 61 Lothagam, 213 Lagomorpha, 53 Lower Hutt, 90 Lagostomus maximus, 313 Lower Puesto Almendra Member, 244, 251. Laguna Blanca dust sources, 316–317 See Sarmiento Formation Laguna Blanca Reserve, 315–316 lowest and flattest continent, 120 Lake Bungunnia, 149 Loxodonta, 228 Lake Burley Griffin, 124 Ludwig, T.G., 90 Lake Cargelligo, 136 Lumbrera Formation, 313 Lake Colhue-Huapi, 256 Lushilagus, 310 Lake District, United Kingdom, 118 luxurious forest, 176 Lake Eyre Basin, 134, 138, 144, 301, 303 Lake Malawi, 207 Macauley Island, 166, 170–171, 179–180, 184–189, Lake Nicaragua, 145 331 Lake Taupo, 101 MacFadden, Bruce J., 57 Lake Titicaca, 66 Machlydotherium, 13 Lake Turkana, 207 Machupicchu, 66 Lake Tutira, 111, 113, 304, 338 Mackenzie country, 305 land degradation, 299 Macquarie Island, 300, 305, 308 Landcare Research (Lincoln), 169 Macraucheniidae, 52, 55 land-slipping, 94 Macropodidae, 80, 328 Lanin, 61 Macropodidae tooth replacement, 120 larger later-erupting teeth, 120 macrotephra, 202 Las Flores Formation, 256 Madden, Richard H., 26 Last Glacial Maximum (LGM), 149, 194 Madeira Islands, 257 Latania, 306 Magdalena River, 293 later-erupting teeth migrate forward, 120 Mahoe, 177 Laventan SALMA, 313 Main Ethiopian Rift, 200, 202 Laysan Island, 305 Makran coast, 210 Leaf Area Index (LAI), 260 Malbe Tuff, 207 leaf morphology, 252–253 Mallee, 138, 147 Leakey, Meave G., 196 Mallorca, 154, 156–157 Leontinia, 271 Malvinas Current, 240 Leontiniidae, 271 Malvinas Plateau, 241, 248, 276, 338 Leporidae, 54, 57, 160, 309 Manawatu district, North Island, New Zealand, 86 Index 415

Manawatu-Wanganui, North Island, New Zealand, Meridiungulata, 52 99, 338 Mesaxonia, 52 Maori, 146 Meserve, Peter, 64 Mar Chiquita, 317 Mesotheriidae, 13, 36, 40, 284–285 Maralinga, 133 mesowear, 189 Maremma, 154, 158 Messinien Salinity Crisis, 157 Maremmia, 1, 155, 285 Metatheria, 236 Maremmia haupti, 158 Metridiochoerus, 195, 213, 216, 221 Maremmia lorenzi, 158 Metrosideros, 307 marine paleotemperatures, 245–248 Metrosideros kermadecensis. See Pohutukawa marine productivity, 266–270, 276–277 Metrosideros polymorpha. See Pohutukawa Marmota ﬂaviventris, 321 Mexico, valley of, 209 Marsh, Othniel Charles, 42 Microcavia, 313 marsupial. See Marsupialia Microlaena stipoides, 190 Marsupialia, 13, 39, 323 microspherules, 132 mass accumulation rate (MAR), 203 microtephra, 202 Massey Agricultural College, 86 Middle Awash, 200, 214 Masterton, 91, 97 Middle Awash Valley, 207 masticatory muscle mass, 55 middle Cenozoic of Patagonia, 236–238 MAT. See mean annual temperature (MAT) Middle Eocene Climate Optimum, 244–245 matorral, 266 Mikrotia, 160 Matthew, William Diller, 7 Mildura, 136, 147 Maud Rise, 245 mineral composition, 203 Mauriceville, 97 mineral particle consumption, 317–318 Mauritius, 305 Mioclaenidae, 51 Maxschlosseria, 49 Misiones Province, 249 Maxschlosseria consumata, 49 Mississippi River, 8 Mayoan. See Mayoan SALMA Mitchum, Gerald D., 90 Mayoan SALMA, 313 moas, 146 