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In the Light of Evolution


Volume II: Biodiversity and Extinction



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JOHN C. AVISE, STEPHEN P. HUBBELL, and FRANCISCO J. AYALA, Editors THE NATIONAL ACADEMIES PRESS Washington, D.C. www.nap.edu

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THE NATIONAL ACADEMIES PRESS 500 Fifth Street., N.W. Washington, DC 20001 This volume is based on the Arthur M. Sackler Colloquium of the National Academy of Sciences, “In the Light of Evolution II: Biodiversity and Extinction,” held December 7-8, 2007, at the Arnold and Mabel Beckman Center of the National Academies of Sciences and Engineering in Irvine, California. The articles appearing in these pages were contributed by speakers at the colloquium and have been anonymously reviewed. Any opinions, findings, conclusions, or recommendations expressed in this volume are those of the authors and do not necessarily reflect the view of the National Academy of Sciences. In the light of evolution / John C. Avise and Francisco J. Ayala, editors. p. cm. Vol. I based on a colloquium of the National Academy of Sciences, held December 1–2, 2006, in Irvine, California. Includes bibliographical references. ISBN-13: 978-0-309-10405-0 (hardcover) ISBN-10: 0-309-10405-X (hardcover) ISBN-13: 978-0-309-66786-9 (pdf) ISBN-10: 0-309-66786-0 (pdf) 1. Evolution (Biology)—Congresses. I. Avise, John C, 1948-. II. Ayala, Francisco José, 1934- III. National Academy of Sciences (U.S.) QH359.I55 2007 576.8--dc22 2007032455 Additional copies of this book are available from the National Academies Press, 500 Fifth St., N.W., Lockbox 285, Washington, DC 10055; (800) 624-6242 or (202) 334-3313 (in the Washington metropolitan area); Internet, http://www.nap.edu. Cover image: Stylized turtle, street art from Quito, Ecuador (artist unknown). Driven by human agriculture and industry, the Earth is currently undergoing the sixth mass extinction episode in its history. This image symbolizes both human industry and the countless unknown species that are disappearing before they can be catalogued and studied. Image courtesy of John C. Avise. Copyright 2008 by the National Academy of Sciences. All rights reserved. Printed in the United States of America

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The National Academy of Sciences is a private, nonprofit, self-perpetuating society of distinguished scholars engaged in scientific and engineering research, dedicated to the furtherance of science and technology and to their use for the general welfare. Upon the authority of the charter granted to it by the Congress in 1863, the Academy has a mandate that requires it to advise the federal govern- ment on scientific and technical matters. Dr. Ralph J. Cicerone is president of the National Academy of Sciences. The National Academy of Engineering was established in 1964, under the charter of the National Academy of Sciences, as a parallel organization of outstanding engineers. It is autonomous in its administration and in the selection of its mem- bers, sharing with the National Academy of Sciences the responsibility for advis- ing the federal government. The National Academy of Engineering also sponsors engineering programs aimed at meeting national needs, encourages education and research, and recognizes the superior achievements of engineers. Dr. Charles M. Vest is president of the National Academy of Engineering. The Institute of Medicine was established in 1970 by the National Academy of Sciences to secure the services of eminent members of appropriate professions in the examination of policy matters pertaining to the health of the public. The Insti- tute acts under the responsibility given to the National Academy of Sciences by its congressional charter to be an adviser to the federal government and, upon its own initiative, to identify issues of medical care, research, and education. Dr. Harvey V. Fineberg is president of the Institute of Medicine. The National Research Council was organized by the National Academy of Sciences in 1916 to associate the broad community of science and technology with the Academy’s purposes of furthering knowledge and advising the federal government. Functioning in accordance with general policies determined by the Academy, the Council has become the principal operating agency of both the National Academy of Sciences and the National Academy of Engineering in pro- viding services to the government, the public, and the scientific and engineering communities. The Council is administered jointly by both Academies and the Institute of Medicine. Dr. Ralph J. Cicerone and Dr. Charles M. Vest are chair and vice chair, respectively, of the National Research Council. www.national-academies.org

