American and Australasian Marsupials: An Evolutionary, Biogeographical, and Ecological Approach 3031084187, 9783031084188

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Nilton C. Cáceres Christopher R. Dickman Editors

American and Australasian Marsupials An Evolutionary, Biogeographical, and Ecological Approach

American and Australasian Marsupials

Nilton C. Ca´ceres • Christopher R. Dickman Editors

American and Australasian Marsupials An Evolutionary, Biogeographical, and Ecological Approach

With 266 Figures and 68 Tables

Editors Nilton C. Cáceres Department of Ecology and Evolution Universidade Federal de Santa Maria Santa Maria, Brazil

Christopher R. Dickman School of Life and Environmental Sciences The University of Sydney Camperdown, NSW, Australia

ISBN 978-3-031-08418-8 ISBN 978-3-031-08419-5 (eBook) https://doi.org/10.1007/978-3-031-08419-5 © Springer Nature Switzerland AG 2023 This work is subject to copyright. All rights are solely and exclusively licensed by the Publisher, whether the whole or part of the material is concerned, specifically the rights of translation, reprinting, reuse of illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way, and transmission or information storage and retrieval, electronic adaptation, computer software, or by similar or dissimilar methodology now known or hereafter developed. The use of general descriptive names, registered names, trademarks, service marks, etc. in this publication does not imply, even in the absence of a specific statement, that such names are exempt from the relevant protective laws and regulations and therefore free for general use. The publisher, the authors, and the editors are safe to assume that the advice and information in this book are believed to be true and accurate at the date of publication. Neither the publisher nor the authors or the editors give a warranty, expressed or implied, with respect to the material contained herein or for any errors or omissions that may have been made. The publisher remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. This Springer imprint is published by the registered company Springer Nature Switzerland AG. The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland

This book is dedicated to the modern-day pioneers of marsupial biology, Michael Archer, Rui Cerqueira, Alfred Gardner, Francisco Goin, John Kirsch, Marilyn Renfree, and Hugh Tyndale-Biscoe, whose inspirational guidance for students and original studies on this mammalian clade provide the foundation for much of the knowledge that is summarized in this major reference work.

Foreword

The Class Mammalia includes two subclasses that diverged back in the Triassic: Prototheria and Theria. The egg-laying platypus and echidnas (Order Monotremata) belong to the former group, while the latter group contains both Metatheria (marsupials) and Eutheria (placental mammals). Marsupials and placentals differ dramatically in extant diversity: there are 7 orders and 407 species of extant marsupials chiefly found in Australia and the American tropics, whereas the 19 orders and 6184 species of placentals are found on every continent and in every ocean. Because placentals comprise virtually all our pets, livestock, laboratory animals, and those humans hunt or trap, they are more familiar and we know far more about them. Australasia’s four orders of marsupials include 268 species and these represent fully 45% of Australia’s indigenous mammals. Encompassing forms that burrow, run, hop, climb, and glide, Australasian marsupials today range in size from the 4 g Planigale to the 85 kg Macropus and Osphranter, but this is a truncated range of their full evolutionary flowering. Diprotodon, a giant herbivore weighing up to 2 tons, and many other large marsupials went extinct shortly after humans colonized Australia in the Late Pleistocene. Only those lineages that managed to reach Australia could diversify there, as it was isolated for most of the Cenozoic from other faunas and floras. Evolving in the absence of placental mammal competitors for most of the last 65 million years, Australian marsupials came to occupy many vacant niches and attain a remarkable ecological breadth and morphological disparity. The conspicuous success and prominence of marsupials in Australasia long overshadowed another equally remarkable radiation. Like Australia, South America was an island continent for most of the Cenozoic, an era when its faunas and floras experienced their “Splendid Isolation” from the rest of the world. However, South America’s isolation was not total but rather episodic, permitting late Cretaceous and late Neogene biotic exchanges with North America, Paleogene exchanges with Africa, and mid-Cenozoic exchanges with Australia (via Antarctica). Like Australia, South America was home to both monotremes and marsupials, but these groups shared South American landscapes with one of the oldest groups of placental mammals (represented today by sloths, anteaters, and armadillos), as well as with a host of archaic ungulates. This assemblage of mammals was joined in the Paleogene by caviomorph rodents (guinea-pigs and their relatives) and platyrrhine primates, vii

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Foreword

each group clearly derived from Afrotropical relatives (i.e., phiomorph rodents and catarrhine primates). Finally, in the Neogene, the converging North and South American plates triggered a geomorphic revolution that culminated in the emergence of the Panamanian Isthmus – a landbridge between the two continents enabling freer dispersal and colonization between them. The resultant “Great American Biotic Interchange” brought South America all of its carnivorans, deer, peccaries, camels, tapirs, horses, proboscideans, shrews, rabbits, squirrels, and mice. As readers of this volume will appreciate, marsupial radiations in Australasia and the Americas differ in several important respects. Marsupials originated in South America and their early radiation unfolded over a continent more than twice as large; South America is centered on the Equator and has immense tropical rainforests and wetlands, the most productive terrestrial environments on Earth. However, its three living orders of marsupials evolved amidst the world’s richest biotic realm – the Neotropics – with 1500 other mammal species preempting ecological space. In contrast, the four orders of Australasian marsupials descended from an American colonist arriving via Antarctica in the Paleogene. Without other therian mammals, this lineage had far greater ecological opportunity and attained far greater morphological and ecological diversity. In this volume, editors Nilton Cáceres and Chris Dickman have assembled a multidisciplinary team of contributors to explore and document the extraordinary evolutionary and ecological radiations of American and Australasian marsupials. Each author is expert in one of more of the themes used to organize this volume: systematics, biogeography, ecology, and conservation. The authors each have vigorous, ongoing research programs and concisely summarize their complementary sketches for the volume. Together, they offer a far-reaching synthesis of current understanding of the marsupial radiations, one certain to impress and amaze us. Field Museum of Natural History Chicago, IL

Bruce D. Patterson

Preface

The book has 50 chapters divided into three general sections, each containing several chapters that address different aspects of the biology of American and Australasian marsupials. The first section, “Evolution and Diversification,” contains chapters that review the origins and radiation of marsupials from the earliest times in the Mesozoic through to their flowering in the Cenozoic in the Americas and Australasia. This section also provides up-to-date lists of all the living species that have been described with notes on their taxonomy and systematics. In the second section, “Biogeography,” there are chapters that describe large-scale patterns in the physical traits of marsupials, patterns in their species richness and diversity, as well as regional patterns in marsupial diversity and endemism in the Americas and Australasia. The third section, “Ecology and Conservation,” contains chapters that present overviews of marsupial population dynamics, reproduction, use of space and habitat, diet, and patterns of activity. This section also describes key aspects of marsupial physiology, before concluding with several chapters that describe the conservation status of the world’s marsupials, the factors that affect their status, and the strategies that are being used to ensure that marsupials will persist in the future. A brief sketch of each chapter is presented in the following. The section on “Evolution and Diversification” opens the book with our introductory chapter (Chap. ▶ 1) dealing with the development of research on American and Australasian marsupials, highlighting both the major contributors and the contributions they have made, to our current knowledge. After the opening chapter, Robin Beck takes a deep-time perspective to provide a profound and detailed discussion of the diversity and phylogenetic position of the main extant and fossil metatherian clades (Chap. ▶ 2). The next chapter, led by Pablo Teta, provides a detailed overview of research on the development of taxonomy and systematics of the American marsupials (Chap. ▶ 3). The following two chapters (Chaps. ▶ 4 and ▶ 5) present, with detailed notes, revised checklists of living marsupial faunas in the Americas and Australasia, resulting in more than 400 recognized extant marsupial species in the world. These chapters are written by teams of experts in marsupial taxonomy in both western and eastern hemispheres, led by Diego Astúa and Andrew Baker, respectively. The next two chapters (Chaps. ▶ 6 and ▶ 7) begin to address the diversity and history of extinct species of marsupials and non-marsupial metatherians, focusing on the Cenozoic of South ix

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America in an overall overview but also on the Paleogene metatherians of the Itaboraí basin, which harbors a peculiar and ancient fauna. These chapters are led by Francisco Goin and Leonardo Carneiro. In Chap. ▶ 8, led by Sally Potter, a detailed discussion is presented of the molecular evolution of Australasian marsupials, with new insights provided by the use of advanced analytical techniques and the interrogation of the most complete databases of marsupials that are available. The following chapters address different aspects of the morphological diversity of marsupials, sometimes including fossil metatherians. The first one deals with the skull ontogeny of living marsupials, led by David Flores (Chap. ▶ 9), and the next examines function and constraint in the marsupial postcranium (Chap. ▶ 10), led by Meg Martin. The next chapter, led by Jamile Bubadué, similarly analyzes the drivers and constraints imposed on the marsupial skull based on the modern marsupial fauna (Chap. ▶ 11). The next two chapters deal with form and function, including biomechanics, in the living American and Australasian marsupial faunas, and some fossil taxa, as well as analyses of teeth and musculature. These chapters are led by Steve Wroe (Chap. ▶ 12) and Diego Astúa (Chap. ▶ 13). The chapter led by Juliana Quadros addresses morphological variation in the structure of the hair of American marsupials (Chap. ▶ 14). The last two chapters in this section deal with the diversification of two speciose genera of extant marsupials. Silvia Pavan (Chap. ▶ 15) discusses Monodelphis from the Americas and Mathew Crowther (Chap. ▶ 16) leads discussion on Antechinus from Australia, with both treatments including recently described taxa and placing emphasis on phenotypic evolution. The section on “Biogeography” opens with a presentation on trait variation in American marsupials (Chap. ▶ 17), led by Nilton Cáceres. The following two chapters address how old and new marsupial lineages occupy the geographical space today, and the factors explaining the marsupial diversity in the Americas. These chapters are led by Marcelo Weber (Chap. ▶ 18) and Felipe Cerezer (Chap. ▶ 19). The next four chapters focus on the diversity patterns, population variation, and endemism in the main biogeographical regions of South America, from the Amazon basin and Guiana’s uplands to the open, savanna, grassland, and marshland areas, south to the Amazon. These chapters are led by Cibele Bonvicino (Chap. ▶ 20), François Catzeflis (Chap. ▶ 21; in memoriam), Ana Paula Carmignotto (Chap. ▶ 22), and Ana Delciellos (Chap. ▶ 23). The next four chapters describe patterns of marsupial endemism, origin, diversity, and species status in major regions of Australia. Chapter ▶ 24, led by Alyson StoboWilson, discusses the environment and marsupial fauna of Australia’s Top End and Kimberley regions. Chapters ▶ 25–▶ 27, led in turn by Tyrone Lavery, Chris Dickman, and Menna Jones, then characterize the marsupials and their respective environments in Australia’s north-eastern tropics, arid zone, and temperate forests, woodlands, and heathlands. The final section of the book, on “Ecology and Conservation,” begins with a review of the population dynamics of American marsupials. Led by Rosana Gentile, Chapter ▶ 28 describes population attributes of Neotropical marsupials and uncovers the major factors that shape patterns of population change. The next two

Preface

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chapters (Chaps. ▶ 29 and ▶ 30) describe aspects of the reproductive biology of marsupials. The first chapter, led by Priscilla Zangrandi, focuses in particular on the phenomenon of semelparity in American marsupials, while the next chapter, led by Marissa Parrott, covers both semelparity and the range of other reproductive strategies that is exhibited by Australasian marsupials. Chapter ▶ 31, led by Ana Delciellos, discusses the locomotor performance of American marsupials and how this is influenced by the habitats and substrates where they occur. The next chapters cover the broad topic areas of movements, home range, and habitat selection in marsupials, and the factors that affect these aspects of the animals’ ecology. The review of these topics for American marsupials is led by Nilton Cáceres (Chap. ▶ 32), and the equivalent chapter for Australasian marsupials is by Ross Goldingay (Chap. ▶ 33). Three chapters then follow on marsupial food habits and diets. The first of these, led by Leonardo Lessa (Chap. ▶ 34), classifies and describes the diets of American marsupials; the next is led by Nícholas de Camargo (Chap. ▶ 35) and focuses on the variation in marsupial diets in the Neotropical savanna. In Chap. ▶ 36, led by Chris Dickman, the diets and activity patterns of Australasian marsupials are described. The activity theme is continued by Mariana Ferreira in Chap. ▶ 37, and covers what is known of the daily and longer term activity patterns of American marsupials. The two following chapters in this section review key aspects of marsupial physiology and how physiological adaptations equip marsupials to exploit a broad range of environments. Chap. ▶ 38, led by Fritz Geiser, collates and reviews information on torpor and heterothermy in American and Australasian marsupials, and Chap. ▶ 39, led by Phil Withers, provides an equivalently broad overview of energy and water balance in the world’s marsupials. The final 11 chapters deal with different aspects of marsupial conservation, reflecting the importance of this topic in the American and Australasian regions where so much environmental change is now occurring. Chapters ▶ 40 and ▶ 41 provide overviews of the conservation biogeography of modern marsupials. The first of these chapters (Chap. ▶ 40), led by Gabriel M. Martin, deals with the American marsupial fauna, and the second (Chap. ▶ 41), led by John Woinarski, considers the marsupials of Australasia. Four chapters then are concerned with the impacts of habitat loss and habitat fragmentation on marsupials. Chapters ▶ 42–▶ 44 document the effects of these disturbance processes on American marsupials, then on the didelphid marsupials of Brazil’s Atlantic forest, and then on the marsupials of the Australasian region. These chapters are led, respectively, by Marcus Vieira, Geruza Melo, and David Lindenmayer. Led by Rafael Loyola, Chap. ▶ 45 then provides a different perspective on habitat loss by reviewing the marsupials that occur in protected areas in Brazil. The next two chapters consider urban marsupials. Led by Stephanie Simioni, Chap. ▶ 46 discusses interactions between people and a large marsupial – Didelphis aurita – in a Brazilian case study, while Chap. ▶ 47, led by Loren Fardell, provides a general review of the risks and rewards that marsupials face when exploiting urban environments. The next chapter (Chap. ▶ 48), led by Francisco Fontúrbel, documents the habitat-related threats to a range-restricted and relict marsupial, the Monito

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del Monte. The two concluding chapters focus mostly on Australasian marsupials and consider the broad range of threats that they face as well as potential solutions for effective conservation management. Chapter ▶ 49, led by Tim Doherty, reviews the problems posed by multiple and simultaneously operating threats, while Chap. ▶ 50, led by Sarah Legge, provides a prospectus of novel and emerging strategies to improve the conservation outlook for marsupials. Santa Maria, Brazil Camperdown, Australia June 2023

Nilton C. Cáceres Christopher R. Dickman

Acknowledgments

For the encouragement and excellent collaboration with the publishing staff and editorial team at Springer Nature: João Pildervasser Susanne Friedrichsen Sonal Nagpal Dharini Palanivel Jawahar Babu For Prof. Cáceres’ family: Roger Ferreira Cáceres Valeriano Milton Cáceres Jr. Eneida Gonçalves Cáceres For Prof. Dickman’s family: Carol McKechnie-Dickman Alice Dickman-Butler Matthew Butler For the giving of wisdom: Honors, postgraduate research students and colleagues, and the marsupials who were the subjects of collective study over many years.

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Contents

Volume 1 Part I 1

.......................................

1

American and Australasian Marsupials: An Introduction . . . . . . . Nilton C. Cáceres and Christopher R. Dickman

3

Part II 2

Introduction

Evolution and Diversification . . . . . . . . . . . . . . . . . . . . . . . . .

21

Diversity and Phylogeny of Marsupials and Their Stem Relatives (Metatheria) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Robin M. D. Beck

23

3

Taxonomy and Diversity of Living American Marsupials . . . . . . . Pablo Teta, M. Amelia Chemisquy, and Gabriel M. Martin

89

4

Taxonomic Checklist of Living American Marsupials . . . . . . . . . . Diego Astúa, Jorge J. Cherem, and Pablo Teta

115

5

Taxonomy and Diversity of Living Australasian Marsupials . . . . . Andrew M. Baker, Mark D. B. Eldridge, Diana O. Fisher, Greta Frankham, Kristofer Helgen, Stephen M. Jackson, Sally Potter, Kenny J. Travouillon, and Linette S. Umbrello

163

6

Cenozoic Metatherian Evolution in the Americas Francisco Javier Goin

.............

249

7

Paleogene Metatherians from the Itaboraí Basin: Diversity and Affinities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Leonardo M. Carneiro and Édison Vicente Oliveira

269

8

Molecular Evolution in Australasian Marsupials . . . . . . . . . . . . . . Sally Potter, Mark D. B. Eldridge, and Simon Y. W. Ho

325

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9

Contents

Postweaning Skull Growth in Living American and Australasian Marsupials: Allometry and Evolution . . . . . . . . . . . . David A. Flores, Fernando Abdala, and Norberto P. Giannini

357

10

Function and Constraint in the Marsupial Postcranium . . . . . . . . Meg L. Martin and Vera Weisbecker

403

11

Skull Morphological Evolution in Faunivorous Marsupials . . . . . . Jamile Bubadué, Nilton C. Cáceres, Mariana N. Brum, and Carlo Meloro

431

12

Marsupial Functional Morphology, Biomechanics, and Feeding Ecology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Stephen Wroe and Gabriele Sansalone

453

13

Morphology, Form, and Function in Didelphid Marsupials . . . . . . Diego Astúa and Gabby Guilhon

14

Hair Microstructure Diversity in Neotropical Marsupials: Roles of Phylogenetic Signal and Adaptation . . . . . . . . . . . . . . . . . Juliana Quadros, Felipe O. Cerezer, and Nilton C. Cáceres

515

Short-Tailed Opossums Genus Monodelphis: Patterns of Phenotypic Evolution and Diversification . . . . . . . . . . . . . . . . . . . . Silvia E. Pavan

537

Patterns of Phenotypic Evolution and Diversification in Antechinus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Mathew S. Crowther and Andrew M. Baker

559

15

16

Part III 17

18

19

20

Biogeography . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

Trait Variation in American Marsupials Based on Biological Rules . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Nilton C. Cáceres, Mariana N. Brum, Thaís F. Battistella, and Jamile Bubadué

483

577

579

Age-Area Relationships in American Marsupials: A Macroevolutionary Approach . . . . . . . . . . . . . . . . . . . . . . . . . . . Marcelo M. Weber and Marcos S. L. Figueiredo

605

Species Richness and Beta Diversity Patterns of American Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Felipe O. Cerezer, Nilton C. Cáceres, and Andrés Baselga

623

.......