Mazzoni, Mario Martin, 6, 263 Moiti Tuff, 207 McHenry, Henry M., 197 Molina, Juan Ignacio, Fr., 1 mean annual precipitation (MAP), 73, 251 montane shrubland, 266 mean annual temperature (MAT), 73, 250 Monte León Formation, 278 measurement of crown height, 288–289 Monte León marine transgression, 19 Medicago sativa, 132 monte seco, 266 Medieval Climate Anomaly, 321 Montehermosan SALMA, 19 Medistylus dorsatus, 36 Moquegua Department, Peru, 66 Mediterranean, 163, 257, 324, 340 Motukai, 99 Mediterranean climate, 161 Mount Ainslie, 124 Mediterranean eolian proesses, 162–163 Mount Kosiusko, 134 Mediterranean Islands, 154–156, 161 Mount Majura, 124 Mediterranean Sea, 154 mouse, 289 Mediterranean volcanism, 161–162 Moutohora, 307 Megaceroides cretensis, 160 Moyogalpa, plain of, 145 mega-droughts, 321 Mt. Kulal, 205 Megalagus, 310 Mt. Nyiru Range, 205 Megaloceros cazioti, 159 multichambered stomach, 50 Megaloceros sardus, 159 multiple-occurrence regional landslide event Megatherium americanum, 1 (MORLE), 338 MEI. See Multivariate ENSO Index Multivariate ENSO Index (MEI), 107 Melanesian Borderlands, 146 Muridae, 63, 160, 300 Melicytus ramiﬂorus, 177 Murray River, 147–148, 330, 338 Mendoza, Pedro de, 57 Murray–Darling, 131 Menindee Lakes, 147 Murray–Darling basin, 124, 144 Meniscotherium, 52 Murray–Darling system, 302 Merbein, 136 Murrumbidgee basin, 131 Mericoidodontidae, 57 Murrumbidgee River, 124, 138, 302–303, 338 416 Index

Mus, 288 Notochoerus scotti, 227 Museum of New Zealand Te Papa Tongarewa Notohippidae, 3, 5, 25, 27, 34, 46, 236, 271, (Wellington), 169 299 Mustersan. See Mustersan SALMA Notohippus, 299 Mustersan SALMA, 25, 251, 277 Notopithecinae, 45, 298 Myoporum, 179 Notopithecus, 270 Myotragus, 1, 154, 285, 330 Notopithecus adapinus, 46 Myotragus balearicus, 156 Notostylopidae, 38–39, 49, 236, 271 Mytonolagus, 310 Notostylops, 49, 270 Myxoma, 302, 306, 308–309 Notostylops beds. See Casamayoran SALMA Notostylops murinus, 49, 271 Nabon Basin, 280 Notostylops pendens, 49 Nachukui, 213 Notostylops sp., 50 Nachukui Formation, 207 Notoungulata, 13, 25, 236 Ñahuel Huapi, 61 evolving lineages, 41–50 Namidgi National Park, 124 hypsodonty in Toxodontidae, 22–25 Napier region, 100 notoungulate evolution, 19–22 native grass, 88 single-chambered stomach, 50–51 natural grassland, 179 functional and ecological morphology, Navidad Formation, 252 53–54 NCEAS, 80 phylogenetic affinity, 51–53 Neanderthals, 147 notoungulates. See Notoungulata Neotoma lepida, 321 Numidotheriidae, 52 Neotropical loess, 315 NW Indian Ocean monsoon, 201 Nesodon, 23 Nyanzachoerus, 195 Nesogoral, 159 Nyanzachoerus syrticus, 227 Neuquen Province, Argentina, 278 Nyanzachoerus syrticus–Notochoerus scotti, Nevada state, 145 227 New Britain, 146 Nyanzachoerus–Notochoerus, 195, 216–218, 221, New Guinea, 145–146 333 New Hebrides, 146 Nyanzachoerus–Notochoerus scotti lineage, 213, New Mexico state, 8 216 New South Wales, 121, 134, 301–302, 329 New World rats and mice. See