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Arthur M. Sackler, M.D. 1913-1987 Born in Brooklyn, New York, Arthur M. Sackler was educated in the arts, sciences, and humanities at New York University. These interests remained the focus of his life, as he became widely known as a scientist, art collector, and philanthropist, endowing institutions of learning and culture throughout the world. He felt that his fundamental role was as a doctor, a vocation he decided upon at the age of four. After completing his internship and service as house physician at Lincoln Hospital in New York City, he became a resident in psychiatry at Creedmoor State Hospital. There, in the 1940s, he started research that resulted in more than 150 papers in neuroendocri- nology, psychiatry, and experimental medicine. He considered his scien- tific research in the metabolic basis of schizophrenia his most significant contribution to science and served as editor of the Journal of Clinical and Experimental Psychobiology from 1950 to 1962. In 1960 he started publica- tion of Medical Tribune, a weekly medical newspaper that reached over one million readers in 20 countries. He established the Laboratories for Therapeutic Research in 1938, a facility in New York for basic research that he directed until 1983. As a generous benefactor to the causes of medicine and basic science, Arthur Sackler built and contributed to a wide range of scientific insti- tutions: the Sackler School of Medicine established in 1972 at Tel Aviv University, Tel Aviv, Israel; the Sackler Institute of Graduate Biomedical Science at New York University, founded in 1980; the Arthur M. Sackler Science Center dedicated in 1985 at Clark University, Worcester, Massachu- setts; and the Sackler School of Graduate Biomedical Sciences, established in 1980, and the Arthur M. Sackler Center for Health Communications, established in 1986, both at Tufts University, Boston, Massachusetts. His pre-eminence in the art world is already legendary. According to his wife Jillian, one of his favorite relaxations was to visit museums and art galleries and pick out great pieces others had overlooked. His interest in art is reflected in his philanthropy; he endowed galleries at the Metro- politan Museum of Art and Princeton University, a museum at Harvard vii

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University, and the Arthur M. Sackler Gallery of Asian Art in Washing- ton, D.C. True to his oft-stated determination to create bridges between peoples, he offered to build a teaching museum in China, which Jillian made possible after his death, and in 1993 opened the Arthur M. Sackler Museum of Art and Archaeology at Peking University in Beijing. In a world that often sees science and art as two separate cultures, Arthur Sackler saw them as inextricably related. In a speech given at the State University of New York at Stony Brook, Some reflections on the arts, sciences and humanities, a year before his death, he observed: ‘‘Commu- nication is, for me, the primum movens of all culture. In the arts . . . I find the emotional component most moving. In science, it is the intellectual content. Both are deeply interlinked in the humanities.’’ The Arthur M. Sackler Colloquia at the National Academy of Sciences pay tribute to this faith in communication as the prime mover of knowledge and culture. viii

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Contents Arthur M. Sackler Biography vii Preface to the In the Light of Evolution Series xiii Preface to In the Light of Evoluion Volume II: xv Biodiversity and Extinction PART I CONTEMPORARY PATTERNS AND PROCESSES IN ANIMALS 1 1 Ecological Extinction and Evolution in the Brave New Ocean 5 Jeremy B. C. Jackson 2 Are We in the Midst of the Sixth Mass Extinction? A View from the World of Amphibians 27 David B. Wake and Vance T. Vredenburg 3 Patterns of Biodiversity and Endemism on Indo-West Pacific Coral Reefs 45 Marjorie L. Reaka, Paula J. Rodgers, and Alexei U. Kudla 4 Homage to Linnaeus: How Many Parasites? How Many Hosts? 63 Andy Dobson, Kevin D. Lafferty, Armand M. Kuris, Ryan F. Hechinger, and Walter Jetz ix

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x / Contents PART II CONTEMPORARY PATTERNS AND PROCESSES IN 83 PLANTS AND MICROBES 5 Species Invasions and Extinction: The Future of Native Biodiversity on Islands 85 Dov F. Sax and Steven D. Gaines 6 How Many Tree Species Are There in the Amazon and How Many of Them Will Go Extinct? 107 Stephen P. Hubbell, Fangliang He, Richard Condit, Luis Borda-De-Água, James Kellner, and Hans ter Steege 7 Microbes on Mountainsides: Contrasting Elevational Patterns of Bacterial and Plant Diversity 127 Jessica A. Bryant, Christine Lamanna, Hélène Morlon, Andrew J. Kerkhoff, Brian J. Enquist, and Jessica L. Green 8 Resistance, Resilience, and Redundancy in Microbial Communities 149 Steven D. Allison and Jennifer B. H. Martiny PART III TRENDS AND PROCESSES IN THE PALEONTOLOGICAL PAST 165 9 Extinction as the Loss of Evolutionary History 171 Douglas H. Erwin 10 Extinction and the Spatial Dynamics of Biodiversity 189 David Jablonski 11 Dynamics of Origination and Extinction in the Marine Fossil Record 207 John Alroy 12 Megafauna Biomass Tradeoff as a Driver of Quaternary and Future Extinctions 227 Anthony D. Barnosky