639

Diversification of South American Didelphid Marsupials Cibele R. Bonvicino, Ana Lazar, Tatiana P. T. de Freitas, Rayque de O. Lanes, and Paulo S. D’Andrea

Contents

21

22

23

24

25

26

27

xvii

Marsupials in the Guiana Region (Northeastern Amazonia): Diversity and Endemism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . François Catzeflis

675

Marsupials from the South American “Dry Diagonal”: Diversity, Endemism, and Biogeographic History . . . . . . . . . . . . . . . . . . . . . Ana Paula Carmignotto and Diego Astúa

693

Species Richness and Endemism of Marsupials in the Atlantic Forest: Spatial Patterns and Drivers . . . . . . . . . . . . . . . . Ana C. Delciellos, Jayme A. Prevedello, Marcos S. L. Figueiredo, Marcelo M. Weber, and Maria L. Lorini

723

Diversity and Endemism of the Marsupials of Australia’s Top End and Kimberley . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Alyson M. Stobo-Wilson and Teigan Cremona

745

Diversity and Endemism of the Marsupials of Australia’s North-Eastern Tropics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Tyrone H. Lavery and Luke K.-P. Leung

769

Diversity and Endemism of the Marsupials of Australia’s Arid Zone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Chris R. Dickman and Chris R. Pavey

797

Marsupials of Australia’s Temperate and Subtropical Forests, Woodlands and Heathlands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Menna Jones, Peter Menkhorst, and Barbara Wilson

839

Volume 2 Part IV

Ecology and Conservation . . . . . . . . . . . . . . . . . . . . . . . . . .

877

28

Population Dynamics of Neotropical Marsupials . . . . . . . . . . . . . . Rosana Gentile, Maja Kajin, and Helena Godoy Bergallo

29

Semelparous Reproductive Strategy in New World Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Priscilla L. Zangrandi and Emerson M. Vieira

903

Reproductive Strategies and Biology of the Australasian Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Marissa L. Parrott and Amy M. Edwards

931

30

31

Positional Behavior and Locomotor Performance of American Marsupials: Links with Habitat and Substrate Use . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ana C. Delciellos and Marcus V. Vieira

879

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Contents

32

Movement, Habitat Selection, and Home Range of American Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1005 Nilton C. Cáceres, Ana C. Delciellos, Jayme A. Prevedello, Mariana N. Brum, and M. Soledad Albanese

33

Movement Patterns, Home Range and Habitat Selection of Australasian Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1033 Ross L. Goldingay

34

Food Habits of American Marsupials . . . . . . . . . . . . . . . . . . . . . . . 1095 Leonardo G. Lessa, Rone F. Carvalho, and Diego Astúa

35

Marsupials in a Neotropical Savanna: Diet Variation and Seasonal Patterns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1123 Nícholas F. de Camargo and Emerson M. Vieira

36

Food Habits and Activity Patterns of Australasian Marsupials . . . 1151 Christopher R. Dickman and Michael C. Calver

37

Activity Patterns of American Marsupials . . . . . . . . . . . . . . . . . . . 1189 Mariana Silva Ferreira

38

Daily Torpor, Hibernation, and Heterothermy in Marsupials . . . . 1221 Fritz Geiser and Christine E. Cooper

39

Energy and Water Balance of Marsupials . . . . . . . . . . . . . . . . . . . 1249 Philip C. Withers and Christine E. Cooper

40

Conservation Biogeography of Living American Marsupials: Didelphimorphia, Microbiotheria, and Paucituberculata . . . . . . . . 1291 Gabriel M. Martin, Baltazar González, Federico Brook, and Adrian Monjeau

41

Conservation Biogeography of Modern Species of Australasian Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1319 John C. Z. Woinarski and Diana O. Fisher

42

Impact of Habitat Loss and Fragmentation in Assemblages, Populations, and Individuals of American Marsupials . . . . . . . . . 1367 Marcus V. Vieira, Camila S. Barros, and Ana C. Delciellos

43

Impact of Habitat Loss and Fragmentation in Didelphid Marsupials of the Atlantic Forest . . . . . . . . . . . . . . . . . . . . . . . . . . 1395 Geruza L. Melo

44

Impact of Habitat Loss and Fragmentation on Assemblages, Populations, and Individuals of Australasian Marsupials . . . . . . . 1413 David B. Lindenmayer and Christopher R. Dickman

Contents

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45

Marsupials and the Coverage Provided by Protected Areas in Brazil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1445 Rafael Loyola, Raísa R. S. Vieira, and Bruno R. Ribeiro

46

Human-Wildlife Interactions in Urban Areas: Case of Didelphis aurita . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1463 Stephanie Santos Simioni, Fernando Silvério Ribeiro, Renata Pardini, and Thomas Püttker

47

Marsupials in Urban Environments . . . . . . . . . . . . . . . . . . . . . . . . 1483 Loren L. Fardell and Christopher R. Dickman

48

Relict Marsupial (Dromiciops) from Southern South American Temperate Rainforests: Threatened by Habitat Loss, Fragmentation, and Transformation . . . . . . . . . . . . . . . . . . . . . . . 1515 Francisco E. Fontúrbel and Gloria B. Rodríguez-Gómez

49

Multiple Threats Affecting the Marsupials of Australasia: Impacts and Management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1531 Tim S. Doherty, William L. Geary, Vivianna Miritis, and Darcy J. Watchorn

50

Novel Conservation Strategies to Conserve Australian Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1555 Sarah Legge, Matt Hayward, and Andrew Weeks

Glossary

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1585

Index . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1605

About the Editors

Nilton Cáceres work focuses mostly on the ecology and evolution of mammals, particularly marsupials, rodents, carnivores, and primates. Nilton is a Professor of Vertebrate Zoology and Animal Behavior at the Federal University of Santa Maria and a Research Fellow at the Brazilian National Council for Scientific and Technological Development (CNPq). He has written more than 150 journal articles and book chapters, as well as been editor and co-editor of Marsupials of Brazil (2006 and 2012) and The Mammals of Rio Grande do Sul (2013). His research has had international collaborations with, among others, Argentinean, Spanish, Italian, and English researchers, focusing mainly on the Neotropical fauna. Christopher R. Dickman work focuses mostly on the ecology of mammals and on a range of projects in applied conservation and management. Chris is a Professor of Ecology (personal chair) at The University of Sydney and a Fellow of both the Australian Academy of Science and the Royal Zoological Society of New South Wales. He has written more than 500 journal articles and book chapters, as well as several monographs on marsupials including the award-winning A Fragile Balance: The Extraordinary Story of Australian Marsupials and Secret Lives of Carnivorous Marsupials (with Andrew Baker); he is also co-editor of Marsupials and Predators with Pouches: The Biology of Carnivorous Marsupials. He is the recipient of several national and international awards, including the Troughton Medal from the Australian Mammal Society and the C. Hart Merriam award from the American Society of Mammalogists. xxi

List of Reviewers

Ana Paula Carmignotto São Carlos, Brazil Andrew M. Baker Brisbane, Australia Bruce D. Patterson Chicago, USA Burtom Lim Toronto, Canada Carlos E. V. Grelle Rio de Janeiro, Brazil Christopher R. Dickman Sydney, Australia David B. Lindenmayer Canberra, Australia Diego Astúa Recife, Brazil Douglass Rovinsky Melbourne, Australia Emerson M. Vieira Brasília, Brazil Erin Mein Brisbane, Australia Felipe Barreto Covallis, USA Fernando Fernandez Rio de Janeiro, Brazil Fernando Perini Belo Horizonte, Brazil Gabriel M. Martin Esquel, Argentina Geruza L. Melo Santa Maria, Brazil Heather Liwanag San Luis Obispo, USA Janine M. Ziermann Washington, DC, USA Jonas Sponchiado Alegrete, Brazil Laura Wilson Sydney, Australia Leonardo G. Lessa Diamantina, Brazil xxiii

xxiv

Loren L. Fardell Sydney, Australia M. Amelia Chemisquy La Rioja, Argentina M. Soledad Albanese Mendoza, Argentina Marcelo M. Weber Palmeira das Missões, Brazil Marcelo Sánchez-Villagra Zurich, Switzerland Marcus V. Vieira Rio de Janeiro, Brazil Mathew S. Crowther Sydney, Australia Maurício Graipel Florianopolis, Brazil Mike Archer Sydney, Australia Michael C. Calver Perth, Australia Natalia Zimicz Salta, Argentina Nícholas F. de Camargo Brasíllia, Brazil Nilton C. Cáceres Santa Maria, Brazil Olga Chernova Moscow, Russia Renan Maestri Porto Alegre, Brazil Rita Gomes Rocha Vairão, Portugal Robert Voss New York, USA Rosana Gentile Rio de Janeiro, Brazil Silvia E. Pavan Belém, Brazil Thomas Püttker Diadema, Brazil Tom Giarla Loudonville, USA

List of Reviewers

Contributors

Fernando Abdala Unidad Ejecutora Lillo (Consejo Nacionalde Investigaciones Científicas y Técnicas-Fundación Miguel Lillo), Tucumán, Argentina Evolutionary Studies Institute, University of the Witwatersrand, Johannesburg, South Africa M. Soledad Albanese Grupo de Investigaciones de la Biodiversidad (GiB), Instituto Argentino de Investigaciones de las Zonas Áridas (IADIZA), CCT Mendoza, CONICET, CP, Mendoza, Argentina Diego Astúa Laboratório de Mastozoologia, Departamento de Zoologia, Centro de Biociências, Universidade Federal de Pernambuco, Recife, PE, Brazil Andrew M. Baker School of Biology and Environmental Science, Queensland University of Technology, Brisbane, QLD, Australia Biodiversity and Geosciences Program, Queensland Museum, South Brisbane, Australia Natural Environments Program, Queensland Museum, South Brisbane, QLD, Australia Camila S. Barros Departamento de Ecologia, Programa de Pós-Graduação em Ecologia, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil Andrés Baselga Depto de Zoología, Facultad de Biología, Univ. de Santiago de Compostela, Santiago de Compostela, Spain Thaís F. Battistella Programa de Pós-Graduação em Biodiversidade Animal, CCNE, Universidade Federal de Santa Maria, Santa Maria, RS, Brazil Robin M. D. Beck School of Science, Engineering and Environment, University of Salford, Salford, UK Helena Godoy Bergallo Department of Ecology, Institute of Biology Roberto Alcantara Gomes – IBRAG, Rio de Janeiro State University – UERJ, Rio de Janeiro, Brazil

xxv

xxvi

Contributors

Cibele R. Bonvicino Genetics Division, José Gomes de Alencar National Cancer Institute, Rio de Janeiro, RJ, Brazil Laboratório de Biologia e Parasitologia de Mamíferos Reservatórios, Instituto Oswaldo Cruz, Rio de Janeiro, RJ, Brazil Federico Brook Centro de Investigación Esquel de Montaña y Estepa Patagónica (CIEMEP), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) – Universidad Nacional de la Patagonia “San Juan Bosco” (UNPSJB), Esquel, Chubut, Argentina Laboratorio de Investigaciones en Evolución y Biodiversidad, Facultad de Ciencias Naturales y Ciencias de la Salud. Sede Esquel, UNPSJB, Esquel, Chubut, Argentina Mariana N. Brum Programa de Pós-Graduação em Biodiversidade Animal, CCNE, Universidade Federal de Santa Maria, Santa Maria, RS, Brazil Jamile Bubadué Laboratório de Ciências Ambientais, Universidade Estadual do Norte Fluminense Darcy Ribeiro, Campos dos Goytacazes, RJ, Brazil Nilton C. Cáceres Laboratório de Mastozoologia, Departamento de Ecologia e Evolução, CCNE, Universidade Federal de Santa Maria, Santa Maria, RS, Brazil Michael C. Calver Environmental and Conservation Sciences, Murdoch University, Murdoch, WA, Australia Ana Paula Carmignotto Laboratório de Diversidade Animal, Departamento de Biologia, Centro de Ciências Humanas e Biológicas, Universidade Federal de São Carlos, Sorocaba, Brazil Leonardo M. Carneiro Programa de Pós-graduação em Geociências (PPGEOC), Departamento de Geologia, Centro de Tecnologia e Geociências, Universidade Federal de Pernambuco, Recife, PE, Brazil The Paleontology and Paleoecology Laboratory, Natural History Society, Torres Vedras, Portugal Rone F. Carvalho Laboratório de Ecologia, Departamento de Ciências Biológicas, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina, MG, Brazil François Catzeflis Emeritus Researcher. CNRS and University of Montpellier. Institute of Evolutionary Sciences, University of Montpellier, Montpellier, France Felipe O. Cerezer Programa de Pós-Graduação em Biodiversidade Animal, Centro de Ciências Naturais e Exatas, Universidade Federal de Santa Maria, Santa Maria, RS, Brazil M. Amelia Chemisquy CONICET, Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina Museo de Ciencias Antropológicas y Naturales, Universidad Nacional de La Rioja, La Rioja, Argentina

Contributors

xxvii

Jorge J. Cherem Caipora Cooperativa, Av. Desembargador Vítor Lima, Florianópolis, SC, Brazil Christine E. Cooper School of Molecular and Life Sciences, Curtin University, Perth, WA, Australia Teigan Cremona Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT, Australia Mathew S. Crowther School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, Australia Paulo S. D’Andrea Laboratório de Biologia e Parasitologia de Mamíferos Reservatórios, Instituto Oswaldo Cruz, Rio de Janeiro, RJ, Brazil Nícholas F. de Camargo Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade de Brasília, Brasília, Brazil Ana C. Delciellos Programa de Pós-Graduação em Ecologia e Evolução, Instituto de Biologia Roberto Alcântara Gomes, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, RJ, Brazil Christopher R. Dickman School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, Australia Tim S. Doherty School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, Australia Amy M. Edwards New South Wales National Parks and Wildlife Service, Dubbo, NSW, Australia University of New England, Armidale, NSW, Australia Mark D. B. Eldridge Australian Museum Research Institute, Darlinghurst, NSW, Australia Loren L. Fardell School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, Australia Mariana Silva Ferreira Mestrado Profissional em Ciências do Meio Ambiente. Rua Ibituruna, Universidade Veiga de Almeida, Rio de Janeiro, Brazil Marcos S. L. Figueiredo Instituto de Biociências, Programa de Pós-Graduação em Biodiversidade Neotropical, Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro, Brazil Diana O. Fisher School of Biological Sciences, University of Queensland, St Lucia, QLD, Australia David A. Flores Unidad Ejecutora Lillo (Consejo Nacional de Investigaciones Científicas y Técnicas-Fundación Miguel Lillo), Instituto de Vertebrados, Fundación Miguel Lillo, Tucumán, Argentina

xxviii

Contributors

Francisco E. Fontúrbel Instituto de Biología, Facultad de Ciencias, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile Greta Frankham Australian Museum Research Institute, Darlinghurst, NSW, Australia Tatiana P. T. de Freitas Laboratório de Biologia e Parasitologia de Mamíferos Reservatórios, Instituto Oswaldo Cruz, Rio de Janeiro, RJ, Brazil William L. Geary Centre for Integrative Ecology, School of Life and Environmental Sciences (Burwood campus), Deakin University, Waurn Ponds, VIC, Australia Biodiversity Strategy and Knowledge Branch, Biodiversity Division, Department of Environment, Land, Water and Planning, East Melbourne, VIC, Australia Fritz Geiser Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, NSW, Australia Rosana Gentile Laboratory of Biology and Parasitology of Wild Reservoir Mammals, Oswaldo Cruz Institute, Oswaldo Cruz Foundation – FIOCRUZ, Rio de Janeiro, Brazil Norberto P. Giannini Unidad Ejecutora Lillo (Consejo Nacionalde Investigaciones Científicas y Técnicas-Fundación Miguel Lillo), Tucumán, Argentina Cátedra de Biogeografía, Universidad Nacional de Tucumán, Tucumán, Argentina Francisco Javier Goin CONICET (Consejo Nacional de Investigaciones Científicas y Técnicas), Buenos Aires, Argentina División Paleontología Vertebrados, Facultad de Ciencias Naturales y Museo, Universidad Nacional de La Plata, La Plata, Argentina Ross L. Goldingay Faculty of Science & Engineering, Southern Cross University, Lismore, NSW, Australia Baltazar González Centro de Investigación Esquel de Montaña y Estepa Patagónica (CIEMEP), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) – Universidad Nacional de la Patagonia “San Juan Bosco” (UNPSJB), Esquel, Chubut, Argentina Gabby Guilhon Laboratório de Mastozoologia, Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, MG, Brazil Matt Hayward Conservation Science Research Group, School of Environment and Life Sciences, University of Newcastle, Callaghan, NSW, Australia

Contributors

xxix

Centre for African Conservation Ecology, Nelson Mandela University, Gqeberha, South Africa Kristofer Helgen Australian Museum Research Institute, Darlinghurst, NSW, Australia Simon Y. W. Ho School of Life and Environmental Sciences, University of Sydney, Sydney, NSW, Australia Stephen M. Jackson Australian Museum Research Institute, Darlinghurst, NSW, Australia School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW, Australia Menna Jones School of Natural Sciences, University of Tasmania, Hobart, TAS, Australia Maja Kajin Ecology and Environment Conservation, Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia Department of Zoology, University of Oxford, Oxford, UK Rayque de O. Lanes Postgraduate Program in Genetics, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil Tyrone H. Lavery Fenner School of Environment and Society, The Australian National University, Canberra, ACT, Australia Ana Lazar Department of Vertebrates, National Museum, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil Sarah Legge Fenner School of Environment and Society, The Australian National University, Canberra, ACT, Australia Research Institute of Environment and Livelihoods, Charles Darwin University, Casuarina, NT, Australia Leonardo G. Lessa Laboratório de Ecologia, Departamento de Ciências Biológicas, Universidade Federal dos Vales do Jequitinhonha e Mucuri, Diamantina, MG, Brazil Luke K.-P. Leung Rodent Testing Centre, Gatton, QLD, Australia David B. Lindenmayer Fenner School of Environment & Society, The Australian National University, Canberra, ACT, Australia Maria L. Lorini Instituto de Biociências, Departamento de Ciências Naturais, Universidade Federal do Estado do Rio de Janeiro, Rio de Janeiro, Brazil Rafael Loyola International Institute for Sustainability, Rio de Janeiro, RJ, Brazil Departamento de Ecologia, Universidade Federal de Goiás, Goiânia, Brazil

xxx

Contributors

Gabriel M. Martin Centro de Investigación Esquel de Montaña y Estepa Patagónica (CIEMEP), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) – Universidad Nacional de la Patagonia “San Juan Bosco” (UNPSJB), Esquel, Chubut, Argentina Laboratorio de Investigaciones en Evolución y Biodiversidad (LIEB), Facultad de Ciencias Naturales y Ciencias de la Salud. Sede Esquel, UNPSJB, Esquel, Chubut, Argentina Meg L. Martin College of Science & Engineering, Flinders University, Adelaide, SA, Australia Geruza L. Melo Instituto Federal de Educação, Ciência e Tecnologia Farroupilha – IFFAR – Campus Alegrete, Alegrete, Brazil Carlo Meloro Research Centre in Evolutionary Anthropology and Palaeoecology, School of Biological and Environmental Sciences, Liverpool John Moores University, Liverpool, UK Peter Menkhorst Arthur Rylah Institute for Environmental Research, Department of the Environment, Land, Water and Planning, Heidelberg, VIC, Australia Vivianna Miritis School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, Australia Adrian Monjeau Fundacion Bariloche and CONICET, San Carlos de Bariloche, Argentina Édison Vicente Oliveira Laboratório de Paleontologia, Departamento de Geologia, Centro de Tecnologia e Geociências, Universidade Federal de Pernambuco, Recife, PE, Brazil Renata Pardini Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil Marissa L. Parrott Wildlife Conservation and Science, Zoos Victoria, Parkville, VIC, Australia Silvia E. Pavan California State University, Cal Poly Humboldt, Department of Biological Sciences, Arcata, CA, USA Chris R. Pavey CSIRO Environment, Winnellie, NT, Australia Sally Potter Australian Museum Research Institute, Darlinghurst, NSW, Australia School of Natural Sciences, Macquarie University, Sydney, NSW, Australia Jayme A. Prevedello Departamento de Ecologia, Laboratório de Ecologia de Paisagens, Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil Thomas Püttker Departamento de Ciências Ambientais, Universidade Federal de São Paulo, Diadema, SP, Brazil