Sigmodontinae ocean chlorophyll concentrations, 267 (Muridae) Oceania, 145, 330 New Zealand, 248, 250, 257, 285, 339 Ocepeia, 52 New Zealand alpine glaciers, 303 Ochotonidae, 160, 309 New Zealand alps, 302 Octodontidae, 19 New Zealand Stock Station Agents Association, 88 octodontids. See Octodontidae Ngauruhoe, 114 ODP Site 1090, 228, 245, 267–268 Ngorongoro, 145 ODP Site 1094, 267 Nicaragua, 257 ODP Site 1128, 270 NIH Image (v1.62/3D), 293 ODP Site 689, 268, 276 Ñirihuau Formation, 262 ODP Site 722, 216 NLLJ. See nocturnal low-level jets ODP Site 748, 270, 277 nocturnal low-level jets, 205 ODP Sites 689 and 690, 245 Norfolk Island, 306 ODP Sites 721 and 722, 198 normalized difference vegetation index (NDVI), 261 ODP Sites 721/722, 193 North American Dust Bowl, 320–322 ODP Sites 744 and 738, 243 North Andean Volcanic Zone, 61, 78 Oi-1, 245, 258, 276 North Island of New Zealand, 260, 317, 326 Oldfieldthomasia, 27, 49 North Pacific Decadal Oscillation Index (PDO), Oldfieldthomasia debilitata, 49 109 Oldfieldthomasiidae, 49 North Patagonian High Plateau, 242 Olduvai, 207, 214, 231 Nothofagus, 64, 260, 262 Olduvai Tuff 1, 207 Nothofagus forests, 73 Olduvai Tuff 1B, 207 Notochoerus, 195 Olfers, Ignaz von, 1 Index 417

Oligocene, 4 paramo, 266 Oligoryzomys flavescens, 67 Paranthropus, 193 Olorgesailie Formation, 195 Paranthropus boisei, 197 Oman, 210 Paranthropus robustus, 194 omnivory, 63 Parastrapotherium, 271 Omo Basin, 214 Parkes, John P., 177 Omo Group, 211 Parkin, Don M., 204 Omo River, 210, 232 parna, 130, 138 Omo River Delta, 211 Parque Nacional Vicente Pérez Rosales, 64 Omotepe Island, Nicaragua, 145 Pascual, Rosendo, 5 open-habitat chloridoid grasses, 264 pasto agrio, 58 open-habitat grasses, 262 pasto blando, 58 orbital timescale, 215 pastos altos y pajonales, 58 Oregon state, 145, 257 pastos tiernos, 58 Orellan. See Orellan NALMA Patagonhippus canterensis, 48 Orellan NALMA, 310 Patagonhippus dukei, 46 Oreopithecus–Maremmia fauna, 158 Patagonia, 4, 237, 324 Orkney Islands, 166 Patagonian Hinge, 39 Ortiz-Jaureguizar, Edgardo, 8 Patagoniidae, 13, 286, 323 Oryctolagus cuniculus, 301, 305, 308–309, 314 Payne wear stage, 174 Oryzomyini, 63 PC. See phytolith counts (PCs) Oschiri fauna, 159 Pearson, Oliver Payne, 66 Osorno Province, Chile, 64 peccary, 51 Otago, South Island, New Zealand, 305 Pedregoso Formation, 19 Ovis, 156, 288 peladares, 316 Ovis aires, 164, 173, 331 Pergamino, 67 Ovis musimon, 308 Pericotoxodon platignathus, 293 Owen Ridge, 198 perikymata, 293 Owen, Sir Richard, 2, 57 periodontal ligaments, 295 Periphragnis, 42–43, 272 Pachygazella, 159 Periptychidae, 52 Pacific “Ring of Fire”, 257 periradicular bands, 289 Pacific Decadal Oscillation (PDO), 108, 327 Perissodactyla, 52–53, 160 Pacific Plate, 146 Perito Moreno, 61, 78 Paenungulata, 52 Persian Gulf, 202 pajonales, 58 persistent enamel-forming organ, 295–296 Pakistan, 202 Peru, 66, 257 Palaeolagus, 309 Pezosiren, 52 Palazzesi, Luis, 5 Phalaris, 126, 330 paleo-Omo