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Contents / xi PART IV PROSPECTS FOR THE FUTURE 243 13 A Phylogenetic Perspective on the Distribution of Plant Diversity 247 Michael J. Donoghue 14 Phylogenetic Trees and the Future of Mammalian Biodiversity 263 T. Jonathan Davies, Susanne A. Fritz, Richard Grenyer, C. David L. Orme, Jon Bielby, Olaf R. P. Bininda-Emonds, Marcel Cardillo, Kate E. Jones, John L. Gittleman, Georgina M. Mace, and Andy Purvis 15 Three Ambitious (and Rather Unorthodox) Assignments for the Field of Biodiversity Genetics 281 John C. Avise 16 Engaging the Public in Biodiversity Issues 297 Michael J. Novacek 17 Further Engaging the Public on Biodiversity Issues 317 Peter J. Bryant 18 Where Does Biodiversity Go From Here? A Grim Business-as-Usual Forecast and a Hopeful Portfolio of Partial Solutions 329 Paul R. Ehrlich and Robert M. Pringle References 347 Index 395

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Preface to the In the Light of Evolution Series B iodiversity—the genetic variety of life—is an exuberant product of the evolutionary past, a vast human-supportive resource (aesthetic, intellectual, and material) of the present, and a rich legacy to cherish and preserve for the future. Two urgent challenges, and opportunities, for 21st-century science are to gain deeper insights into the evolutionary processes that foster biotic diversity, and to translate that understanding into workable solutions for the regional and global crises that biodiversity currently faces. A grasp of evolutionary principles and processes is impor- tant in other societal arenas as well, such as education, medicine, sociol- ogy, and other applied fields including agriculture, pharmacology, and biotechnology. The ramifications of evolutionary thought also extend into learned realms traditionally reserved for philosophy and religion. In 1973, Theodosius Dobzhansky penned a short commentary entitled “Nothing in biology makes sense except in the light of evolution.” Most scientists agree that evolution provides the unifying framework for inter- preting biological phenomena that otherwise can often seem unrelated and perhaps unintelligible. Given the central position of evolutionary thought in biology, it is sadly ironic that evolutionary perspectives outside the sciences have often been neglected, misunderstood, or purposefully misrepresented. The central goal of the In the Light of Evolution (ILE) series is to pro- mote the evolutionary sciences through state-of-the-art colloquia—in the series of Arthur M. Sackler colloquia sponsored by the National Academy of Sciences—and their published proceedings. Each installment explores xiii

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xiv / Preface to the In the Light of Evolution Series evolutionary perspectives on a particular biological topic that is scientifi- cally intriguing but also has special relevance to contemporary societal issues or challenges. Individually and collectively, the ILE series aims to interpret phenomena in various areas of biology through the lens of evolution, address some of the most intellectually engaging as well as pragmatically important societal issues of our times, and foster a greater appreciation of evolutionary biology as a consolidating foundation for the life sciences. The organizers and founding editors of this effort (Avise and Ayala) are the academic grandson and son, respectively, of Theodosius Dobzhansky, to whose fond memory this ILE series is dedicated. May Dobzhansky’s words and insights continue to inspire rational scientific inquiry into nature’s marvelous operations. John C. Avise and Francisco J. Ayala Department of Ecology and Evolutionary Biology, University of California, Irvine (January 2007)