Contributors

xxxi

Juliana Quadros Setor Litoral, Universidade Federal do Paraná, Matinhos, PR, Brazil Bruno R. Ribeiro Programa de Pós-graduação em Ecologia e Evolução, Universidade Federal de Goiás, Goiânia, Brazil Fernando Silvério Ribeiro Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil Gloria B. Rodríguez-Gómez Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Santiago, Chile Gabriele Sansalone Function, Evolution and Anatomy Research Lab, Zoology Division, School of Environmental and Rural Science, University of New England, Armidale, NSW, Australia Stephanie Santos Simioni Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil Alyson M. Stobo-Wilson CSIRO Land and Water, Winnellie, NT, Australia Pablo Teta División Mastozoología, Museo Argentino de Ciencias Naturales “Bernardino Rivadavia”, Buenos Aires, Argentina CONICET, Consejo Nacional de Investigaciones Científicas y Técnicas, Buenos Aires, Argentina Kenny J. Travouillon Collections and Research, Western Australian Museum, Welshpool, WA, Australia Linette S. Umbrello School of Biology and Environmental Science, Queensland University of Technology, Brisbane, Australia Collections and Research, Western Australian Museum, Welshpool, WA, Australia Emerson M. Vieira Laboratório de Ecologia de Vertebrados, Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade de Brasília, Brasília, DF, Brazil Marcus V. Vieira Departamento de Ecologia, Laboratório de Vertebrados, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil Raísa R. S. Vieira Instituto Internacional para Sustentabilidade, Rio de Janeiro, Brazil Darcy J. Watchorn Centre for Integrative Ecology, School of Life and Environmental Sciences (Burwood campus), Deakin University, Waurn Ponds, VIC, Australia Marcelo M. Weber Departamento de Zootecnia e Ciências Biológicas, Universidade Federal de Santa Maria, Palmeira das Missões, Brazil

xxxii

Contributors

Andrew Weeks School of BioSciences, University of Melbourne, Parkville, VIC, Australia Cesar Australia, Brunswick, VIC, Australia Vera Weisbecker College of Science & Engineering, Flinders University, Adelaide, SA, Australia Centre of Excellence for Australian Biodiversity and Heritage, Flinders University, Adelaide, SA, Australia Barbara Wilson School of Life and Environmental Sciences, Deakin University, Geelong, VIC, Australia Philip C. Withers School of Biological Sciences, University of Western Australia, Crawley, WA, Australia John C. Z. Woinarski Research Institute for the Environment and Livelihoods, Charles Darwin University, Darwin, NT, Australia Stephen Wroe Function, Evolution and Anatomy Research Lab, Zoology Division, School of Environmental and Rural Science, University of New England, Armidale, NSW, Australia Priscilla L. Zangrandi Laboratório de Ecologia de Vertebrados, Departamento de Ecologia, Instituto de Ciências Biológicas, Universidade de Brasília, Brasília, DF, Brazil

Abbreviations

The abbreviations below include standard abbreviations used for items such as units of measurement as well as abbreviations that have been adopted for specific purposes in different chapters. Occasionally the same abbreviation may be used to connote different things (e.g., C is used as an abbreviation for “Carnivore,” “Degrees Celsius,” and “Thermal conductance”), but it will be obvious from the context which meaning is intended. Additional abbreviations, not listed here, are defined where they are used in the headings of tables or the legends of figures in specific chapters. ΔP ΔT A AA ACR ACTH ADF AET AF AIC AICc AM AMF AMNH AO

AP Ar asl AUC AUS AVP βjac

Precipitation seasonality Temperature seasonality Arboreal Age-area model Atlantic Coast restingas Adrenocorticotropic hormone Atlantic dry forests Actual evapotranspiration Atlantic Forest biome Akaike information criterion Akaike information criterion corrected for small samples Amazon biome Araucaria moist forests American Museum of Natural History, New York, NY, USA Area of occupancy, an area that describes the locations where a species is most likely to be found within its larger extent of occurrence (EOO) Alto Paraná Atlantic forests Araucária Above sea level Area under the receiver operating characteristic curve Australia Arginine vasopressin Jaccard dissimilarity index xxxiii

xxxiv

βjtu βjne Ba BAM bp BCF BEAST BIF BM BMR BN BOM C C o C CA CBD CBG Cdry CEWL CMF CMR CR CR CREA CRH CSIRO Cwet CYP CYP2C

DD DD DEPAVE-3 Di DMNT1 DMNT2 DMNTs DNA E

Abbreviations

Spatial turnover Nestedness-resultant dissimilarities Bahia Breadth between molars Base pairs Bahia coastal forests Bayesian evolutionary analysis sampling trees Bahia interior forests Brownian motion Basal metabolic rate Brejos Nordestinos Australian Bureau of Meteorology Thermal conductance Carnivore Degree Celsius Caatinga biome Convention on Biological Diversity Corticosteroid-binding globulin (transcortin) Dry thermal conductance Cutaneous evaporative water loss Caatinga enclaves moist forests Capture-mark-recapture technique Campos rupestres montane savanna Critically endangered Craniofacial evolutionary allometry Corticotropin-releasing hormone Commonwealth Scientific and Industrial Research Organisation (Australia) Wet thermal conductance Cape York Peninsula Gene which plays roles in detoxification (Koala), part of the subfamily of the cytochrome P450 mixed-function oxidase system Data deficient “Dry Diagonal” Divisão Técnica de Medicina Veterinária e Manejo da Fauna Silvestre 3 Diamantina DNA methyltransferase 1 DNA methyltransferase 2 DNA methyltransferases, a conserved family of cytosine methylases which facilitate DNA methylation Deoxyribonucleic acid East

Abbreviations

EECO EHL ELEV ELEV- SD EN ENM EOB EOO EPBC Act ESF EWL EX F FABI FI FMR FVS FWTR g GABI Gb GBIF GC GEE GI GIS GLM ha HAH HPA HPD i I IBE IBRA Id IEPA ILs IMG IMGF In IND

xxxv

Early Eocene climatic optimum Evaporative heat loss Elevation Standard deviation of elevation or surface roughness Endangered Ecological niche modeling Eocene-Oligocene boundary Extent of occurrence, a minimum convex polygon that encompasses all distributional records of a species Environment Protection and Biodiversity Conservation Act (Australia) Eigenvector spatial filters Evaporative water loss Extinct Fisher statistic value of analysis of variance First American Biotic Interchange Family inference Field metabolic rate Forest vertical structure Field water turnover rate Grams Great American Biotic Interchange Gigabases Global Biodiversity Information Facility Glucocorticoids (cortisol/corticosterone) Geometric edge effects Genus inference Geographic information system Generalized linear model Hectare Habitat amount hypothesis Hypothalamic-pituitary-adrenal Highest posterior density intervals Lower incisors (numbers indicate their corresponding locus) Insectivore Interbout euthermia Interim biogeographic regionalization for Australia Idiosyncratic model Instituto de Pesquisas Científicas e Tecnológicas do Estado do Amapá Indigenous lands Itaboraí metatherian group Itaboraí metatherian group femur Interior Indonesia

xxxvi

IUCN JL JS K2p km km2 KoRV KTR LC LC LINEs LTRs m m m1-4 M M M1-4 Ma, Megannum MACN MAHAL MAM MASH masl MAT MCNFZB MCN-PV

MCT (ex DGM) MD MDS MF MFL MHC MHNC MHNCI MHP MJ ML MLP

Abbreviations

International Union for Conservation of Nature Jaw length Jolly-Seber method (for estimating population size) Kimura two parameter distance Kilometer Square kilometers Koala retrovirus, a major pathogen of the Koala Cretaceous terrestrial revolution Least concern Locomotion categories Long interspersed nuclear elements Long terminal repeats Meter Lower molars Lower first-fourth molar Body mass Upper molars Upper first-fourth molar One million years in the radioisotopic time scale Museo Argentino de Ciencias Naturales “Bernardino Rivadavia” Mahalanobis distance Moment arm of masseter Minimum area of suitable habitat Meters above sea level Moment arm of temporalis Museu de Ciências Naturais da Fundação Zoobotânica do Rio Grande do Sul Seção de Paleontologia, Museu de Ciências Naturais da Fundação Zoobotânica do Rio Grande do Sul, Porto Alegre, RS, Brazil Museu de Ciências da Terra, Rio de Janeiro, RJ, Brazil Morphological disparity Multidimensional scaling Inference based on morphological features Masseteric fossa length Major histocompatibility complex Museo de Historia Natural de Cochabamba, Cochabamba, Bolivia Museu de História Natural Capão do Imbuia Metabolic heat production Median-joining Maximum likelihood Museo de La Plata, La Plata, Argentina

Abbreviations

mm MMR MN MNHN MNKA MPEG MPTs MR MRCA MS mt-Cytb mtDNA MWP MYA MZUSP n N NA NALMA NE NG NHM NPP NST NT O OU p P P P PA PA PC PCA PC1 PC2 PCF PCoA PCR PCSA PCV Pe PET

xxxvii

Millimeters Maximal metabolic rate Museu Nacional do Rio de Janeiro, Rio de Janeiro, RJ, Brazil Muséum National d’Histoire Naturelle, Paris, France Minimum number known alive Museu Paraense Emílio Goeldi Most parsimonious trees Metabolic rate Most recent common ancestor Length of upper molar series Mitochondrial cytochrome b Mitochondrial DNA Metabolic water production Million years ago Museu de Zoologia da Universidade de São Paulo number, or sample size North Not assessed North American land-mammal age Not evaluated New Guinea Natural History Museum Net primary productivity Non-shivering thermogenesis Near threatened Omnivore Ornstein-Uhlenbeck Lower premolars Upper premolars Primary forest Probability Pampa biome Protected area Principal component Principal components analysis First axis of a principal component analysis Second axis of a principal component analysis Pernambuco coastal forests Principal coordinate analysis Polymerase chain reaction Physiological cross-sectional area Pixel conservation value Pernambuco Potential evapotranspiration

xxxviii

PETM PGLS PIF PL Pmin PMS PNG PRWE PT PVA R2 REM REWL RH RMR RMT RNA RSX RT RTESINE2 RWE S SALMA SAq Sc SC SD SdM SDM SE SEM SEM SF SI SINEs SL SL SLD SM SM SMR SNUC

Abbreviations

Paleocene-Eocene thermal maximum Phylogenetic generalized least squares Pernambuco interior forests Palatal length Precipitation of driest month Length of upper pre-molar series Papua New Guinea Point of relative water economy Pantanal biome Population viability analysis Coefficient of determination Rapid eye-movement sleep Respiratory evaporative water loss Relative humidity Resting metabolic rate Relative medullary thickness of the kidney Ribonucleic acid RNA on the silent X, non-coding RNA on the X chromosome which is silenced Radio telemetry A short interspersed nuclear elements with an RTE (retrotransposon element) Relative water economy South South American Land-Mammal Age Semiaquatic Scansorial Total number of specimens with cranium Standard deviation Serra do Mar Species distribution model Standard error Scanning electron microscope Structural equation model São Francisco Subfamily inference Short interspersed nuclear elements Skull length Spool-and-line tracking Straight line distance Serra do Mar coastal forests Total number of specimens with mandible Standard metabolic rate National system of protected areas

Abbreviations

SOI SOL SPE spp. SRTM SRY SSD SShD StA StB StC StD StE SVM SWS T Ta Tb TBD TBW TC TCR TEMP Tlc Tmax Tmean Tmin TMR TNZ TNZbreadth TSS Tuc UCP1 UCP2 UCP3 UFPE UFRGS UFRJ UFSC UFSM UM

xxxix

Southern oscillation index Solomon Islands Stasis post-expansion model Refers to multiple species in a genus Shuttle radar topography mission Sex-determining region Y Sexual size dimorphism Skull shape Stylar cusp A Stylar cusp B Stylar cusp C Stylar cusp D Stylar cusp E Support vector machine Short wave sleep Terrestrial Ambient temperature Body temperature Torpor bout duration Total body water Taxon cycle model T-cell receptor, a novel immune gene found in the Tammar Wallaby Temperature, can be temperature seasonality Lower critical temperature of thermoneutral zone Maximum temperature of hottest month Annual mean temperature Minimum temperature of coldest month Torpor metabolic rate Thermoneutral zone Breadth of the thermoneutral zone True skill statistic Upper critical temperature of thermoneutral zone Uncoupling protein one Uncoupling protein two Uncoupling protein three Universidade Federal de Pernambuco, Recife, PE, Brazil Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil Universidade Federal de Santa Catarina Universidade Federal de Santa Maria Marsupial specific MHC class Ib gene

xl

Umax UNEMAT VIF VU W WALLSI1 WDPA WEI WHO wi WML WSINE1 WT WTR XIST ZAW

Abbreviations

Maximum urinary concentration Universidade do Estado de Mato Grosso Variance inflation factor Vulnerable West Wallaby SINEs, short interspersed nuclear elements in the Tammar Wallaby World Database on Protected Areas Water economy index World Health Organization Akaike weight World Museum of Liverpool A CORE short interspersed nuclear element present in around 200,000 copies, is the most recently active element Wet Tropics Water turnover rate X-inactive specific transcript, locus on the X chromosome Zygomatic arm width

Part I Introduction

1

American and Australasian Marsupials: An Introduction Nilton C. Ca´ceres and Christopher R. Dickman

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 A Brief History of Research on American Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4 Origin, Evolution, and Diversification of the New World Marsupials . . . . . . . . . . . . . . . . . . . . . . 8 A Brief History of Research on Australasian Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9 Origin, Evolution, and Diversification of Australasian Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . 14 Cross-References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

Abstract

This chapter introduces the book by telling how the history of research on American and Australasian marsupials has developed up to now. It focuses on the main disciplines that aim to study the diversity of marsupials and other metatherians, from the past to today. These disciplines are taxonomy, systematics, biogeography, ecology, and conservation. Through these lines the reader will meet some of the key researchers in these disciplines and discover how they led to fantastic discoveries of marsupials in different continents. Later, a brief introduction to the evolution and diversification of marsupials in the Americas and Australasia is provided.

N. C. Cáceres Departamento de Ecologia e Evolução, CCNE, Universidade Federal de Santa Maria, Santa Maria, RS, Brazil e-mail: [email protected] C. R. Dickman (*) School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, Australia e-mail: [email protected] © Springer Nature Switzerland AG 2023 N. C. Cáceres, C. R. Dickman (eds.), American and Australasian Marsupials, https://doi.org/10.1007/978-3-031-08419-5_2

3

N. C. Ca´ceres and C. R. Dickman

4

Keywords

America · Australia · Metatherians · Ecology · Evolution · Diversification · Taxonomy · Systematics

Introduction A great deal has been learned about marsupials over the last couple of hundred years, with the rate of discovery of new species and increase in understanding of different aspects of marsupial biology escalating in recent decades. Much of this knowledge expansion has occurred because of an increased appreciation of marsupials and the roles they play in the varied environments where they occur, as well as recognition that many species are faring poorly in a world that is increasingly dominated by human activity. The following chapters in this book capture much of the new information that has been generated and update it regarding earlier knowledge, resulting in overviews of marsupial evolution, diversification, biogeography, ecology, physiology, and conservation. This introductory chapter provides a brief overview of how the understanding of marsupial biology has been gained, with respect to the origin, radiation, specialization, and extinctions within this mammalian clade. Studies focusing on American and Australasian marsupial faunas are usually carried out separately by different teams of researchers. The Americas encompass the great marsupial radiation in South America and Central America, but with North America (north of Mexico onward) preponderantly including a single extant marsupial species, the Virginia Opossum Didelphis virginiana. Australasia is taken here operationally to encompass Australia, New Guinea, islands east to the Solomon Group and west to the Makassar and Lombok Straits where Wallace’s Line demarcates the westward limit of marsupial occurrence. Through these lines the reader will learn who were the key researchers and how they led fantastic discoveries about marsupials in different continents, particularly South America and Australia. Later, a brief introduction on the evolution and diversification of marsupials in the Americas and Australasia is provided.