river, 203 Phalaris aquatica, 124, 144 paleoprecipitation, 251 Phalaris staggers, 144 paleosol oxides, 252 Phenacodonta, 52 paleosols and trace fossil associations, 264–265 Phenacodontidae, 52 Paleostylopidae, 52 Phenacodus, 52 Palmerston North, 86, 93, 103 Phillip Island, 300, 306 palms, 245, 248, 262, 264 Phosphatherium, 52 Palouse, 258 Phylica nitida, 308 Palyeidodon obtusum, 23 Phyllotini, 60, 63, 313 Pampa de las Salinas, 317 phytolith abundance, 7 Pampa Formation, 58 phytolith concentrations, 102, 122, 124, 126, 130, Pampahippus, 27 165, 180, 189, 319, 326 Pampas, 58, 250 phytolith consumption, 318 Pampas of Argentina, 57 phytolith counts (PCs), 126 Pandanus, 306 phytolith hardness, 132 Panicum chloroleucum, 316, 319 phytolith morphology, 264 Pantodonta, 52 phytolith record, 237, 262–263, 335 papionins. See Theropithecus phytolith-based reconstructions, 260 418 Index

phytoliths, xii, 6, 54, 118, 121, 263 volcanic eruption frequency, 274 soil, 67 wind and marine productivity, 267 tooth wear, 124 premature dental senescence, 93 pig. See Suidae prevalence of hypsodonty, 9 Pilcaniyeu belt, 256 globally, 80 Pinturas Formation, 19 dust storm frequency, 82 Pizzimenti, John, 66 zonal distribution, 81 Plagiarthrus clivus, 46 in South America, 59 Pleurostylodon, 43, 270, 272 diet, 70 Plexotemnus, 27, 43 dust storm frequency, 79 Plinian, 161 environmental correlates, 59 Pliny the Younger, 161 in mountain environments, 71 Poa, 58, 179 moisture conditions, 76 Poa litorosa, 180, 189 volcanism, 72 Poaceae, 5, 264, 304 prismatolite, 264 Pohangina, 91, 99 Proadinotherium, 23, 40 Pohangina River, 92 Proadinotherium leptognathum, 23, 36, 271 Pohutukawa, 177 Proadinotherium muensteri, 23, 271 Polar Front, 241, 316 Proargyrohyrax, 34, 41 Poleslide Member, 310 Proboscidea, 52, 160 polyhedral phytoliths, 264 Procaprolagus, 310 Polynesian arrival, 304 Progaleopithecus tournoueri, 46 Polynesians, 251 Prohegetotherium sculptum, 36, 45 Polypogon, 179 Prolagus, 160 Polystichum vestitum, 180 Propachyrucos smithwoodwardi, 36 Potoco Formation, 283 Prorastomus, 52 precocious hypsodonty Prosopis, 73 grasses, 5–6 Prosotherium garzoni, 36 grasses as sediment traps, 7–8 Protarchaeohyrax, 27, 39, 41, 44 in Metatheria, 37–38 Protarchaeohyrax gracilis, 45 mountain-uplift and volcanism, 8–9 Protarchaeohyrax intermedium, 45 phytoliths, 6–7 Protarchaeohyrax minor, 45 tangled history, 2–5 Proterotheriidae, 52, 55 precocious hypsodonty in Patagonia, 236 Protlipternidae, 52 atmospheric paleotemperatures, 248 Protungulata, 52 southern limit of Alligatoridae, 248 Protungulatum, 52 southern limit of palms, 250 Pseudhyrax, 39, 41, 44 climate intimacy, 238 Pseudhyrax eutrachytheroides, 45 Drake Passage Pseudoglyptodon, 13 deep time climate variability, 244 Pseudohyrax, 27 formation of ice, 243 Pseudostylops subquadratus, 47 geometry and history, 242 Puelia, 27, 35, 39–40, 271 erosion of the Sarmiento Formation, Puelia coarctatus, 39 258 Puelia plicata, 39 marine