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Preface to In the Light of Evolution, Volume II: Biodiversity and Extinction T he Earth’s biodiversity is a wellspring for scientific curiosity about nature’s workings. It is also a source of joy and inspiration for inquisitive minds, from poets to philosophers, and provides life- support services. According to Kellert (2005), biodiversity affords human- ity nine principal types of benefit: utilitarian (direct economic value of nature’s goods and services), scientific (biological insights), aesthetic (inspiration from nature’s beauty), humanistic (feelings deeply rooted in our inherent attachment to other species), dominionistic (physical and mental well-being promoted by some kinds of interactions with nature), moralistic (including spiritual uplifting), naturalistic (curiosity-driven sat- isfaction from the living world), symbolic (nature-stimulated imagination, communication, and thought), and even negativistic (fears and anxieties about nature, which can actually enrich people’s life experience). Whether or not this list properly characterizes nature’s benefits, the fact is that a world diminished in biodiversity would be greatly impoverished. Many scientists have argued that as a consequence of human activities the Earth has entered the sixth mass extinction episode (and the only such event precipitated by a biotic agent) in its 4-billion-year history (Leakey and Lewin, 1995; Glavin, 2007). The last catastrophic extinction, which occurred about 65 million years ago and was the coup-de-grace for nonavian dinosaurs, marine ammonites, and many other evolutionary lineages, happened rather suddenly after a large asteroid slammed into the planet. Today, most of the biotic holocaust is due—directly or indirectly—to local, regional, and global environmental impacts from a burgeoning xv

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xvi / Preface to In the Light of Evolution, Volume II human population. The first phase of the current extinction episode started about 50,000 to 100,000 years ago when modern humans began dispers- ing around the planet. The second phase started 10,000 years ago with further population increases and land-use changes associated with the invention of agriculture. A third phase of environmental alteration and biodiversity loss was ushered in by the Industrial Revolution. E. O. Wilson (1992) estimated that the Earth is currently losing approximately 0.25% of its remaining species per year (such that at least 12,000 species may be going extinct annually). Such estimates are educated guesses because they represent extrapolations (from species–area curves and other evidence) to taxa that undoubtedly are disappearing even before they can be identified and studied. Nevertheless, they do reveal the general magnitude of the ongoing extinction crisis. For many species that manage to avoid extirpa- tion, local and regional populations are being decimated. The modern extinction crisis is prompting scientific efforts on many fronts. Systematists are striving to describe biodiversity and reconstruct the Tree of Life. Ecologists are mapping the distributions of biodiversity and global hotspots that merit special conservation attention. Paleontolo- gists are placing the current crisis in temporal context with regard to the Earth’s long geological history, and also to the recent history of human impacts on biodiversity across timescales ranging from decades to millen- nia. Educators and concerned scientists are striving to alert government leaders, policymakers, and the public to the biodiversity crisis. Conser- vation efforts (including those by many nongovernment organizations) are underway to slow the pace of biological extinctions. However, unless conservation achievements accelerate quickly, the outlook for biodiversity in and beyond the 21st century remains grim. This book is the outgrowth of the Arthur M. Sackler Colloquium on “Biodiversity and Extinction,” which was sponsored by the National Academy of Sciences on December 7–8, 2007, at the Academy’s Arnold and Mabel Beckman Center in Irvine, California. It is the second in a series of colloquia under the umbrella title “In the Light of Evolution.” The first book in this series was titled In the Light of Evolution, Volume I: Adaptation and Complex Design (Avise and Ayala, 2007). The chapters that follow illustrate current scientific perspectives on biodiversity and extinction across varied timescales and diverse taxo- nomic groups. Chapters are arranged in four parts, each immediately preceded by a brief editorial introduction. Authors in Part I address con- temporary patterns of biodiversity and extinction in animals representing several imperiled taxa and environmental settings, and authors in Part II do likewise for various modern plants and microbes. In Part III, authors add historical perspective by addressing biodiversity trends and extinc- tion processes in the near and distant paleontological past. Authors in Part

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Preface to In the Light of Evolution, Volume II / xvii IV offer their projections for the future of biodiversity given the pace of environmental alteration by human activities. Collectively, the chapters in this book synthesize recent scientific information and ideas about the abundance and threats to biodiversity in the past, present, and projected future. The current extinction crisis is of human making, and any favorable resolution of that biodiversity crisis—among the most dire in the 4-billion- year history of the Earth—will have to be initiated by mankind. Little time remains for the public, corporations, and governments to awaken to the magnitude of what is at stake. Preserving biodiversity is undeni- ably in humanity’s enlightened self-interest, but the tragic irony is that a majority of humanity is not yet enlightened to this fact. It is hoped that the information and sentiments in this book will assist that critical edu- cational mission.

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