A Brief History of Research on American Marsupials The first contact of Nilton Cáceres with marsupials began in the early 1990s, when he began a research project focusing on the dietary ecology of the Southern Blackeared Opossum Didelphis aurita in the Atlantic Forest in eastern Brazil. It is worth remembering that this endemic Atlantic Forest species was first recognized by science in 1826 with the description of Maximilian von Wied-Neuwied, a German naturalist, who collected samples in Bahia, eastern Brazil. In the recent past, it was considered to be the same opossum species occurring in the Amazon, D. marsupialis, a species described by Carl Linnaeus in 1758. Also interesting is

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that such opossums were the first marsupials seen by the European travelers that arrived in eastern South America at the end of the fifteenth century. In the 1990s, when the senior editor of this book started to study marsupials, knowledge of New World marsupials was incipient compared to the knowledge that exists now in the 2020s, for example, in taxonomy, systematics, and ecology. However, overall knowledge on the natural history and ecology of living marsupials had begun in the mid-twentieth century in the Americas with the first field studies carried out with the Virginia Opossum Didelphis virginiana in North America substantially since the 1940s (e.g., Lay 1942; Reynolds 1945; and several others), which is the sole marsupial species occurring in temperate North America today. Indeed, studies on reproductive biology of opossums in North America are as old as those from the 1920s, with some focusing on the breeding season and estrous cycle of the Virginia Opossum (e.g., Hartman 1928). However, such studies on the Virginia Opossum maybe encouraged the first studies in South America such as those by Davis (1944) in eastern Brazil, Tyndale-Biscoe and Mackenzie (1976) in Colombia, and Fleming (1973) in Panamá. Hence, Donald Hunsaker II published the book The Biology of Marsupials in 1977 which was a reference on marsupial biology in the Western Hemisphere. With the start of the 1980s, some important, pioneering studies on marsupial ecology and biogeography were carried out in South America, particularly in Brazil (Cerqueira 1985; Fonseca 1989). Some of these authors latterly became leaders in the ecology and biogeography of marsupials, guiding important marsupial specialists thereafter. Something similar occurred in French Guiana with the pioneering works led by Charles-Dominique et al. (1981) and then Atramentowicz (1986). Indeed, the 1980s saw the start of dedicated studies focusing on ecology and biogeography in South America, with other relevant research projects scattered across the continent, such as those of August (1981), Austad and Sunquist (1986), Cordero and Nicolas (1987), and O’Connell (1989) in Venezuela. At that time, opossums of the genus Didelphis were usually the focus of ecological (or other biological) studies (see Fig. 2 in ▶ Chap. 34, “Food Habits of American Marsupials”), because of its vast distribution and commonness in the Americas and being found also around cities and rural areas. However, some other genera were also used quite commonly in ecological studies carried out in the American tropics, such as Marmosa, Philander, and Caluromys, particularly in studies performed in French Guiana (e.g., see Atramentowicz 1986 and, later, Julien-Laferrière 1995) and eastern Brazil (see below). This can be extended for some Patagonian species (e.g., Thylamys pallidior; Albanese and Ojeda 2012) and for the Monito del Monte, Dromiciops, in the southern cone of South America (e.g., Amico and Aizen 2000), with mainly a Chilean distribution, being the unique living representative of the order Microbiotheria today. On the other hand, community studies have been carried out using square grids of traps, providing information for more than one species in each locality. This has been traditional in eastern Brazil where different specialists have been generated in postgraduate courses on zoology, ecology, or evolutionary biology, focusing their researches on small mammals including marsupials or solely

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on marsupials. Pioneering and interesting papers from these authors are, for example, Vieira (1997), Pires and Fernandez (1999), Vieira (1999), Costa (2003), and Pardini (2004). Since then, a growing body of studies has been produced, and more and more genera and species of marsupials have been studied in the Americas, from Chile and Argentina to Mexico and the USA, particularly using small trapping grids (usually 1 to 2 ha in size) because of the small average size of the American marsupials, but more rarely using radio-telemetry in larger species (e.g., Lira and Fernandez 2009 with Philander frenatus ¼ P. quica; Ryser 1995 with D. virginiana) and other methods like artificial nest boxes. However, the spool and line technique has been commonly used more recently (Prevedello and Vieira 2010) rather for species smaller than Didelphis (1 to 2.5 kg), which is the largest American marsupial living today. Despite the pioneering, punctual revisions like that of Tate (1933) on the Marmosa complex, comprehensive studies on New World marsupial systematics started in the early 1980s with researchers organizing New World species in new subfamilies, tribes, and genera and subgenera, while studies on taxonomy substantially increased the number of species around, or after, 2000 when new molecular techniques helped to discriminate morphologically cryptic species (e.g., Patton and Da Silva 1997; Voss et al. 2005). For example, from Honacki et al. (1982) to Astúa et al. (▶ Chap. 4, “Taxonomic Checklist of Living American Marsupials”), in a time interval of ~40 years, American marsupial diversity changed from 1 order, 15 genera, and 84 species to 3 orders, 22 genera, and 137 species. This effort resulted in comprehensive books such as Gardner (2007)’s Mammals of South America (first volume), which includes marsupials and some placental orders. However, older books were fundamental to the development of marsupial knowledge in South America such as that of Cabrera (1957). Over the last few decades, research areas have developed unevenly, with studies on marsupial ecology (or on small mammals that include marsupials) being more common with time than those with systematics and taxonomy, at least in Brazil (see above), but reflecting in some way the scientific tradition of each country. For example, Argentina and the United States of America apparently have developed further in the fields of systematics and taxonomy of marsupials rather than ecology. At least in Argentina, taxonomy and systematics are strongly related with paleontology (P. Teta, personal communication), something different to the situation in Brazil. The systematics and taxonomy of New World marsupials have attracted explosive attention in recent years (▶ Chap. 3, “Taxonomy and Diversity of Living American Marsupials”), mostly led by Robert Voss from the American Museum of Natural History in New York, who has elucidated the phylogenetic relationships of several marsupial taxa (Voss and Jansa 2009), has found new species for science, and has guided new marsupial taxonomists (e.g., Giarla et al. 2010; Pavan and Voss 2016). Furthermore, it is worth mentioning the early guidance of Elio Massoia, Francisco Goin, Ulyses Pardiñas (Argentina), Mario de Vivo (Brazil), and James Patton (USA) for generating the great team of marsupial taxonomists that exist today in the Americas.

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The extant marsupial fauna in the Americas is just the tip of an “iceberg” of a highly diversified marsupial fauna that existed in the past in South America, when the continent was isolated from the other land masses, the period of the so-called splendid isolation. While there are important fossil sites for marsupials and other metatherians, such as Tiupampa in Bolivia, Las Flores in Argentina, and Itaboraí in Brazil, there is a great team of specialists studying such fauna (see ▶ Chaps. 2, “Diversity and Phylogeny of Marsupials and Their Stem Relatives (Metatheria),” and ▶ 6, “Cenozoic Metatherian Evolution in the Americas” reviews in this book). While tropical South America has not proved favorable to find marsupial fossils (but an important exception is Itaboraí), temperate southern regions like those in Argentina have revealed a plethora of ancient marsupials, like the sabertooth marsupial Thylacosmilus atrox (Sparassodonta). In this regard, the paleontological work and guidance of Francisco Goin from the National University of La Plata, Argentina, have been outstanding in elucidating the diversity of the marsupial fauna from the past of South America and guiding excellent paleontologists and evolutionary biologists working on New World marsupials today. Amazingly, this resulted in the book A Brief History of South American Metatherians, in 2016, led by Francisco Goin with collaboration of Michael Woodburne, Ana Zimicz, Gabriel Martin, and Laura Chornogubsky. Furthermore, it is worth mentioning the fundamental roles of Florentino Ameghino, Ángel Cabrera, and Rosendo Pascual for developing the fine mammalian (metatherian) paleontological studies in South America. Today, a few countries, especially Argentina, Brazil, and the USA, lead research on New World marsupials, although other countries also have important roles such as Chile, Colombia, and Mexico. But this is not by chance because, besides encompassing a great diversity of both living and fossil marsupial faunas, they have public (and sometimes private) agencies that support researchers usually at scientific institutions. This is remarkable, for example, in Brazil where federal universities lead scientific research in the country, with important research centers even far from the Atlantic coast, as in Amazonia. The same happens in Argentina with its national scientific agency for research, contributing to the training and continued employment of high-standard researchers working in areas like taxonomy, biogeography, and paleontology of marsupials (and other metatherians). The study of marsupials was certainly improved with the fundamental roles of agencies created to give support for the study of mammals of the Americas, such as the American Society of Mammalogists (since 1919), the “Sociedad Argentina para el Estudio de los Mamíferos” (since 1982), the “Asociación Chilena de Mastozoología” (since 1982), the “Asociación Mexicana de Mastozoología” (since 1984), the “Sociedade Brasileira de Mastozoologia” (since 1985), and the “Sociedad Colombiana de Mastozoología” (since 2010). Although marsupials have to share space with several placental mammals in the Americas, special attention has been given to this mammalian fauna, which is reasonably diversified, with around 137 species today (▶ Chap. 4, “Taxonomic Checklist of Living American Marsupials”). The senior author of this chapter is glad to be part of the team studying marsupials, even with a small piece of the overall contribution when one realizes there is so much to find yet, but contemplating the beauty of what is known currently.

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Origin, Evolution, and Diversification of the New World Marsupials Metatherians, which include marsupials, originated in the northern hemisphere in the early Cretaceous (see ▶ Chap. 2, “Diversity and Phylogeny of Marsupials and Their Stem Relatives (Metatheria)”) and only later arrived in South America, by the time of late Cretaceous-early Paleocene, and in Australia, by the Paleocene-Eocene period (Case et al. 2005; Pascual 2006; Goin et al. 2016; Goin 2021). Their history is fantastic because North America, where they first diversified, is now a continent with few marsupial species, whereas the last continent they dispersed to (Australia) is where they show the highest extant diversity. This is because they had a northern origin with subsequent regional extinction (North America, Eurasia, and Africa), and their highest diversity was in the southern continents, namely, South America and Australia (Sánchez-Villagra 2013; Williamson et al. 2014; Goin et al. 2016; Goin 2021). Marsupial fossils dating from the Eocene have been found in Antarctica (Chornogubsky et al. 2009), from which these early forms dispersed to the Australian continent. Australasian marsupials were then able to evolve in isolation from placental mammals, and because of this they diversified substantially to occupy various available niches, from subterranean and arboreal life styles to large-sized herbivores (Black et al. 2012; Beck et al. 2008, 2020). In contrast, in South America, they also evolved during most of the Cenozoic period in isolation but in association with some placental clades such as the “condylarths” (primitive ungulates), Primates, Xenarthra, and caviomorph rodents (Sánchez-Villagra 2013; Goin et al. 2016). Coexisting with these placentals in South America, marsupials could evolve and diversify during the first half of the Cenozoic (Paleogene), generating different forms like insectivores, carnivores (sable marsupial cat), and frugivores, with variable body sizes (Zimicz 2012). This great diversification was possible due to the greenhouse effect during the Paleogene followed by a decrease in marsupial diversity during the Neogene which experienced an overall cooling event (Goin et al. 2016; Goin 2021). Besides such marsupial-placental coexistence, during the late Miocene and Pliocene, North and South America connected once again via the “Panamanian” Isthmus (Bacon et al. 2015), triggering the so-called Great American Biotic Interchange (GABI; Webb 2006). Hence, marsupials, formerly semi-isolated from most placentals, were broadly exposed to them in South America. This shock of faunas (marsupials vs. placentals) in South America may have led to extinctions of some marsupials, which are thought to be less competitive in regard to the allochthonous placentals. According to Sánchez-Villagra (2013), it was more a question of ecological opportunities for marsupials than something related to the inferiority of the clade. The great radiation of Sigmodontinae rodents in South America after the GABI (Maestri et al. 2017) suggests that there was some degree of past competition with ecologically similar species like the small sigmodontine rodents and didelphid marsupials, which are usually small in size (see Prevosti et al. 2011 for a different overview on carnivorous forms). Anyway, this hypothesis of overall competition between marsupials and placentals in the past of South America still needs to be

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tested (Sánchez-Villagra 2013). Another natural event that decreased the extant diversity of marsupials is the overall megafaunal extinction, which in part included marsupials, mainly in Australia. Large-sized species of mammals in both world regions became extinct, culminating in the body size distributions we see today (e.g., Prevosti et al. 2011; Beck et al. 2020). However, according to Goin (▶ Chap. 6, “Cenozoic Metatherian Evolution in the Americas”), marsupials were not affected by the megafaunal extinction in South America, but slightly larger forms than the extant Didelphis (up to ~3 kg) lived in the late Pliocene of Argentina such as the fossil didelphid Thylophorops lorenzinii, varying from 4.8 and 7.4 kg (Goin et al. 2009). Overall, both marsupial faunas were rather larger in size and potentially more diversified in the recent past, especially during the Pliocene and Pleistocene. Nonetheless, they are still diverse today, even the South American marsupial fauna which recolonized Central and North America during the GABI. In Australia, marsupials also dispersed to the north in recent times, to the more tropical island of New Guinea and the eastern (Asian) Indonesian islands, but lacking an isthmus like the one connecting the American continents.

A Brief History of Research on Australasian Marsupials Chris Dickman’s first encounter with a free-living marsupial occurred in the mid-1970s in a place far removed from both the Americas and Australasia: the Peak District in England. Here, a feral population of the Red-necked Wallaby Notamacropus rufogriseus had established several decades previously and was thriving despite severe winter conditions and potential competition from native placental mammals. The early to mid-1970s marked the beginning of an auspicious period for the formal study of marsupials, especially in Australia, and provides a convenient break point to consider knowledge of Australasian marsupials before and afterward.

Marsupial Studies Pre-1973 Evidence from archaeological sites indicates human presence in Australia for at least 60,000 years and in New Guinea and the broader region for perhaps just as long. Arriving from lands to the west of Wallace’s Line, the early colonists would have encountered environments that were dramatically unlike those with which they were familiar. The peaks of the Central Cordillera in New Guinea are high enough to support equatorial glaciers, while the low-lying and undulating topography of much of Australia houses a diverse, expansive arid region that is subject to extremes of climate. The native Australasian fauna also would have been quite unfamiliar to the first peoples, with gigantic elements – the megafauna – that included flightless birds, snakes, and lizards, as well as very large marsupials such as Diprotodon optatum, Palorchestes spp., and several genera of giant kangaroos. Although the megafaunas are now extinct, they are remembered by First Nations people in dreamtime stories and represented in rock art. With a land tenure exceeding 2000 generations, First

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Nations peoples in the Australasian region have acquired deep insight and knowledge of the marsupials and other biota that survive to the present day. Different species of marsupials are used as totems, as food, as indicators of changing seasons or of shifting environmental conditions; the pelts of some species are used for clothing or ceremonial purposes, and various tissues are deployed for a wide variety of other purposes such as to make tools, instruments, and weapons. In consequence of their utility and function and as integral parts of the world, marsupials are well known and respected by First Nations peoples in the Australasian region; local or regional losses of species, especially midsized and larger marsupials, are felt keenly by Indigenous communities. Although Indigenous knowledge has not always been appreciated by European colonists and explorers (e.g., Joyce and McCann 2011), the depth of this knowledge was recognized by naturalists and zoologists such as Gerard Krefft, Alice Duncan Kemp, Frederic Wood Jones, and Hedley Finlayson who engaged respectfully with Indigenous people. For example, in his classic book The Red Centre, Finlayson (1935) wrote about the “extraordinary intimacy” and “command of every relevant detail of its life-history and habits” that Aboriginal hunters display about marsupials and other prey animals. Partnerships between First Nations peoples and western scientists now commonly recognize the legitimacy of different approaches to knowing, and the linkage between Indigenous and western knowledge is forging extraordinarily deep understanding of the habits of some marsupial species (e.g., Newsome and Newsome 2016). Written accounts about marsupials first appeared in the early sixteenth century when exploration vessels began to move from Europe in search of new lands and resources. The first contact between European explorers and marsupials most likely occurred in 1500 when Spanish explorer Vicente Yáñez Pinzón captured several opossums in eastern Brazil and returned at least one animal to Spain to present to King Ferdinand and Queen Isabella. Shortly after, around 1540, António Galvão, Portuguese Governor of the Moluccas, documented the appearance and habits of a strange tree-dwelling animal that the local people called a “kusus” or “kuso.” As Galvão was stationed on the island of Ternate when his observations were made, he was almost certainly describing the Ternate and Tidore form of the Moluccan Cuscus Phalanger ornatus matabiru (¼ P. matabiru). European arrival and settlement expanded from the Moluccas and Micronesia progressively from the late sixteenth century, with scattered accounts of different cuscuses, kangaroos, quolls, and other species being made by mariners visiting the eastern Moluccan islands, New Guinea, and the north and west coast of Australia (Flannery 1995). However, it was not until the late eighteenth and early nineteenth centuries that marsupials began to be catalogued systematically. During this period large collections of marsupials from the broader Australasian region made their way back to the great science museums of England, France, Germany, the Netherlands, and, later, the USA to be inspected and described by the taxonomists and natural historians of the day (e.g., Lesson 1827; Waterhouse 1843). Following the voyages of James Cook to Australia between 1768 and 1771 and the arrival of settlers at Sydney Cove in 1788, local Australian marsupials were described and depicted in the journals of the newcomers, and both preserved

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marsupial specimens and living animals were sent to London for analysis and display. Within 30 years of settlement, 23 species of marsupials had been recognized and described, and French zoologist Henri de Blainville had shown that marsupials could be distinguished from all other mammals by the unique structure of their reproductive system (Dickman 2007). Descriptions of further marsupial species continued apace through the nineteenth century, with accounts for some species being accompanied by notes on their habits, distribution, diets, and reproduction. Among the most astute of the field naturalists at the time were John Gilbert, John Gould, and Gerard Krefft, whose works collectively increased understanding of marsupials and did much to sustain public interest in these mammals in Australia and Europe. Despite the fascination with marsupials in some quarters, in areas that had been usurped for sheep or cattle grazing, there was widespread dislike, even hatred, of marsupials. By the 1930s, for example, the Thylacine Thylacinus cynocephalus had been deliberately exterminated in Tasmania at the behest of sheep farmers and others before the animal could be properly studied; legislation intended to destroy marsupials was also in place in the eastern Australian mainland states of New South Wales and Queensland between 1877 and 1930, resulting in the killing of tens of millions of kangaroos, wallabies, wombats, bandicoots, and even the Koala Phascolarctos cinereus (Dickman 2007). Fortunately, the plight of marsupials in production landscapes was balanced by rising advocacy for their conservation in the general population, and this stimulated new research into the habitat and resource requirements of selected marsupial species and into previously unstudied aspects of their biology. For example, James Hill carried out a series of detailed anatomical, behavioral, endocrinological, and reproductive investigations on the Eastern Quoll Dasyurus viverrinus in the early years of the twentieth century (Hill 1910), while dedicated and supremely skilled naturalists such as David Fleay and Hedley Finlayson described the habits of marsupials by observing them in the field. These pioneering studies paved the way for later research on physiology, ecology, behavior, paleontology, and phylogenetic relationships in an increasingly wide range of marsupials. By the mid-twentieth century, new tools had been forged to allow deeper insights into marsupial biology within these discipline areas, with focal species including the Quokka Setonix brachyurus, Tammar Wallaby Notamacropus eugenii, Red Kangaroo Osphranter rufus, Long-nosed Bandicoots Perameles spp., Common Brushtail Possum Trichosurus vulpecula, and several species of dasyurid marsupials (Dickman 2005). The Australian Mammal Society was established in 1958 with its first object stating that it would seek “to promote the scientific study of the mammals of the Australasian region” (https://australianmammals.org.au/about_ us/overview, accessed 2 August 2022). The Society held meetings and conferences, published a bulletin that provided summaries of current research and lists of current literature, and began publication of its flagship journal Australian Mammalogy in December 1972. The burgeoning research interest in marsupials was captured in popular texts such as Ellis Troughton’s Furred Animals of Australia (1941), Basil Marlow’s Marsupials of Australia (1962), and David Ride’s A Guide to the Native

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Mammals of Australia (1970) and in international syntheses such as R. F. Ewer’s Ethology of Mammals (1968). However, an important landmark was achieved in 1973 with the publication of Life of Marsupials by Hugh Tyndale-Biscoe (1973). Although running to only 254 pages, this succinctly written book summarized and synthesized much of the research that had been carried out up to 1973 and provided a compelling refutation of the then-prevalent notion that marsupials were inferior to their distant placental relatives. Marsupials had come of age.