paleotemperatures, 245 Puerto Aysen, 240 paleoprecipitation, 251 Pukekaikoire, 114 Sarmiento Formation Puna, 313 forest versus grassland, 262 Punapithecus, 41 geographic area, 277 Puno Department, Peru, 66 grass phytoliths, 263 Punomys, 63 grazing morphology, 270 pyroclastic volcanism, 70 paleosols and trace fossils, 264 Pyrotheria, 51–52 sedimentation rates, 276 Pyrotherium, 271 shrublands, 265 Pyrotherium beds. See Deseadan SALMA temperature and precipitation, 273 tephric loessites, 258 Queensland, Australia, 136, 302 vegetation and surface processes, 261 Quehua-Achiri, 280 volcanic activity, 255 questions unanswered, 130–132 Index 419

Rabaul, 146 Riverside, 99 rabbit, 336 Rodentia, 236 calicivirus, 302 rodents, 285, See Rodentia eradication, 299 Romero, E.J., 5 fossil record, 309–311 Rosado Member, 252, 258, 265, 270. See Sarmiento hemorrhagic disease, 302 Formation in Australia, 301–304 Roth, Santiago, 3 in New Zealand, 304–305 Rotorua area, 260 introductions, 299 Round Island, 305 on Carnac Island, 306–307 Royal Cabinet in Madrid, 2 on Ile Saint-Paul, 307–308 Ruahine Range, 91, 304 on Kerguelen Islands, 308 Ruamahanga River valley, 99 on Macquarie Island, 308–309 Ruapehu, 114 on Phillip Island, 306 Rudge, Mike R., 171, 187, 190, 341 on Round Island, 305–306 Rumble Islands, 114 on Whale Island, 307 ruminants, 53 rabbit-like notoungulates, 312–313 Rupricaprinae, 154 rabbits, 284, See Leporidae ryegrass, 86 Raetihi, 91 rainstorm-induced land-sliding, 94 saddle “chloridoid” phytoliths, 264 Rajasthan, 202 Sahara, 163, 258 Rangitikei River, 99 Sahel, 163, 258 Ranui, 99 Saint Helena Island, 165 Raoul Island, 169, 175–177, 184, 331 Saint Paul Island, 307 Rapid Assessment Program, 62 Salar de Antofalla, 317 rats. See Muridae Salar de Arizaro, 316–317 Rattus rattus, 308 Salinas Grandes, 316 Red Sea, 202, 257 Salla, 40, 280 red-clay mantle. See parna Salla fauna, 283 Refugio La Picada, 64 Salta Province, Argentina, 61, 250 regolith landslides, 112 San Jorge Basin, 241, 276, 278 Reguero, Marcelo, 7, 27 San Juan Province, Argentina, 317 Reig, Osvaldo Alfredo, 60 San Julián Formation, 278 reindeer, 166 San Luis Province, Argentina, 250, 266 Reithrodon, 314 Sandy Bay Tephra, 179 Reithrodontomys megalotis, 321 Sanson, Gordon Drummon, 120 relative wear rate, 174 Santa Cruz Formation, 19 Renmark, 147 Santa Cruz Province, Argentina, 278 research method, 124 Santa Cruz stage. See Santacrucian SALMA Reunion Island, 308 Santa Fe Province, Argentina, 250 rhinos (Rhinocerotidae), 53 Santa Rosa, 66, 284 Rhopalostylis baueri. See Raoul Island Santacrucian SALMA, 299 Rhopalostylis sapida, 250 Santiagorothia, 27, 34, 41–42 Rhynchippus equinus, 48–49, 271 Sardinia, 154, 158–159, 257 Rhynchippus pumilus, 46, 48 Sardomeryx oschirensis, 159 Rhyphodon, 42, 272 Sarmiento, 240 Rift System, 332 Sarmiento Formation, 29, 238, 244, 250, 255, 258, Rimutaka Range, 189 267, 284, 338 Rio Chico, 51 SAS Institute, 70 Rio Chico del Chubut, 277 Saskatchewan, 310 Rio Chico Group, 256 savanna biome, 262 Rio Deseado, 278 savannas, 262 Rio Loro, 51 Savelli, Carlo, 162 Rio Negro Province, Argentina, 278 Scarabaeinae, 265 Rio Pinturas, 278 Scarritt Pocket, 46, 48, 277 Rio Salado, 57 Scarrittia, 271 Rio Turbio, 5, 262 scattering coefﬁcient, 140 Rio Zeballos Group, 19 Schlosser, Max, 4 420 Index