Marsupial Studies from 1973 In a new and comprehensively updated Life of Marsupials in 2005, Tyndale-Biscoe noted that, while it had been possible to cover the whole literature on marsupials in 1973, 32 years later this could no longer be accomplished. Indeed, post-1973, research on marsupials flourished. In 1977 two volumes entitled The Biology of Marsupials appeared. The first volume, edited by Bernard Stonehouse and Desmond Gilmore, focused largely on Australian marsupials but included a chapter by Alan Ziegler that reviewed knowledge of New Guinea’s marsupial fauna. The second volume, edited by Donald Hunsaker II, focused largely on New World marsupials and provided a synthesis that arguably helped to stimulate the expansion of marsupial research in Central and South America in recent decades, as noted above. In Australia, interest in marsupial studies was catalyzed by several factors. There was an increasing realization that marsupials provide excellent models for biomedical research (Tyndale-Biscoe and Janssens 1988) and could illuminate the mechanisms of control of mammalian growth because of the ease of access that pouch young provide for researchers (Tyndale-Biscoe and Renfree 1987). Extraordinary discoveries were being made, such as the synchronous post-mating death of all males in wild populations of Antechinus (▶ Chap. 30, “Reproductive Strategies and Biology of the Australasian Marsupials”), the ability of both small dasyurid and large macropodid marsupials to move long distances to track shifting resources in Australia’s central deserts (▶ Chap. 26, “Diversity and Endemism of the Marsupials of Australia’s Arid Zone”), and the spectacularly fossil-rich sites at Riversleigh and Naracoorte. New methods and new tools were also coming online in the 1970s, including Elliott traps and radio-tags that enabled live capture and tracking of small marsupials, probes and instruments that uncovered diverse aspects of marsupial endocrinology and physiology, and serological and electrophoretic techniques that enabled deeper insights to be gained into marsupial relationships. Cohorts of new masters and PhD students were also recruited, galvanizing studies in the field and at the lab bench. Two further factors helped to stimulate research interest in Australian marsupials during the 1970s. The first was an increasing awareness that many species were faring poorly in the face of profound habitat changes and other disturbances that had been introduced by the new settlers over the previous 200 years. This realization led to dedicated research on the habits, resource, and conservation requirements of many rare marsupials that previously had been poorly known, such as the Dibbler Parantechinus apicalis, Leadbeater’s Possum Gymnobelideus leadbeateri, and Parma Wallaby Notamacropus parma. The second key catalytic factor was the increasing activity of scientific societies, most notably the Australian Mammal Society (AMS)

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and the Royal Zoological Society of New South Wales (RZS). For example, attendances at annual conferences run by the former society swelled as postgraduate students sought opportunities to present their research and make connections, with encouragement provided also by society awards for high-quality work. The junior editor of this book attended his first AMS conference as a new PhD student in 1978. In 1980, following earlier symposia on kangaroos and monotremes, the RZS helped to support a 3-day symposium on carnivorous marsupials in Sydney. Organized by Michael Archer, the symposium was wildly successful and resulted in the publication of two volumes entitled Carnivorous Marsupials (Archer 1982). The venture succeeded in part because the symposium encouraged both students and established researchers to discuss research on a focal marsupial group and resulted in the presentation of major reviews, primary data studies, and valuable datasets that may have otherwise sat forever on researchers’ shelves. The two volumes of Carnivorous Marsupials were printed by a family business, Surrey Beatty & Sons, and published by the RZS, resulting in a product that was high quality but relatively cheap and thus accessible even to impoverished research students. Following Carnivorous Marsupials, many other volumes appeared that used the same model of holding a symposium on a focal marsupial group and publishing the contributions after review via an independent printer, with society support. Thus, Possums and Gliders appeared 2 years after Carnivorous Marsupials (Smith and Hume 1984), then Kangaroos, Wallabies and Rat-Kangaroos (Grigg et al. 1989), Bandicoots and Bilbies (Seebeck et al. 1990), as well as two volumes entitled Possums and Opossums, edited by the visionary and indefatigable Michael Archer in 1987. As the economic benefits of working with independent printers and publishers became apparent, a trickle of books on marsupials became a flood. Hesperian Press published Vertebrate Zoogeography and Evolution in Australasia (Archer and Clayton 1984), with seven chapters on marsupials, and university publishing houses also focused some attention on marsupials. For example, the University of Queensland Press published Spotlight on Possums (Russell 1980), and the New South Wales University Press began publishing volumes as part of its Australian Natural History Series under the editorship of Terry Dawson. The series covered both individual species such as the Koala (Lee and Martin 1988) and Mountain Pygmy-possum Burramys parvus (Mansergh and Broome 1994) and species groups such as kangaroos (Dawson 1995), possums (Kerle 2001), and tree-kangaroos (Martin 2005). In collaboration with the Australian Museum, other independent publishers helped to support the production of the first major syntheses of the mammals of New Guinea (Flannery 1990) and the south-west Pacific and Moluccan Islands (Flannery 1995). CSIRO Publishing now supports the production of journals such as Australian Mammalogy and Pacific Conservation Biology as well as many books on marsupials and related topic areas (e.g., Tyndale-Biscoe 2005; Baker and Dickman 2018), thus ensuring that excellent research findings continue to be made accessible and widely available. In the half century since Tyndale-Biscoe’s landmark Life of Marsupials, there has been an immense surge in research on the pouched mammals, initially in Australia and then in South America and to a lesser extent in New Guinea and the eastern Indonesian archipelago. The junior author of this chapter gained initial inspiration from Life of Marsupials soon after it was published in 1973 and has since been

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privileged to witness and perhaps even contribute in a small way to the improvement in understanding of marsupial biology and the current appreciation of these fascinating “alternative” mammals.

Origin, Evolution, and Diversification of Australasian Marsupials Despite their dominance in the modern mammalian fauna of Australasia, the Antipodes represent the last major continental area to be colonized by marsupials. After diverging from other early mammals in the northern hemisphere during the Jurassic (Luo et al. 2011), ancestral marsupials spread throughout much of Laurasia and arrived in what is now South America probably around the late Cretaceous-early Paleocene boundary (Goin 2021). Here, they flourished, with early forms moving south on terra firma into lands that now comprise west Antarctica before moving eastward across the Antarctic land bridge into Australia and arriving in the late Paleocene or very early Eocene (Pascual 2006). At this point, however, the narrative becomes more complicated as the identity of the marsupials that reached Australia remains shrouded in debate. Fossilized teeth, dentaries, and other fragmentary materials of early Eocene marsupials have been recovered from Seymour Island near the northern Antarctic Peninsula, but these belong to orders – Microbiotheria and Polydolopimorphia – whose members are, or were, endemic to southern South America and Antarctica (Gelfo et al. 2015). The earliest marsupial fossils in Australia come from deposits at Murgon in eastern Queensland and date to the Paleocene-Eocene boundary. Some of these show affinity with South American marsupials of similar age, but it is not clear whether these marsupials were progenitors of the Australian radiation or failed evolutionary lines. There is, however, some consensus that a small, enigmatic, and highly plesiomorphic marsupial, Djarthia murgonensis, may approximate the ancestral phenotype of the Australian marsupial radiation (Beck et al. 2008). Dating to the earliest Eocene, Djarthia suggests marsupial tenure in Australia for at least 55 million years. Australia severed its last land links with Antarctica during the middle to late Eocene some 38 million years ago, having received what may have been several waves of marsupial immigrants over the preceding 17+ million years. Unfortunately, understanding of marsupial radiation over this period is limited by a frustrating hiatus in the fossil record, with no useful deposits appearing anywhere in Australia until the late Oligocene. Even then, marsupial fossils remain relatively scant. By the Miocene, however, an explosive radiation of marsupials was underway, with species-rich and trophically diverse assemblages of herbivorous, omnivorous, and carnivorous marsupials represented. Geological evidence associated with rich fossil strata at sites such as Riversleigh and the Tirari Desert in South Australia shows that Australia entered a greenhouse period in the early Miocene, with the humid climate favoring the formation of lakes and rivers and a pan-continental expansion of rainforest. Then, as now, such conditions were conducive for marsupial life and for rapid radiation of new forms. Early dasyurids, thylacinids, notoryctids, and diprotodontians appeared for the first time, as well as

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representatives of families such as Ilariidae, Yaralidae, Miralinidae, Wynyardiidae, and Yalkaparidontidae that disappeared well before the Miocene epoch had concluded (Long et al. 2002). Losses of marsupial species, genera, and families from the mid-Miocene were almost certainly driven by a dramatic change in climate. Around 15 million years ago, the formerly lush greenhouse conditions of the early Miocene began to give way to cool, dry conditions that saw Australia – and much of the world – enter a prolonged icehouse phase. Arboreal marsupials and other forest-dependent species became increasingly scarce as the forests dwindled, although some persisted in local refuge areas in northeastern Australia and New Guinea where rainfall remained high. Unfortunately, the icehouse conditions arising in the mid-Miocene were not conducive to the preservation of organic material, and few productive sites for marsupial fossils have been discovered between 12 million and five million years ago. However, evidence from diverse sources indicates that, as the continental forests shrank, they were replaced by extensive grasslands, shrublands, and savanna woodlands, with these habitats providing conditions suitable for grazing animals such as kangaroos and wombats (Martin 2006). By the Pliocene (5.3–2.6 million years ago), such terrestrial grazers and browsers were becoming more abundant and more diverse in fossil deposits (Long et al. 2002). A further trend during this period was that surviving marsupials increased progressively in body mass. Large size would have been selectively advantageous to animals in minimizing loss of body heat and water during the prevailing cool and dry conditions and, for herbivores, would have allowed increased gut capacity for storage, processing, and digestion of low-quality grasses and other plant tissues. The trend toward gigantism reached its zenith in the Pleistocene (2.6 million–11,700 years ago). Until the arrival of people toward the end of this epoch in Australia, very large marsupials, flightless dromornithid birds, lizards, turtles, and snakes abounded (Rich et al. 1990). At least three dozen Australian marsupials weighed in at 50 kg or more, with two thirds of these achieving body weights of more than 100 kg. Several more giants occurred in New Guinea (Heinsohn and Hope 2006). Among the marsupials that comprised the so-called megafauna were diprotodontids that weighed up to 2800 kg, long-snouted palorchestids, shortfaced kangaroos, wombats, and marsupial “lions” Thylacoleo carnifex that averaged ~110 kg (Johnson 2006). Then, 45,000 years ago, these large beasts suddenly vanished. Considerable debate surrounds the cause of this extinction event, but the weight of evidence appears to favor a role for human hunting: as Johnson (2006) has argued, very large marsupials would have grown slowly to maturity and had slow rates of reproduction, so that light and even transient hunting pressure would have sufficed to put their populations on downward trajectories. Whatever the causes of the demise, Australia and New Guinea had lost their largest mammals, and up to 60 marsupials in total, by the end of the Pleistocene epoch. As the fortunes of marsupials waxed and waned in Australia, the lands that now form the island of New Guinea were becoming the new frontier for marsupial colonization. After Australia and the continental plate on which it sits sundered from Antarctica to begin a slow drift northward, the Australian plate collided with

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the Pacific plate in the early Oligocene around 30 million years ago. Although parts of New Guinea and other lands had existed as islands as long ago as the Jurassic, the collision of the Australian and Pacific continental plates resulted in massive uplift of what is now New Guinea, forming a continuous land connection with Australia (Flannery 1990, 1995). Subsequent changes in sea level saw the submersion of lower-lying areas at different times since the Oligocene, the most recent being the formation of Torres Strait around 15,000 years ago after the Last Glacial Maximum. For marsupials (and other biota), the emergence of land to Australia’s north meant opportunities for rafting or overland dispersal; the marsupial fauna outside Australia in the broader region is exclusively Australian in origin. The fossil record in New Guinea is poor and does not currently extend further back than the mid-Pliocene, but some inferences about the radiation of New Guinea’s marsupials can be made from studies of plate tectonics, morphological comparisons, and phylogenetic reconstructions (Long et al. 2002). Taken together, the evidence suggests that the first wave of marsupial immigrants into New Guinea took place in the early Miocene and represented the ancestors of present-day bandicoots and cuscuses (Aplin et al. 1993). Members of these two groups are now among the most widespread of marsupials throughout New Guinea and the furthest-flung outposts of the region, with distinctive and endemic taxa such as the Seram Bandicoot Rhynchomeles prattorum and the bear cuscuses Ailurops spp. of Sulawesi and nearby islands supporting the antiquity of this initial radiation. Subsequent dispersal events saw the ancestors of New Guinea’s forest-dwelling marsupials making the northward trek from Australia, including kangaroos, smaller diprotodontians, and dasyurids (e.g., Kerr and Prideaux 2022). The presence of the Chestnut Dunnart Sminthopsis archeri, Red-cheeked Dunnart S. virginiae, Northern Brown Bandicoot Isoodon macrourus, Red-legged Pademelon Thylogale stigmatica, and Agile Wallaby Notamacropus agilis in New Guinea probably reflect dispersal events from Australia during Pleistocene glacial maxima, whereas New Guinean marsupials that made the reverse journey back to Australia include the Long-nosed Echymipera Echymipera rufescens, Southern Common Cuscus Phalanger mimicus, and the Australian Spotted Cuscus Spilocuscus nudicaudatus. The former five species occupy similar lowland savanna and grassland habitats in New Guinea to those that are preferred in their more extensive ranges in Australia, whereas the latter three species are confined in Australia to rainforest and adjacent habitats on Cape York Peninsula. The late Pleistocene extinction events depleted the marsupial fauna of both Australia and New Guinea, and further extinctions have followed. For example, the Thylacine disappeared from mainland Australia and New Guinea following the introduction of dogs Canis spp. in the late Holocene and was eradicated from its last stronghold in Tasmania in the first half of the twentieth century. Range reductions and extinctions have escalated sharply within the last 200 years due to pervasive changes to habitats and other environmental disturbances and that have been wrought by European settlers, largely in Australia. Nonetheless, the modern-day marsupial fauna remains astonishingly diverse. Indeed, in 1959 the celebrated Australian mammalogist Ellis Troughton stated memorably that “... Australia [had]

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fostered the greatest phylogenetic deployment of a single mammalian Order that the World can ever know” (Troughton 1959).

Cross-References ▶ Diversity and Phylogeny of Marsupials and Their Stem Relatives (Metatheria) ▶ Taxonomic Checklist of Living American Marsupials ▶ Taxonomy and Diversity of Living American Marsupials ▶ Taxonomy and Diversity of Living Australasian Marsupials Acknowledgments Nilton Cáceres was supported by a fellowship from the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq) in Brazil. Chris Dickman’s work over many years has been supported by grants and fellowships from the Australian Research Council.

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Part II Evolution and Diversification

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Diversity and Phylogeny of Marsupials and Their Stem Relatives (Metatheria) Robin M. D. Beck

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Phylogenetic Definitions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Earliest Metatherians and the Timing of the Metatheria-Eutheria Split . . . . . . . . . . . . . . . . . . . . Deltatheroida . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Late Cretaceous Marsupialiforms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cenozoic Laurasian Marsupialiforms . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Earliest Southern Hemisphere Marsupialiforms and the Age of Marsupialia . . . . . . . . . . . . . . . . . . . Sparassodonta . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Polydolopimorphia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Paucituberculata . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Didelphimorphia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Australidelphia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Microbiotheria . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Diprotodontia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dasyuromorphia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Notoryctemorphia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Peramelemorphia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Yalkaparidontia . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Summary and Prospectus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cross-References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

The diversity and phylogeny of marsupials and their stem relatives (collectively, Metatheria) are reviewed, from their divergence from their sister taxon (Eutheria) and the earliest fossil record of metatherians, to the relationships between and within the seven extant marsupial orders. An up-to-date list of published phylogenetic definitions relevant to the clade is also provided. Molecular data appears R. M. D. Beck (*) School of Science, Engineering and Environment, University of Salford, Salford, UK e-mail: [email protected] © Springer Nature Switzerland AG 2023 N. C. Cáceres, C. R. Dickman (eds.), American and Australasian Marsupials, https://doi.org/10.1007/978-3-031-08419-5_35

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to have resolved most higher-level (subfamily and above) relationships within Marsupialia, with the notable exceptions of the position of the marsupial root, the branching pattern among the four modern subfamilies of Didelphidae (opossums), and the relationships between the modern families of Peramelemorphia (bandicoots and bilbies). However, recent molecular clock estimates for the age of the Metatheria-Eutheria divergence and the first diversification within Marsupialia vary considerably, and robust estimates will probably require a well-sampled fossil record that convincingly brackets these divergences. Relationships among fossil metatherians are much less clear, with numerous areas of uncertainty and disagreement, including the relationships between Cretaceous and Cenozoic taxa, and the composition and relationships of several groups that are of broad biogeographical and macroevolutionary significance, such as the families Peradectidae and Herpetotheriidae and the order Polydolopimorphia. Resolution of these issues will (unsurprisingly) require much better sampling of the fossil record and improved methods of phylogenetic analysis, but there may be limitations on the ability of morphological data (even when analyzed in combination with molecular data) to robustly resolve some parts of metatherian phylogeny, particularly given the heavy reliance on characters of the dentition. Keywords

Deltatheroida · Marsupialiformes · Sparassodonta · Polydolopimorphia · Peradectidae · Herpetotheriidae · Didelphimorphia · Paucituberculata · Australidelphia · Diprotodontia · Yalkaparidontia

Introduction Marsupialia is the crown clade of the total clade Metatheria, which is sister to Eutheria (Table 1). Over 400 extant or recently extinct marsupial species have been described (Beck et al. 2022: Table 1), each of which can be referred to 1 of 7 orders: Didelphimorphia (the “true” opossums), Paucituberculata (the “shrew” or “rat” opossums), Microbiotheria (the “monito del monte”), Dasyuromorphia (Australian faunivorous marsupials such as quolls, dunnart, the Tasmanian devil, the thylacine, and the numbat), Diprotodontia (wombats, koalas, macropods, “possums”), Notoryctemorphia (marsupial moles), and Peramelemorphia (bandicoots and bilbies). Modern paucituberculatans (3 genera and 7 described species in the family Caenolestidae; Beck et al. 2022: table 1) and microbiotherians (a single genus, Dromiciops, and 2 or 3 species, in the family Microbiotheriidae; Quintero-Galvis et al. 2022; ▶ Chap. 4, “Taxonomic Checklist of Living American Marsupials”) are entirely South American. Modern didelphimorphians (18 genera and >120 species in the family Didelphidae) are likewise predominantly South American, although some species occur in Central America and on adjacent islands, and a single species (Didelphis virginiana) is found in North America north of Mexico (Beck et al. 2022:

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Table 1 Summary of formal phylogenetic definitions of clades relevant to this review

Clade Theria

Definition “The least inclusive clade containing Mus musculus and Didelphis marsupialis”

Eutheria

“The most inclusive clade containing Mus musculus but not Didelphis marsupialis”

Placentalia

“The least inclusive clade containing Dasypus novemcinctus, Elephas maximus, Erinaceus europaeus and Mus musculus” “The most inclusive clade containing Didelphis marsupialis but not Mus musculus”

Metatheria

Marsupialiformes

Glasbiidae Herpetotheriidae

Peradectidae

Pediomyidae

Stagodontidae

Node-, stem-, or apomorphybased Reference(s) Node Sereno (2006: table 10.1; see also O’Leary et al. 2013: table S4) Stem Sereno (2006: table 10.1; see also O’Leary et al. 2013: table S4) Node Sereno (2006: table 10.1; see also O’Leary et al. 2013: table S4) Stem

“The most inclusive clade containing Didelphis marsupialis but not Deltatheridium pretrituberculare” “Glasbius spp.”

Stem

“The most inclusive clade containing Herpetotherium fugax but not Peradectes elegans Pediomys elegans, Didelphodon vorax or Didelphis virginiana” “The most inclusive clade containing Peradectes elegans but not Herpetotherium fugax, Pediomys elegans or Didelphis virginiana” “The most inclusive clade containing Pediomys elegans, but not Peradectes elegans, Herpetotherium fugax, Didelphis virginiana or Didelphodon vorax” “The most inclusive clade containing Didelphodon vorax but not Glasbius intricatus, Dakotadens morrowi, Turgidodon praesagus, Herpetotherium fugax,

Stem

Node

Sereno (2006: table 10.1; see also O’Leary et al. 2013: table S4) Beck (2017a: table 13.1)

Williamson et al. (2014: 18) Williamson et al. (2012: 629)

Stem

Williamson et al. (2012: 629)

Stem

Williamson et al. (2012: 629)

Stem

Williamson et al. (2012: 629)

(continued)

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R. M. D. Beck

Table 1 (continued)

Clade

Pucadelphyda

Proborhyaenidae

Thylacosmilinae

Marsupialia

Didelphimorphia

Australidelphia

Crown-clade Australidelphia

Eomarsupialia

Definition Peradectes elegans, Pediomys elegans or Didelphis virginiana” “The least inclusive clade containing Pucadelphys and Borhyaena” “All sparassodonts more closely related to Proborhyaena gigantea than to Borhyaena tuberata, Prothylacynus patagonicus, Lycopsis torresi, Cladosictis patagonica, or Sipalocyon gracilis” “All sparassodonts more closely related to Thylacosmilus atrox than to Proborhyaena gigantea, Borhyaena tuberata, Prothylacynus patagonicus, Lycopsis torresi, Cladosictis patagonica, or Sipalocyon gracilis” “The least inclusive clade containing Didelphis marsupialis, Caenolestes fuliginosus and Phalanger orientalis” “The most inclusive clade containing Didelphis marsupialis, but not Caenolestes fuliginosus or Phalanger orientalis” “The most inclusive clade exhibiting a ‘continuous lower ankle joint pattern’ (CLAJP; i.e. confluent ectal and sustentacular facets) and a triplefaceted, or ‘tripartite’, calcaneocuboid (CaCu) joint synapomorphic with that in Dromiciops” “The least inclusive clade containing Dromiciops gliroides, Phalanger orientalis, Perameles nasuta, Notoryctes typhlops and Dasyurus maculatus” “The least inclusive clade containing Phalanger orientalis, Perameles nasuta, Notoryctes

Node-, stem-, or apomorphybased Reference(s)

Node

Muizon et al. (2018: 419)

Stem

Engelman et al. (2020: 7)

Stem

Engelman et al. (2020b: 7–8)

Node

Beck et al. (2014: 131)

Stem

Beck and Taglioretti (2020: 391)

Apomorphy Beck (2012: 717)

Node

Beck (2017a: table 13.1)

Node

Beck et al. (2014: 132) (continued)

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Table 1 (continued)

Clade

Agreodontia

Dasyuromorphia

Dasyuroidea

Dasyuridae

Myrmecobiidae

Thylacinidae

Dasyurinae

Sminthopsinae

Dasyurini

Phascogalini

Definition typhlops and Dasyurus maculatus” “The most inclusive clade containing Perameles nasuta, Notoryctes typhlops and Dasyurus maculatus but not Phalanger orientalis” “The most inclusive clade including Dasyurus viverrinus, but excluding Perameles nasuta, Notoryctes typhlops, Phalanger orientalis and Dromiciops gliroides” “The least inclusive clade including Dasyurus viverrinus, Myrmecobius fasciatus and Thylacinus cynocephalus” “The most inclusive clade including Dasyurus viverrinus, but excluding Myrmecobius fasciatus and Thylacinus cynocephalus” “The most inclusive clade including Myrmecobius fasciatus, but excluding Dasyurus viverrinus and Thylacinus cynocephalus” “The most inclusive clade including Thylacinus cynocephalus, but excluding Dasyurus viverrinus and Myrmecobius fasciatus” “The most inclusive clade including Dasyurus viverrinus, but excluding Sminthopsis crassicaudata” “The most inclusive clade including Sminthopsis crassicaudata, but excluding Dasyurus viverrinus” “The most inclusive clade including Dasyurus viverrinus, but excluding Phascogale tapoatafa” “The most inclusive clade including Phascogale tapoatafa,

Node-, stem-, or apomorphybased Reference(s)

Stem

Beck et al. (2014: 132)

Stem

Kealy and Beck (2017: table 1)

Node

Kealy and Beck (2017: table 1)

Stem

Kealy and Beck (2017: table 1)

Stem

Kealy and Beck (2017: table 1)

Stem

Kealy and Beck (2017: table 1)

Stem

Kealy and Beck (2017: table 1)

Stem

Kealy and Beck (2017: table 1)

Stem

Kealy and Beck (2017: table 1)

Stem

Kealy and Beck (2017: table 1) (continued)

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R. M. D. Beck

Table 1 (continued)

Clade

Planigalini

Sminthopsini

Diprotodontia

Vombatiformes

Vombatomorphia

Phascolarctomorphia

Vombatoidea

Diprotodontoidea

Macropodiformes

Balbaridae

Definition but excluding Dasyurus viverrinus” “The most inclusive clade including Planigale ingrami, but excluding Sminthopsis crassicaudata” “The most inclusive clade including Sminthopsis crassicaudata, but excluding Planigale ingrami” The most inclusive clade including Phalanger orientalis but not Dasyurus viverrinus, Dromiciops gliroides, Notoryctes typhlops or Perameles nasuta “The most inclusive clade including Vombatus ursinus but not Phalanger orientalis” “The most inclusive clade including Vombatus ursinus but not Phascolarctos cinereus” “The most inclusive clade including Phascolarctos cinereus but not Vombatus ursinus” “The most inclusive clade including Vombatus ursinus but not Diprotodon optatum, Phascolarctos cinereus or Thylacoleo carnifex” “The most inclusive clade including Diprotodon optatum, but not Phascolarctos cinereus, Thylacoleo carnifex or Vombatus ursinus” “The most inclusive clade including Balbaroo nalima, Hypsiprymnodon moschatus, Potorous tridactylus and Macropus giganteus, but excluding Cercartetus concinnus and Phalanger orientalis” “The most inclusive clade including Balbaroo nalima, but excluding Hypsiprymnodon moschatus, Potorous tridactylus and Macropus giganteus”

Node-, stem-, or apomorphybased Reference(s)

Stem

Kealy and Beck (2017: table 1)

Stem

Kealy and Beck (2017: table 1)

Stem

Beck et al. (2020: table 1)

Stem

Beck et al. (2020: table 1)

Stem

Beck et al. (2020: table 1)

Stem

Beck et al. (2020: table 1)

Stem

Beck et al. (2020: table 1)

Stem

Beck et al. (2020: table 1)

Stem

Westerman et al. (2022: table 1)

Stem

Westerman et al. (2022: table 1)

(continued)

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Table 1 (continued)

Clade Macropodoidea

Definition “The least inclusive clade including Hypsiprymnodon moschatus, Potorous tridactylus and Macropus giganteus” Hypsiprymnodontidae “The most inclusive clade including Hypsiprymnodon moschatus and Propleopus oscillans, but excluding Balbaroo nalima, Potorous tridactylus and Macropus giganteus” Hypsiprymnodontinae “The most inclusive clade including Hypsiprymnodon moschatus, but excluding Propleopus oscillans” Propleopinae “The most inclusive clade including Propleopus oscillans, but excluding Hypsiprymnodon moschatus” Macropodia “The least inclusive clade including Potorous tridactylus and Macropus giganteus, but excluding Hypsiprymnodon moschatus” Potoroidae “The least inclusive clade including Potorous tridactylus and Aepyprymnus rufescens, but excluding Hypsiprymnodon moschatus and Macropus giganteus” Potorinae “The least inclusive clade including Potorous tridactylus, but excluding Aepyprymnus rufescens” Bettonginae “The least inclusive clade including Aepyprymnus rufescens, but excluding Potorous tridactylus” Macropodidae “The most inclusive clade including Simosthenurus occidentalis, Lagostrophus fasciatus and Macropus giganteus, but excluding Potorous tridactylus and Hypsiprymnodon moschatus”

Node-, stem-, or apomorphybased Reference(s) Node Westerman et al. (2022: table 1)

Stem

Westerman et al. (2022: table 1)

Stem

Westerman et al. (2022: table 1)

Stem

Westerman et al. (2022: table 1)

Node

Westerman et al. (2022: table 1)

Node

Westerman et al. (2022: table 1)

Node

Westerman et al. (2022: table 1)

Node

Westerman et al. (2022: table 1)

Stem

Westerman et al. (2022: table 1)

(continued)

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R. M. D. Beck

Table 1 (continued)

Clade Sthenurinae

Lagostrophinae

Macropodinae

Dorcopsini

Dendrolagini

Macropodini

Definition “The most inclusive clade including Simosthenurus occidentalis, but excluding Lagostrophus fasciatus and Macropus giganteus” “The most inclusive clade including Lagostrophus fasciatus, but excluding Simosthenurus occidentalis and Macropus giganteus” “The most inclusive clade including Macropus giganteus, but excluding Simosthenurus occidentalis and Lagostrophus fasciatus” “The least inclusive clade including Dorcopsis hageni, but excluding Dendrolagus lumholtzi and Macropus giganteus” “The least inclusive clade including Dendrolagus lumholtzi, but excluding Dorcopsis hageni and Macropus giganteus” “The least inclusive clade including Macropus giganteus, but excluding Dorcopsis hageni and Dendrolagus lumholtzi”

Node-, stem-, or apomorphybased Reference(s) Stem Westerman et al. (2022: table 1)

Stem

Westerman et al. (2022: table 1)

Stem

Westerman et al. (2022: table 1)

Node

Westerman et al. (2022: table 1)

Node

Westerman et al. (2022: table 1)

Node

Westerman et al. (2022: table 1)

Table 1). The remaining 4 orders – Dasyuromorphia (21 genera and >70 species in 3 families), Diprotodontia (42 genera and >150 species in 11 families), Notoryctemorphia (1 genus and 2 species in the family Notoryctidae), and Peramelemorphia (8 genera and 30 species in 3 or 4 families, depending on the assumed classification; Travouillon and Phillips 2018; Beck et al. 2022) – are collectively known from Australia, New Guinea, and surrounding islands (Beck et al. 2022: table 1). Continuing advances in phylogenetics, particularly the increasing availability of large amounts of genomic data, mean that higher-level relationships among Recent marsupials are now well understood, with relatively few areas of uncertainty remaining (Duchêne et al. 2018; Eldridge et al. 2019; Beck et al. 2022; Beck in press). By contrast, our knowledge of the phylogeny of fossil marsupials and non-marsupial metatherians is far from adequate, despite ongoing efforts by numerous researchers (see recent reviews by Eldridge et al. 2019; Beck et al. 2022; Beck in press). Fossil metatherians are known from all 7 continents, with well over 300 genera described to date (Bennett et al. 2018; Eldridge et al. 2019). However, the

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metatherian fossil record is undoubtedly highly incomplete and unevenly sampled, with most taxa known from dental remains only, and with certain time periods and biogeographical regions particularly poorly represented (Bennett et al. 2018). For example, there is only a single fossil site in Australia older than ~25 million years that preserves metatherians: the early Eocene Tingamarra local fauna of southeastern Queensland (Beck et al. 2008b; Bennett et al. 2018). The entire fossil record of Antarctic metatherians, meanwhile, comprises 8 named genera from the middle Eocene La Meseta Formation of Seymour Island (Goin et al. 2020: table 3). However, Antarctica undoubtedly played a key (but still largely unknown) role in the evolutionary history of Metatheria, not only as the route by which marsupials (and potentially non-marsupial metatherians) reached Australia via South America (Goin et al. 2016; Beck 2017a) but also presumably (given its enormous size, twice that of the Australian continent) as a center of metatherian diversification, prior to the development of a permanent icecap. This chapter therefore represents a summary of “work in progress,” and it is likely that there will be major revisions to our understanding of the relationships of many fossil metatherian groups in particular. Inevitably, this chapter is also a somewhat subjective, personal view of the topic: in several areas where there is currently disagreement between studies, an indication is given as to what the author of this chapter considers to be the most likely interpretation and why. However, such controversies will only be confidently resolved by new fossil discoveries, new sources of data, improved analyses, or (more likely) a combination of these. Given the many current uncertainties regarding metatherian phylogeny, applying a consistent, strictly taxonomic organization to this chapter would be difficult, if not impossible. This chapter is therefore partly structured by classification and partly by geographical location and time period.

Phylogenetic Definitions An increasing number of metatherian clades now have formal phylogenetic definitions. These definitions are shown in Table 1 and will be followed here.

The Earliest Metatherians and the Timing of the MetatheriaEutheria Split Eutheria and Metatheria together comprise the clade Theria (Table 1). The earliest definitive eutherians and metatherians have fully tribosphenic molar dentitions (Kielan-Jaworowska et al. 2004; Davis et al. 2008; Davis and Cifelli 2011; Cifelli and Davis 2015; Bi et al. 2018), and their common ancestor was presumably also tribosphenic. There seem to be relatively few features of individual molars that clearly differentiate the earliest metatherians from eutherians and tribosphenic stemtherians (Kielan-Jaworowska et al. 2004; Davis and Cifelli 2011; Averianov 2015; Cifelli and Davis 2015). Tribosphenic taxa that cannot be confidently assigned to either Metatheria or Eutheria are sometimes informally grouped together as

32

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“tribotheres” or “therians of metatherian-eutherian grade” (Cifelli 1993; KielanJaworowska et al. 2004). Older studies identified the presence of stylar cusp C in the upper molars as a synapomorphy of Metatheria, and suggested that Holoclemensia texana from the Aptian-Albian (~110 Ma old) Trinity Group of Texas and Oklahoma is an early metatherian based on the presence of this feature (see Aplin and Archer 1987 and references cited therein). However, more recent work has concluded that the earliest metatherians were similar to eutherians in lacking stylar cusp C (Davis and Cifelli 2011; Averianov 2015). Instead, Davis and Cifelli (2011) suggested that Holoclemensia is more likely to be a eutherian (see also Cifelli and Davis 2015), while Averianov (2015) concluded that it was a stem-therian. Both Davis and Cifelli (2011) and Averianov (2015) inferred the presence of only 3 molars and probably also 5 premolars in Holoclemensia, in contrast to the 3 premolars and 4 molars characteristic of definitive metatherians (see below). Several recent phylogenetic analyses have placed Holoclemensia within Metatheria (Fig. 2; Ni et al. 2016; Wang et al. 2021), congruent with earlier studies. However, others have supported eutherian (e.g., Averianov et al. 2010; Rangel et al. 2019) or stem-therian (Fig. 6; Engelman et al. 2020b) affinities, and still others have found its position relative to Theria to be unresolved (Cohen 2017). Potentially more useful in identifying early metatherians is the postcanine dental formula. Stem-therians have 5 premolars and 3 molars, and this dental formula is retained by the earliest eutherians (Kielan-Jaworowska et al. 2004; O’Leary et al. 2013; Bi et al. 2018). By contrast, definitive metatherians are characterized by 3 premolars and 4 molars (Kielan-Jaworowska et al. 2004; O’Leary et al. 2013; Beck et al. 2022). This derived condition has been proposed to have arisen by suppression of 1 premolar locus (P1/p1 according to Averianov et al. 2010; but P3/p3 according to O’Leary et al. 2013) and non-replacement of the last deciduous premolar (dP5/dp5); if this is correct, then the “M1/m1” of metatherians is homologous with dP5/dp5 of stem-therians and eutherians, and the remaining molars (“M/m2-4”) of metatherians in fact represent M1-3/m1-3 (Fig. 1; Averianov et al. 2010; O’Leary et al. 2013; Williamson et al. 2014). Particularly interesting in this regard is Kielantherium gobiense from the Early Cretaceous Höövör locality of Mongolia: this taxon is fully tribosphenic and, based on evidence from partial mandibles, has a postcanine formula of 4 molars and at least 4 premolars (Lopatin and Averianov 2007). It is therefore tempting to interpret Kielantherium as an early metatherian that has already evolved non-replacement of dP5/dp5 (“M1/m1”), but has not yet lost a more anterior premolar, a possibility acknowledged by several authors (e.g., Averianov et al. 2010: 323; Davis and Cifelli 2011). However, although fully tribosphenic, the molars of Kielantherium are highly plesiomorphic compared to definitive therians, with a very small protocone and a small talonid with only 2 cuspids (the entoconid is absent), and it may instead fall outside Theria (Lopatin and Averianov 2007; Davis 2011; Davis and Cifelli 2011). Most recent published phylogenetic analyses have supported this latter interpretation (Fig. 2; Ni et al. 2016; Cohen 2017; Bi et al. 2018; Wang et al. 2021), although a tipdating analysis by King and Beck (2020: fig. 2) placed Kielantherium þ Aegialodon in an unresolved trichotomy with Metatheria and Eutheria.