scientific impact, 122–123 rainfall-induced, 94 Sciuridae, 314 susceptibility, 97–98 Scotamys, 13 soil erosion and tooth wear, 92 Scotia Archipelago, 165 soil erosion scars, 114 Scotland, 166 soil ingestion, 7, 54, 90–91, 98, 117, 119, 147, 168, Scott, William Berryman, 2, 4 318 SE Atlantic Ocean, 237 tooth wear, 92, 102 SE dust path, 147–148 soil inputs, 90 seasonal variation, 102–103 soil intake, 89 seasonally dry forests, 266 soil load, 86, 92, 100, 115, 140, 256, 318–319 SeaWiFS, 267 soil loss, 143, 205, 280, 305–306 sedimentation rate, 215, 274–276 soil mineral abrasives, 192 sedimentology, 251–252 soil mineral particle flux, 115, 140, 234 Seggeurius, 52 soil mineral transport, 79 semiarid steppes, 238 soil moisture, 67, 92, 134, 136, 140, 257, 320 Ses Fontanelles fauna, 160 soil organic matter, 228 Shamal winds, 202 soil parent material, 61, 67, 71, 94, 108, 114, 138, Shamolagus, 310 144, 162, 164, 209, 252, 257, 299, 306 sheep. See Ovis soil radiocesium, 133 Shockey, Bruce, 27 soil surface, 55, 70, 92, 101, 122 short-grass prairie, 58 bare ground, 265, 305, 319 shrub savanna, 266 soil temperature, 229 shrub steppe, 263, 316 soils shrubland, 180, 260, 265–266 organic peat, 180 shrubland-steppe, 266 Somún Curá plateau, 256 Shungura Formation, 195, 207 source-to-sink sediment cascade, 198–200 Sicily, 257 South America exceptional?, 55–58 Sidi Hakoma Tuff, 208 South Andean Volcanic Zone, 79 Sierra de la Huerta, 317 South Atlantic Ocean, 248 Sierra de San Bernardo, 242 South Australia Sand Drift Act, 301 Sierra Pie de Palo, 317 South Dakota state, 310 Sigmodontinae, 19, 28, 59, 63, 73, 75, 273, 314, 323 South Georgia Island, 166 Sigmodontinae (Muridae), 21, 63, 323 South Pacific Ocean, 237, 248, 331, 338 Silbo Tuff, 207 southeast dust path, 124, 330 Silvilagus, 1 Southern Alps, 305 Simpson, George Gaylord, 42 Southern Andean Volcanic Zone, 61, 267 Simpson’s Y Tuff, 6, 29 Southern Andes, 284, 313 Sinai, 258 southern limit of Alligatoridae, 248–250 single-chamber stomach, 50 southern limit of palms, 250 Sinolagomys, 309 Southern Ocean, 166, 237, 243, 245, 338 Sirenia, 52 Southern Oscillation Index (SOI), 135 six farms, 98–100 southern tablelands, 124 sloths, 53, 312 southwest Atlantic Ocean, 238 Smithsonian Volcano Inventory, 66 Southwest Majorca Volcanic Field, 157 smoothing splines, 80, 130, 214–216 Spalletti, Luis, 6 Snowy Mountains, 138, 140 Sparnotheriodontidae, 52 Soay sheep, 166 spatial (geographic) complexity, 202 soil, 55, 70–71, 157, 238 St Kilda archipelago, 166 bare ground. See peladares stable carbon isotopes, 254 oceanic islands, 164 Stanway, 91 organic peat, 166, 189, 308 station data, 62 volcanic ash. See andisol Statview, 70 soil accession, 131, 134, 138, 260, 264, 320 stereotyped grazing morphology, 270 soil carbonate, 124, 229, 264 Stertomys, 160 soil disturbance, 147, 231 Stipa, 58, 316 soil erodibility, 205 Stipa ichu, 66 soil erosion, 85, 87, 93, 101, 162, 192, 222, 301 Stirton, Reuben Arthur, 7, 42 Index 421

stocking rate, 89, 117 terrigenous dust ﬂux, 201 stratocladistics, 42 terrigenous sediments, 200–201 Strenulagus, 310 Teruggi, Mario, 6 striae of Retzius, 291 Tethytheria, 52 Strömberg, Caroline A.E., 7 Tetraconodontinae, 195 Stromboli, 161 Theropithecus, 195–196, 219, 233 Stromer von Reichenbach, Ernst Freiherr, Theropithecus brumpti, 195, 213, 219 51 Theropithecus gelada, 196 study site, 123–124 Theropithecus oswaldi, 195, 213, 218, 221, 225, Stylinodontidae, 55 233 sub-Andean megafans, 315 Theropithecus oswaldi darti, 218 Sub-Saharan Africa, 144 Theropithecus oswaldi leakeyi, 195, 213 Sudamerica, 55 Theropithecus oswaldi lineage, 195 Sudamericidae, 13 Theropithecus oswaldi oswaldi, 195, 213 Sudan, 205 Thomashuxleya, 42–43, 270, 272 Suidae, 195, 226, 330, 333 Thomasomyini, 63 suids. See Suidae threshold of erosion intensity, 219 Suina, 51 Thurley, D.C., 91 Suinae, 195 Thurley, T.G., 97 surface winds, 204–208 Tibet, 258 Surinam, 63 tierra cocida, 58 survey by New Zealand Stock and Station Agents Tierra del Fuego, 314 Association, 100–101 Tillodontia, 52, 55 Sus sondaari, 159 time series analysis, 215–216 suspended sediment yield (SSY), 107, 115 time series data, 216 Suteijun Tuff, 208 Tinguiririca, 34, 45 SW Asian monsoon, 201 Tinguirirican SALMA, 277 Swanport, 147–148 Tiupampa, 51 Swift Current Creek fauna, 310 Toba eruption, 207 Sydney, 306 Tola shrub, 66 Sylvilagus, 314, 321 Tongariro, 114 Tongariro National Park, 189 Tacna Department, Peru, 66 tooth wear, 91, 124–126 Taeniodonta, 55 dust storm frequency, 268 Taihape, 86, 91, 100 tooth wear gradient, 148–150 Tangimoana, 99 Torata, 66 Tanzania, 145, 207, 231, 257 Tournouër, Andrés, 3 Tarata, 66 Toxodon, 2 Tarawera, 114 Toxodontia, 51–52 Tardigrada, 13, 323 Toxodontidae, 23, 26, 36, 40, 236, 271, 285, 291, Tasman glacier, 302 296 Tasman Sea, 134, 149, 268, 338 Toxodontinae, 298 Tasmanian Gateway, 242 Trachytherus, 36, 40, 45 Taupo eruption, 304 Transpithecus obtentus, 46 Taupo volcanic center, 114 Trauth, Martin H., 200 Tauweru River, 97 tree sloths, 312 Te Awa, 86 Trelew Formation, 19 Te Awa Experimental Station, 118 Tremembé, 284 Te Awa vs Feilding, 93–96 trichome (aculeolita) phytoliths, 264 temperature and precipitation, 273–274 Trifolium subterraneum, 124 temporal complexity, 201–202 Trigonostylopidae, 50 temporal fossa, 54 Trigonostylops, 270 temporal patterns, 101–102 Trithrinax, 250 temporal resolution, 227–228 Trogosinae, 55 temporalis muscle, 54 trophic pyramid, 62 tephric loess, 96, 107, 114 Tsamnichoria, 49 tephric loessites, 258–260 Tsamnichoria cabrerai, 49 422 Index