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Fig. 1 Homologies of adult postcanine dental formulae in Eutheria (including the crown clade, Placentalia) and Metatheria (including the crown clade, Marsupialia) proposed by O’Leary et al. (2013). (Reproduced from Williamson et al. (2014: fig. 4) under a Creative Commons Attribution License (CC BY 4.0))

Davis and Cifelli (2011) concluded that another taxon from the Trinity Group, Pappotherium pattersoni, has 4 molars and so may be a metatherian, although its premolar count is uncertain. However, Averianov (2015) argued that Pappotherium does not show the derived metatherian pattern of dental replacement (see below) and is a stem-therian. In support of Davis and Cifelli’s (2011) conclusion, a number of recent published phylogenetic analyses have recovered Pappotherium as a metatherian, specifically a deltatheroidan (Fig. 2; Ni et al. 2016; Wilson et al. 2016; see section “Deltatheroida” below). The oldest definitive evidence of the characteristic metatherian dental formula of 3 premolars and 4 molars, however, is slightly younger than the Trinity Group fossils, namely, an associated pair of partial, largely edentulous dentaries (OMNH 33458) from the Early Cretaceous (Albian; ~104–109 Ma) Cloverly Formation of Montana (Cifelli and Davis 2015). There are several additional craniodental features that represent plausible metatherian apomorphies (Rougier et al. 1998; O’Leary et al. 2013: supplementary materials; Williamson et al. 2014). These include (1) “staggering” of the numerical second lower incisor; (2) a modified pattern of dental replacement in which only the ultimate premolar has 2 fully erupted generations of teeth; (3) presence of a medially inflected angular process; (4) loss of the stapedial artery system, as indicated by a lack of grooves on the promontorium of the petrosal; and (5) transformation of the prootic canal from a large, vertical canal to one that is much smaller and runs horizontally. Postcranial apomorphies that might characterize metatherians are more equivocal. Features of the carpus and tarsus of the Early Cretaceous Sinodelphys szalayi that were proposed as metatherian synapomorphies by Luo et al. (2003) now appear doubtful given that Sinodelphys has been reinterpreted as a eutherian (Bi et al. 2018; but see Celik and Phillips 2020). With Sinodelphys discounted, Asiatherium reshetovi from the Late Cretaceous of Mongolia is the only

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R. M. D. Beck

Fig. 2 Phylogeny of Metatheria (focused on deltatheroidans) based on 156 dental and cranial characters (50% majority rule consensus of 97 most parsimonious trees; numbers at nodes represent the consensus percentage). Red branches are reconstructed as having an origin in Asia, blue

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Mesozoic metatherian known from an associated postcranial skeleton (Szalay and Trofimov 1996; Williamson et al. 2014), but isolated postcranial specimens attributed to metatherians are known from several Cretaceous sites in North America and Asia (Szalay 1994; Horovitz 2000; Szalay and Sargis 2006; Chester et al. 2010, 2012; Williamson et al. 2014; DeBey and Wilson 2017). These postcranial remains can be distinguished from those of eutherians based on a number of features, but the polarities of many of these differences remain unclear (Szalay 1994; Szalay and Trofimov 1996; Horovitz 2000; Szalay and Sargis 2006). The timing of the divergence between Metatheria and Eutheria remains poorly constrained (see Table 2), in part due to controversy regarding the ages and affinities of some key taxa. The oldest generally accepted metatherians described to date are early deltatheroidans (see section “Deltatheroida” below), dating to ~110 Ma (Davis et al. 2008; Davis and Cifelli 2011). However, well-preserved definitive eutherians from the Yixian Formation are considerably older, dating to ~125 Ma (Bi et al. 2018), and thus provide a conservative minimum bound on the Metatheria-Eutheria divergence. Durlstotherium and Durlstodon are two enigmatic tribosphenic taxa, each represented by a single upper molar from the earliest Cretaceous (Berriasian; ~145 Ma old) Purbeck Group of Great Britain, that have been referred to Eutheria based on their resemblance to much younger (Late Cretaceous) eutherians (Sweetman et al. 2017); if Durlstotherium and Durlstodon are indeed eutherian, then this would push the minimum age of the Metatheria-Eutheria divergence back by ~20 Ma (but see Bi et al. 2018; Marjanović 2021: supplementary material). Still older is Juramaia sinensis from the Late Jurassic (Oxfordian, ~160 Ma) Daxishan locality (or Daxigou locality) of northeastern China (Luo et al. 2011; Chu et al. 2016; Xu et al. 2016), which has been found to be a eutherian in most published phylogenetic analyses (e.g., Luo et al. 2011; Bi et al. 2018; King and Beck 2020; Wang et al. 2021), although with some exceptions (e.g., Celik and Phillips 2020). The reported age and provenance of Juramaia have been questioned (e.g., Bi et al. 2018; Marjanović 2021: supplementary material), but this has been based on somewhat circular reasoning, namely, that the known morphology of Juramaia (particularly its molar dentition, which is little different from the Yixian eutherians) is “too advanced” for it to be Jurassic (see also King and Beck 2020). Direct evidence that Juramaia is from a different, younger locality than that reported does not appear to have been presented. Thus, on fossil evidence, the Metatheria-Eutheria split is undoubtedly older than 125 Ma (based on the Yixian eutherians) and may be 160 Ma or more (based on Juramaia). Molecular clock analyses require calibration (typically using fossil evidence) of one or more nodes to calculate absolute divergence times (Nguyen and Ho 2020). Thus, molecular clock estimates for the divergence between metatherians and eutherians will be strongly influenced by whether a minimum bound of (for example) 125 Ma (based on the Yixian eutherians), 145 Ma (based on ä Fig. 2 (continued) branches in North America, and green branches are ambiguous. (Reproduced from Ni et al. (2016: fig. 4) under a Creative Commons Attribution 4.0 International License)

Feng et al. (2022)

Tip-andnode dating Node dating

Nuclear and mitochondrial sequences and craniodental characters Nuclear sequences

Nuclear and mitochondrial sequences

Nuclear sequences

Node dating Node dating Node dating Node dating

Nuclear and mitochondrial sequences Nuclear sequences

Mitchell et al. (2014) Tarver et al. (2016) Duchêne et al. (2018) ÁlvarezCarretero et al. (2021) Beck et al. (2022)

Method Node dating

Data Nuclear sequences

Study Meredith et al. (2011)

Autocorrelated

Independent gamma rates

Independent log-normal rates Autocorrelated

Clock model(s) Autocorrelated and independent log-normal rates Independent log-normal rates Autocorrelated

MCMCTree

MrBayes

MCMCTree

N/A

N/A

141.8 (123.3–166.2)

N/A

163.9 (156.7–169.8)

MCMCTree MCMCTree

N/A

MCMCTree

Software MCMCTree

Estimated age of first divergence within Theria 190.0 (167.2–215.3)

84.5

56.2 (54.7–58.6)

53.7 (49.3–58.9)

78.6 (70.5–86.1)

78.3 (49.1–104.3)

87.0 (79.5–94.9)

Estimated age of first divergence within Marsupialia 81.8 (67.9–97.2)

Table 2 Recent divergence time estimates for the first diversification within Theria and Marsupialia using molecular clock node-dating and total evidence tipand-node dating. Dates in brackets represent 95% confidence/credibility intervals (where available)

36 R. M. D. Beck

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Durlstotherium and Durlstodon), or 160 Ma (based on Juramaia) is used. Published molecular clock estimates for this divergence (see Table 2) – which include 167–215 Ma (Meredith et al. 2011), 157–170 Ma (Tarver et al. 2016), and 123–166 Ma (Álvarez-Carretero et al. 2021) – should therefore probably be treated with some skepticism (see also Bromham 2019; Budd and Mann 2022), because any age older than 125 Ma but younger than the early Triassic (Álvarez-Carretero et al. 2021: supplementary information) is potentially congruent with the known fossil record. The age of this divergence is likely to remain loosely constrained pending further fossil discoveries that can be convincingly shown as tightly bracketing either side of the split. “Tip dating” represents an alternative approach for inferring divergence dates, in which the ages of the sampled taxa are used together with either morphological or total evidence data (if included) to infer divergence times (Turner et al. 2017; King and Beck 2020; Luo et al. 2020). However, improvements in the fossil record will also be needed to improve our confidence in estimates for the Metatheria-Eutheria split using tip dating, because this approach is strongly influenced by taxon sampling (Turner et al. 2017; Luo et al. 2020).

Deltatheroida The affinities of deltatheroidans were controversial for many years after their discovery (Kielan-Jaworowska et al. 2004). Some authors noted derived similarities to marsupialiforms, in particular their dental formula of three premolars and four molars (see section “The Earliest Metatherians and the Timing of the MetatheriaEutheria Split” above; Kielan-Jaworowska et al. 2004). Others, however, emphasised the seemingly very plesiomorphic molar morphology of deltatheroidans compared to that of definitive therians (e.g., Cifelli 1993; Cifelli and Muizon 1997). Discoveries of comparatively well-preserved remains of deltatheroidans from the Late Cretaceous of Asia (Rougier et al. 1998; Averianov et al. 2010; Bi et al. 2015; Velazco et al. 2022) have collectively revealed the presence of several additional putative metatherian apomorphies. These include a staggered second lower incisor, a medially inflected angular process, absence of a stapedial artery groove on the promontorium of the petrosal, and presence of a short, horizontal prootic canal (see section “The Earliest Metatherians and the Timing of the Metatheria-Eutheria Split” above). Also of note is a juvenile specimen of Deltatheridium (PSS-MAE 221) that provides convincing evidence for a marsupial-type pattern of dental replacement (Velazco et al. 2022). Associated postcranial material of Deltatheridium exhibits metatherian features (Horovitz 2000; Velazco et al. 2022), as do isolated several postcranial specimens (humeri, femora, and tarsals) from the Late Cretaceous (~90 Ma) Bissekty Formation of Uzbekistan, at least some of which probably belong to deltatheroidans (e.g., Sulestes; Szalay and Sargis 2006; Chester et al. 2010, 2012). Collectively, these Late Cretaceous specimens provide compelling evidence that deltatheroidans are indeed members of Metatheria. The earliest known deltatheroidans, from the ~110 Ma Trinity Group of North America, are much more poorly known, being represented by fragmentary dental remains only (Davis et al. 2008;

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Averianov 2015). However, these are sufficient to suggest the presence of four molars (as in definitive metatherians) in at least two taxa, namely, Oklatheridium and Atokatheridium (Davis et al. 2008; Averianov 2015). It is therefore unsurprising that recent published phylogenetic analyses of broadscale mammaliaform relationships have consistently placed deltatheroidans within Metatheria, as one of its deepest branches (Fig. 2; Ni et al. 2016; Bi et al. 2018; Celik and Phillips 2020; King and Beck 2020; Wang et al. 2021). This was formally recognized by Vullo et al. (2009), who gave the name Marsupialiformes to the metatherian subclade that excludes Deltatheroida (Table 1; see also Beck 2017a: Table 13.1). The recent study by Velazco et al. (2022) has challenged this consensus view of deltatheroidan affinities by placing Deltatheridium (and also Pucadelphys; see below) within Marsupialia. This result is surprising and warrants further testing; as discussed by Beck et al. (2022: 311), Velazco et al. (2022) included only two extant marsupials (Didelphis and Dromiciops) in their analysis, and at least some of the apomorphies supporting the inclusion of Deltatheridium and Pucadelphys within Marsupialia appear questionable. On current evidence, it seems more likely that deltatheroidans are indeed early-branching metatherians, as found in most published analyses except that of Velazco et al. (2022); this is more congruent with their comparative antiquity compared to definitive marsupials (see section “Earliest Southern Hemisphere Masupialiforms and the Age of Marsupialia” below), as well as the distinctly plesiomorphic morphology of their molars that has been noted by several authors (Cifelli 1993; Cifelli and Muizon 1997). However, it should be borne in mind that some of the seemingly plesiomorphic molar features of deltatheroidans may be the result of secondary simplification connected with the evolution of a carnassial-type dentition (Muizon and Lange-Badré 1997). The most recent published phylogenetic analyses to include a dense sampling of deltatheroidans are those of Ni et al. (2016) and Cohen (2017). These do not support monophyly of separate North American or Asian deltatheroidan clades, suggesting a complex biogeographical history for the group (Fig. 2). Despite their diversity in the Late Cretaceous of both Asia and North America, only a single probable deltatheroidan is known to have survived the K-Pg mass extinction event, the tiny Gurbanodelta kara from the late Paleocene (late Gashatan Asian Land Mammal Age; ~56–57 Ma) South Gobi locality in China (Ni et al. 2016).

Late Cretaceous Marsupialiforms The earliest definitive marsupialiforms are from the early Cenomanian (~98 Ma) Mussentuchit local fauna in the upper Cedar Mountain Formation of Utah (Cifelli and Muizon 1997; Cifelli 2004), and they reach their greatest known diversity during the latest Cretaceous (Campanian-Maastrichtian) of North America (Cifelli and Davis 2003; Bennett et al. 2018). With a few exceptions, these Late Cretaceous marsupialiforms are known from isolated dental remains, and most are characterized by relatively generalized tribosphenic morphologies (Kielan-Jaworowska et al. 2004;

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Vullo et al. 2009; Williamson et al. 2014); their relationships are correspondingly uncertain. Previously recognized groups such as “alphadontids” and “pediomyids” sensu Kielan-Jaworowska et al. (2004) do not form clades in recent phylogenetic analyses (Fig. 3; Davis 2007; Williamson et al. 2012, 2014). Notably, the analyses of Williamson et al. (2012, 2014), which sample most known Cretaceous marsupialiforms, are characterized by numerous polytomies and generally low levels of support (Fig. 3). One Cretaceous marsupialiform clade that does appear to be convincingly monophyletic is Stagodontidae, comprising the North American genera Didelphodon, Eodelphis, Hoodootherium, Fumodelphodon, and (more questionably) Pariadens (Fox and Naylor 2006; Williamson et al. 2012, 2014; Wilson et al. 2016; Cohen 2017). Stagodontids include some of the largest (~5 kg in the case of Didelphodon vorax; Wilson et al. 2016) and most derived Cretaceous marsupialiforms currently known, united by numerous dental and mandibular apomorphies connected with carnivory and durophagy (Fox and Naylor 2006; Wilson et al. 2016; Cohen 2017; Brannick and Wilson 2018). Isolated tarsals tentatively referred to stagodontids by Szalay (1994) are also distinctive, and Didelphodon at least may have been semiaquatic (Szalay 1994; Longrich 2004; but see Fox and Naylor 2006); thus, stagodontids may have occupied a specialized ecological niche. However, the position of stagodontids within the broader marsupialiform radiation is less clear, and the phylogenetic analyses of Williamson et al. (2012, 2014) recovered Stagodontidae as one branch of a major polytomy at the base of Marsupialiformes (Fig. 3). A key question, still not satisfactorily resolved, is the relationship between the various Cretaceous marsupialiforms of Laurasia and Cenozoic taxa. This has important implications for understanding the origin(s) of Cenozoic marsupialiform clades, in particular those of the southern hemisphere. It is also critical for determining the impact of the K-Pg mass extinction event on metatherian diversity: if Cretaceous marsupialiforms include early representatives of multiple different clades that survived into the Cenozoic, this implies that multiple lineages successfully crossed the K-Pg boundary; alternatively, if Cretaceous marsupialiforms cannot be convincingly shown to be related to multiple Cenozoic clades, this may be an indication that the K-Pg mass extinction event had a severe impact on metatherian diversity. Some studies have proposed specific links between a number of these Late Cretaceous taxa and Cenozoic taxa. For example, Case et al. (2005) identified three marsupialiforms from the Lancian (latest Cretaceous) of North America (Glasbius, Ectocentrocristus, and Hatcheritherium) as members of the otherwise predominantly South American, Cenozoic order Polydolopimorphia (see section “Polydolopimorphia” below) and a fourth (Nortedelphys) as an early herpetotheriid (see section “Cenozoic Laurasian Marsupialiforms” below). Several authors (Marshall and Muizon 1988; Muizon 1991; Oliveira and Goin 2012; Goin et al. 2016) have noted close similarities in molar morphology between Khasia cordillerensis (originally described as a microbiotherian; Marshall and Muizon 1988) from the Paleocene Tiupampa fauna of Bolivia and North American Late Cretaceous

Fig. 3 Time-calibrated phylogeny of Metatheria, focused on Cretaceous marsupialiforms and based on 83 dental characters (strict consensus of 2008 most parsimonious trees). Numbers to the right of branches are Bremer support values. (Reproduced from Williamson et al. (2014: fig. 6) under a Creative Commons Attribution License (CC BY 4.0))

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“pediomyoids,” in particular Iqualadelphis lactea and ?Leptalestes cooki (see Davis 2007). Carneiro and Oliveira (2017b) suggested that Eobrasilia from the early Eocene Itaboraí fauna of Brazil is a stagodontid, and Carneiro (2018) argued that the Late Cretaceous North American Varalphadon is an early member of Sparassodonta, an otherwise entirely South American clade of carnivorous marsupialiforms (see section “Sparassodonta” below). Finally, Muizon and Ladevèze (2022) suggested that Aenigmadelphys from the Campanian of North America is closely related to three Paleogene South American genera: Incadelphys and Szalinia from Tiupampa and Marmosopsis from Itaboraí. However, at least some of these proposed links seem questionable. The phylogenetic analyses of Williamson et al. (2012, 2014; see Fig. 3 of this chapter) did not place Nortedelphys within Herpetotheriidae as defined by Williamson et al. (2012; see Table 1). It has been suggested that Ectocentrocristus may be a dP3 of a Turgidodon-like taxon (R. Cifelli, personal communication, in Beck et al. 2008a; Williamson et al. 2012; Beck in press), and neither it nor Hatcheritherium formed a clade with Glasbius or Roberthoffstetteria (a putative early polydolopimorphian from the Paleocene of South America; see section “Polydolopimorphia” below) in the phylogenetic analyses of Williamson et al. (2012, 2014; see Fig. 3 of this chapter). Glasbius has been more convincingly linked with polydolopimorphians: it was placed sister to Roberthoffstetteria in the phylogenetic analyses of Williamson et al. (2012, 2014; see Fig. 3 of this chapter) – although it should be noted that the sampling of South American taxa was extremely limited in both of these studies – and was recovered as a polydolopimorphian in the implied weights analysis of Chornogubsky and Goin (2015). However, the position of Glasbius was unresolved in the equally weighted analysis of Chornogubsky and Goin (2015), and recent analyses by Carneiro and collaborators have instead placed it within Didelphimorphia (Fig. 5b; Carneiro 2018, 2019; Carneiro et al. 2018). A detailed consideration of the distribution of bunodont features within metatherians suggests that the derived similarities shared by Glasbius and definitive polydolopimorphians may be convergent (Beck et al. 2008a; see section “Polydolopimorphia” below). Davis’ (2007) phylogenetic analysis placed Glasbius within Pediomyoidea sensu stricto, with the slightly older North American pediomyoid Aquiladelphis potentially representing a more plesiomorphic relative. Thus, Glasbius may represent a Late Cretaceous North American “experiment” in bunodonty, without a specific relationship to South American bunodont taxa (contra, e.g., Case et al. 2005; Williamson et al. 2012, 2014; Goin et al. 2016). Discovery of more complete remains of Glasbius is needed to more rigorously test its affinities. The proposed link between Khasia and North American Late Cretaceous “pediomyoids” has been criticized by Muizon and co-authors (Muizon and Ladevèze 2020; Muizon et al. in press), but was supported in the phylogenetic analyses of Carneiro et al. (2018) and Carneiro (2019). Eobrasilia is known from extremely fragmentary and heavily worn dental material that preserves little if any occlusal morphology (Marshall 1987), and most of the similarities to stagodontids identified by Carneiro and Oliveira (2017b) appear to be relatively general adaptations to durophagy that have arisen in several different metatherian groups (e.g.,

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malleodectids, Anatoliadelphys, Sarcophilus; Archer et al. 2016b; Maga and Beck 2017). The upper premolars of Eobrasilia also lack the distinctive lingual lobes characteristic of some stagodontids (although they are absent in Eodelphis; Fox and Naylor 2006; Cohen 2017). Carneiro’s (2018) suggestion that the North American Late Cretaceous Varalphadon is an early sparassodont was also rejected by Muizon et al. (2018: 430; see also Muizon and Ladevèze 2020). Muizon and Ladevèze’s (2022) proposal of a clade comprising the North American Late Cretaceous Aenigmadelphys and South American Paleogene Incadelphys, Szalinia, and Marmosopsis (which they referred to as the “SAMI” clade), meanwhile, is based on molar features that appear relatively subtle and/or seem likely to be highly homoplastic (e.g., relative sizes of stylar cusps, trigonid and talonid of subequal width, entoconid taller than hypoconid). Monophyly of the “SAMI” clade was found only in Muizon and Ladevèze’s (2022) implied weights phylogenetic analysis and not their equally weighted analysis. Thus, current evidence in support of specific links between Cretaceous and Cenozoic marsupialiforms does not appear compelling, and confident resolution of their precise relationships will probably require the discovery of more complete fossil remains. Well-preserved material (including crania and associated postcranial skeletons of several taxa) from the Paleocene Tiupampa locality in Bolivia gives an excellent insight into the anatomy of early Cenozoic marsupialiforms (Marshall and Muizon 1995; Marshall and Sigogneau-Russell 1995; Muizon 1998; Ladevèze et al. 2011; Muizon et al. 2018; Muizon and Ladevèze 2020), but there are still few wellpreserved taxa from the Cretaceous (Szalay and Trofimov 1996; Williamson et al. 2014; Wilson et al. 2016), and these are biogeographically widely separated, with some yet to be formally described (e.g., reported cranial remains of Alphadon halleyi; Brannick et al. 2017). Based on specimens described to date, however, cranial anatomy (including petrosal anatomy) appears relatively conservative in Cretaceous marsupialiforms (Szalay and Trofimov 1996; Williamson et al. 2014; Wilson et al. 2016), as it is within Metatheria in general (Wible et al. 2005). Postcranial specimens, particularly tarsal remains, may therefore prove more informative in resolving relationships between Cretaceous and Cenozoic marsupialiforms, building on the pioneering work of Szalay (1994). Focusing purely on fossil record from the Western Interior of North America, which is particularly well sampled, it appears that marsupialiforms were severely affected by the K-Pg mass extinction event. Having been both taxonomically more diverse (Cifelli and Davis 2003; Wilson 2014) and more disparate ecomorphologically (Wilson 2013) than eutherians in the latest Cretaceous (Lancian), only a single, generalized (presumably insectivorous) marsupialiform (Peradectes cf. P. pusillus) is known from the earliest Paleocene (Puercan 1; Wilson 2013; Wilson 2014). Marsupialiformes as a whole remained taxonomically and ecomorphologically depauperate throughout the Cenozoic in North America (Korth 2008; Bennett et al. 2018), particularly in comparison to the diverse and successful eutherian radiation (Rose 2006).