Tubulidentata, 52 Volcán Osorno, 64 Tucuman Province, Argentina, 250 Volcán Puyehue-Cordón Caulle, 255 Tukituki River, 100 Volcán Ubinas, 66 Turkana, 145 volcanic activity, 255–257 Turkana Basin, 193, 198, 202, 210, 228, 231, 332, volcanic ash, 114 338 volcanic ash and erosion, 114 Turkana Channel jet, 205 volcanic ash shard count, 215, 223 Turkana low-level jet, 232, 332 volcanic ash shards, 202 Turkana nocturnal low-level jet, 232, 332 volcanic ash soil(s), 71, 94, 114, 153, 209 Turkish Angora goats, 173 volcanic Cascade Range, 145 Tuscan archipelago, 158 volcanic East African Rift System, 145 Tuscan Magmatic Province, 158 volcanic eruptions, 78 Tuscany, 155 Volcanic Explosivity Index (VEI), 145 Typha angustifolia, 177 volcanism and surface processes, Typotheria, 5, 51, 55, 286 208–211 Tyrrhenian Sea, 158 Vombatidae, 80 Tyrrhenotragus, 160 Vostok ice core, 267 Vulcano, 161 Uetatus, 13 Vulture volcano, 161 UG90–1 Tuff, 207 Uganda, 207 Waddell Sea, 243 Uintamorpha, 52 Wagga Wagga, 134 Uintan. See Uintan NALMA Waipaoa River, 304 Uintan NALMA, 310 Waipawa basin, 100 Uintatheriidae, 52 Waipawa River, 304 K’ U 37 SST, 248 Waipukurau, 98 Ultrapithecus, 49 Wairarapa, 338 Ultrapithecus rutilans, 49 Wairarapa fault, 94 Ungulata, 52 Wairarapa region, North Island, New Zealand, unilateral hypsodonty, 46 90–91 University of Melbourne, 132 Wairarapa Syndrome, 90–91 University of Padova, 47 Wallaceville Animal Research Center, 97 Upper Hutt, 97 Wallaceville versus the Wairarapa, 98 Upper Puesto Almendra Member, 258 Wargolo Tuff, 207 Uquian SALMA, 57 warmest month mean temperature, 248 Uruguay, 250 Washington state, 145, 257 Utah state, 145 Waterhouse, George Robert, 1 wear stage, 173–175 Vacan SALMA, 277 Wellington, 92 Van Roosmalen, M.G.M., 63 Wellington fault, 94 Vanhof cooling event, 245 Wellington, J., 90 vega, 316 West African savanna, 205 vegetation and surface processes, 260–262 West Turkana, 214 vegetation change, 299 West Wind Drift, 242, 338 VEI. See Volcanic Explosivity Index (VEI) western Andean margin, 325 Vera Member, 244–245, 252, 258, 265, 270 Western Rift of Kenya, 207 Vermilingua, 1, 323 wet climate erosion, 112–113 Vesuvius, 161 wet climate processes, 141 Victoria, 136 wet deposition, 141 Vicugna, 1, 19, 154, 285, 315–316, 337 Whale Island, 114, 307 Vietnam, 260 Whanganui, 338 Virrenato del Rio de La Plata, 1 White Island, 114 Volcán Calbuco, 64 White River beds, 7 Volcán Chaitén, 255 White River Group, 310 Volcán Concepción, 145 Whitneyan. See Whitneyan NALMA Volcán El Misti, 66 Whitneyan NALMA, 310 Volcán Hudson, 255 Williams, Coley S., 47 Index 423

WMMT. See warmest month mean temperature Xotodontinae, 13, 24 (WMMT) wombat (Vombatidae), 120, 285 Yass River, 302 woodland, 260 woody dicots, 262 Zajicek, Gershorn, 294 Wrangell–St Elias, 209 Zajicek’s proliferon, 294 Wyoming state, 8, 145 Zalambdalestes, 52 Zhelestidae, 52 Xenarthra, 13, 296 Zittel, Karl Alfred von, 2, 51 xenarthrans. See Xenarthra Zucol, Alejandro, 6 Xenungulata, 52 xerophilous steppe, 316 δ13C in pedogenic carbonate, 228