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Cenozoic Laurasian Marsupialiforms Like the Cretaceous taxa discussed above, most Cenozoic marsupialiforms from Laurasia are morphologically conservative (Crochet 1980; Sánchez-Villagra et al. 2007; Korth 2008; Horovitz et al. 2009), being characterized by an unspecialized tribosphenic molar morphology and small body size ( 0.001). Similarly, NPP directly influences species richness (β ¼ 0.302, P > 0.001), but the indirect effects through the FVS were weak (β ¼ 0.029 [0.504 x 0.059], P ¼ 0.001). The FVS was weakly associated with species richness (β ¼ 0.059, P ¼ 0.001). Interestingly, the topographic complexity was negatively and weakly associated with the variation in richness of American marsupials (β ¼ 0.089, P > 0.001).

Compositional Dissimilarity The taxonomic composition of marsupial species was spatially heterogeneous throughout the Americas (Fig. 3a). In general, the composition of marsupial species was quite homogeneous among cells located in the tropical region of South America (Fig. 3b) and shifted gradually toward the subtropical region of the South American continent (Fig. 3b). However, species composition changes abruptly between Tropical South America and Central America (Fig. 3b). The latter communities form a distinct cluster together with North American ones, implying a markedly different composition than that of South American cells (Fig. 3a).

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Fig. 1 Spatial distribution of marsupial species richness. (a) Observed species richness across the Americas and (b) relationship between marsupial species richness and latitude. Each point in (b) represents the marsupial species richness (in 1
by 1
cells) at a given latitude. Dashed lines delimit the tropical region

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Fig. 2 Structural equation model (SEM) showing the paths and coefficients of the relationship between marsupial species richness and predictor variables. Positive effects are indicated by solid arrows and negative effects by dashed arrows. Values on arrows represent standardized regression coefficients (β). NS represents a nonsignificant effect. Abbreviations: Tmean (annual mean temperature); NPP (net primary productivity); FVS (forest vertical structure); Topography (topographic complexity); Tmin (minimum temperature of the coldest month); ΔT (temperature seasonality); ΔP (precipitation seasonality); Pmin (precipitation of driest month). The total effect of a predictor variable on species richness is equal to the sum of direct and indirect effects. The indirect effects are estimated simply by multiplying the standardized paths involved

A comparison between northern and southern hemispheres revealed that the contribution of geographic and climatic distance on marsupial beta diversity varied across these regions (Fig. 4). More specifically in the northern hemisphere, the turnover component was more strongly related to geographic distance (r2 ¼ 0.22; p < 0.05) than climatic distance (r2 ¼ 0; p < 0.05), with an important portion of variation shared between space and climate (r2 ¼ 0.26; p < 0.05; Fig. 4a). These results indicate that the decrease in species similarity in the northern hemisphere is mainly associated with spatial factors (Fig. 5a and b). In the southern hemisphere, the turnover component was closely associated with both geographic (r2 ¼ 0.10; p < 0.05) and climatic (r2 ¼ 0.06; p < 0.05) distances (Fig. 4b). Therefore, the similarity between marsupial communities decreases with geographic and climatic distance (Fig. 5c and d), although the shared variance explained by space and climate is more important in the southern hemisphere (r2 ¼ 0.29; p < 0.05; Fig. 4b).

Discussion Species Richness There is a latitudinal gradient in marsupial species richness across the Americas (Fig. 1a and b), with higher species richness located in the tropical region. Using structural equation models, temperature seasonality and climatic extremes, as well as energy variables, contribute significantly to the latitudinal pattern, while topographic

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Fig. 3 Spatial variation in the taxonomic composition of American marsupial. (a) Changes in taxonomic composition represented by ordering scores (ranging from 0.4 to 0.5). (b) Changes in taxonomic composition between different regions of the northern and southern hemisphere (SNH

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complexity, forest vertical structure, and precipitation seasonality are weak predictors of spatial variation in species richness. Seasonality and climatic extremes of temperature (ΔT and Tmin) were the variables most strongly related to the observed pattern of marsupial species richness (Fig. 2). These results indicate that there are few marsupial species in areas where the temperature is seasonally unstable and colder. Similarly, some studies have also recorded how latitudinal gradients in species richness can be affected by seasonality and climatic extremes of temperature (Williams and Middleton 2008; Šímová et al. 2011; Stevens et al. 2013; Spasojevic et al. 2014). For example, it has been shown that species richness is lower in climatically unstable areas (i.e., greater seasonality) because of the reduced degree of species specialization, linked with resource scarcity in such areas (Evans et al. 2005; Tello and Stevens 2010). Regarding climatic extremes, it has been suggested that colder environments support a smaller number of species because few species can physiologically tolerate stressful conditions (Currie et al. 2004; Šímová et al. 2011). Once seasonality and climatic extremes of temperature are collinear (Fig. 2), it is difficult to discern the effects of both processes on species richness across latitudes. However, most marsupial species cannot tolerate extreme conditions (Sánchez-Villagra 2013), especially regions with cold and more seasonal temperatures at higher latitudes. The current results also showed that Tmean and NPP are positively correlated with the marsupial species richness (Fig. 2). Climatic determinants, mainly associated with temperature and productivity, were one of the first explanations proposed for global patterns in species richness (Rohde 1992) and are still being supported in empirical studies (Brown 2014). The current results are consistent with the findings of Figueiredo and Grelle (2018), which also point out the importance of environmental energy for species richness of American marsupials. Although strong relationships between climate and diversity have been widely recorded (Evans et al. 2005), it has proved challenging to determine the mechanisms behind this phenomenon. These challenges are a reflection of different processes in which the climate can affect diversity, including direct effects on the metabolism of organisms or indirect effects operating on plant productivity (Storch 2012). Statistical models that mechanistically try to disentangle the relative contribution of these processes are important avenues to be explored in the future (see Cerezer et al. 2021). However, this chapter is in line with other evidence observed in evolutionarily and ecologically distinct groups (Currie et al. 2004; Evans et al. 2005) and shows that the energy is a crucial determinant of species richness at large scales.

ä Fig. 3 (continued) ¼ > 23.4
; TROP ¼ 23.4
to 23.4
; SSH ¼ < 23.4
). Ordering scores were obtained from a principal coordinate analysis (PCoA) using the turnover component of the pairwise Jaccard dissimilarity. Note that the similarity in species composition declines abruptly toward the northern hemisphere (indicated by black arrow). Abbreviations: SSH ¼ subtropical region of the southern hemisphere; TROP ¼ tropical region; SNH ¼ subtropical region of the northern hemisphere

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Fig. 4 Unique and joint contributions of space and climate on marsupial compositional dissimilarity (turnover component of Jaccard dissimilarity) across hemispheres. Effects of geographic and climatic distance on compositional dissimilarity in the (a) northern and (b) southern hemispheres

Surprisingly, variables associated with environmental heterogeneity had low predictive power in the marsupial species richness. Topographic complexity was negatively and weakly associated with species richness (Fig. 2). Indeed, a weak relationship between species richness and topographic variability has been recorded in some previous studies (Hawkins et al. 2003b; Diniz-Filho et al. 2004), suggesting that the explanatory power of topographic complexity may be reduced over a large geographical extent. Additionally, the forest vertical structure (FVS) measure had a very weak effect on species richness (Fig. 2). Previous studies showed that species richness in some continents and clades (primates and amphibians) are better explained by the forest vertical structure, while for other clades this does not apply (birds and mammals) (Roll et al. 2015). American marsupials occupy a wide range of habitat types and encompass diverse locomotor strategies, which may explain this weak association found between species richness and FVS (in opposition to the

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Fig. 5 Relationship between similarity in species composition (1 minus the turnover component of Jaccard dissimilarity) and geographic and climatic distances for all pairwise comparisons of marsupial communities in the northern and southern hemispheres. The decay of compositional similarity with (a) geographic distance and (b) climatic distance in the northern hemisphere. The decay of compositional similarity with (c) geographic distance and (d) climatic distance in the southern hemisphere

mostly arboreal primates). Therefore, it may be suggested that variables representing energy and seasonality are more important than variables representing topographic and habitat heterogeneity to predict broad-scale patterns of marsupial species richness.

Compositional Dissimilarity Species composition is broadly similar across communities located in the southern hemisphere (Fig. 3a), with a slight decrease in the proportion of shared species between the tropical and subtropical regions of this hemisphere (Fig. 3b). However, species composition changed markedly between the southern and the northern hemisphere (Fig. 3a), whereby marsupial communities in the Central and North America are notably dissimilar compared to those observed in South America (Fig. 3b).

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In the northern hemisphere, geographic distance was the main driver structuring the marsupial species turnover (Figs. 4a and 5a, b). In contrast, the distance-decay pattern observed in the northern hemisphere cannot be explained by differences in climate (Figs. 4a and 5b), suggesting that processes related to dispersal and/or historical factors are more important for the turnover in such hemisphere. Marsupials have more restricted physiological/climatic tolerances than placentals (Sánchez-Villagra 2013), and a small number of species occurs in high temperate latitudes. Although glaciation events were much more intense in the northern hemisphere and cannot be ignored (Dunn et al. 2009; Baselga et al. 2012), the connection time between South and Central-North America via Panama Isthmus during the Pliocene (Woodburne 2010) should explain the turnover asymmetry between hemispheres. Recent land connections in the American continents, along with the poor dispersive capacity of marsupials (Schloss et al. 2012) and the presence of the Andes as a great geographic barrier for dispersal (Rahbek et al. 2019), may have limited the colonization of didelphid marsupials from South America to Central and North Americas. As the Panamanian land bridge was effectively created only recently (~2.5 mya; Webb 1991), marsupials probably did not have enough time to colonize all environments, as occurred in South America where they are autochthonous (Voss and Jansa 2009). Thus, it can be argued that marsupial species that arrived in Central and North America are not necessarily better colonizers than those that remained in South America. In fact, some species may have had the chance to cross the Andes at different moments, but difficulties in dispersion and establishment may have been strongly imposed throughout Central and North America. The species turnover between sites in the southern hemisphere was explained by a combination of geographic and climatic distance (Figs. 4b and 5c, d). Factors associated with space and climate were important in explaining the proportion of marsupial species shared across communities in South America. Thus, the current results suggest that species distribution across South America appears to be structured by an interaction between ecological determinism (e.g., environmental filtering) and stochasticity-driven assembly (e.g., dispersal limitation) (Gravel et al. 2006). Exponential decay of similarity to geographic and climatic distances can have many explanations (Soininen et al. 2007). An attractive explanation may be based on the complex biogeographic history of South America, involving the uplift of the Andes mountain chain (Rahbek et al. 2019) and the frequent episodes of expansion and contraction of forest and open environments (Giarla and Jansa 2014). Additionally, extant marsupials are autochthonous to South America (Voss and Jansa 2009) and are highly influenced by the climate (Cerezer et al. 2021) so that the isolation and species accumulation for a long time inside the continent may have limited the expansion toward cold latitudes outside the tropics (Sánchez-Villagra 2013; Jansa et al. 2014). Collectively, all of these events may have left footprints in the patterns of beta diversity and explain why deterministic and stochastic processes are equally important.

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Conclusion This chapter shows that some specific measures of energy and seasonality are better predictors of species richness of American marsupials than measures of environmental heterogeneity. Therefore, a higher restriction of marsupial species in the tropics may be a consequence of an environment with greater energy input and climatically more stable. Concerning beta diversity, a hemispheric asymmetry was recorded in the turnover component (compositional dissimilarity), whereby the contribution of space and climate differs between the southern and northern hemispheres. In summary, the influences of geographic and climatic distances were very similar in the southern hemisphere. In contrast, geographic distance was the main agent structuring the marsupial species turnover in the northern hemisphere, emphasizing the importance of dispersal limitation in this hemisphere. The authors claim that the history of marsupials through the Cenozoic, including the historic biogeography of land bridges and the appearance of geographic barriers (e.g., the Andes mountains), was crucial to the American marsupial diversification.

Cross-References ▶ Impact of Habitat Loss and Fragmentation in Didelphid Marsupials of the Atlantic Forest ▶ Trait Variation in American Marsupials Based on Biological Rules Acknowledgments Financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Finance Code 001 for Felipe O. Cerezer. Nilton Cáceres had a research fellowship in Ecology (Process number 313191/2018-2), granted by the Brazilian Agency for Scientific Research (CNPq) during the chapter elaboration.

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Cibele R. Bonvicino, Ana Lazar, Tatiana P. T. de Freitas, Rayque de O. Lanes, and Paulo S. D’Andrea

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Didelphis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Gracilinanus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Marmosa (Micoureus) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Marmosops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Metachirus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Monodelphis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Philander . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Thylamys . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Marsupial Lineages and Geographic Patterns . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Supplementary Information: The online version contains supplementary material available at https://doi.org/10.1007/978-3-031-08419-5_14. C. R. Bonvicino (*) Genetics Division, José Gomes de Alencar National Cancer Institute, Rio de Janeiro, RJ, Brazil Laboratório de Biologia e Parasitologia de Mamíferos Reservatórios, Instituto Oswaldo Cruz, Rio de Janeiro, RJ, Brazil e-mail: [email protected] A. Lazar Department of Vertebrates, National Museum, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil T. P. T. d. Freitas · P. S. D’Andrea Laboratório de Biologia e Parasitologia de Mamíferos Reservatórios, Instituto Oswaldo Cruz, Rio de Janeiro, RJ, Brazil R. d. O. Lanes Postgraduate Program in Genetics, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil © Springer Nature Switzerland AG 2023 N. C. Cáceres, C. R. Dickman (eds.), American and Australasian Marsupials, https://doi.org/10.1007/978-3-031-08419-5_14

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Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 667 Cross-References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 668 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 668

Abstract

The South American marsupials (Didelphimorphia) have a complex history. Previous studies have tended to focus on the role played by geomorphological arches and shields. In the present chapter, the species diversities of didelphimorphians from the Central Brazil, Atlantic, and Guiana shields and eastern and western Amazonian lowlands are compared, based on cytochrome b sequences. The effect of these regions on the diversification of the marsupials was investigated. The results show many species of Didelphis (2 species), Gracilinanus (2), Marmosops (8), Metachirus (4), Monodelphis (15), Philander (4), and Thylamys (3) restricted to only one of these regions. However, other species, such as Didelphis marsupialis, Gracilinanus emiliae, Marmosa limae, and Marmosa constantiae, have wider distributions, being found in more regions. All the genera except Thylamys have species distributed in at least two of these regions, with structured populations being observed in many cases. The highest marsupial diversity was found in the western Amazonian lowlands (21 species, 15 endemic) followed by that of the Atlantic (17, 12), Central Brazil (19, 8), and Guiana shields (13, 7) and the eastern Amazonian lowlands (8, 3). This emphasizes the importance of each of these regions for the conservation of the South American didelphimorphian diversity. Keywords

Biogeography · Cytochrome b · Didelphidae · Phylogeny · Amazonian lowlands · Atlantic shield

Introduction The biota of South America has a long and complex history. The South American platform, whose Precambrian basement is exposed, is composed of three distinct morphotectonic domains: the Guiana, Central Brazil (or Guaporé), and Atlantic shields (de Alkmim 2015; Fig. 1). The large Amazon craton is traversed by the intracratonic basins of the Solimões and Amazon rivers, which separate the Guiana and Central Brazil shields to the north and south, respectively (Albert et al. 2018). The Guiana, Central Brazil, and Atlantic shields, collectively known as the “eastern highlands” of South America, are composed of Proterozoic (2500–541 MYA) crystalline igneous and metamorphic rocks that form the Amazon craton, together with some overlying Paleozoic (541–252 MYA) sedimentary formations (Hartmann 2002). The Guiana Shield includes eastern Venezuela; the whole of Guyana, Surinam, and French Guiana; and the Brazilian states of Amapá, Roraima, and (partially)

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Fig. 1 South America showing (a) the Vaupes (Miocene), Fitzcarrald (Pliocene), and Purus (Pre-Cambrian/Neoproterozoic era to the Paleozoic era in the Pennsylvanian) arches, and the Amazon, São Luiz, São Francisco, and Luíz Alves cratons from the Pre-Cambrian; (b) limits of the western and eastern Amazonian lowlands and the Guiana, Central Brazil, and Atlantic shields; and (c) the Cerrado, Caatinga, Atlantic Forest, and Amazonia ecoregions, and the principal tracts of savanna vegetation in the Amazon region. (Modified from Albert et al. 2018; Alkmin 2015)

Amazonas and Pará (Steiner and Catzeflis 2004). Although it does not have the highest mammalian biodiversity in the Neotropics (Lim 2012), this region encompasses the Guiana center of endemism, one of the largest of the Amazonian biogeographic regions (Silva et al. 2005). The Guiana Shield is characterized by the presence of tableland formations or “tepuis” in the form of isolated mesas, which are part of the oldest geological formation found in South America, dating to the Precambrian era (Hershkovitz 1969). The role of the Guiana Shield as a zoogeographical unit has been recognized by many authors, beginning with Wallace (1852) and including Hoogmoed (1979), Voss and Emmons (1996), and Voss et al. (2001). Furthermore, despite the long-term shifts in the distribution of savanna and forest habitats, the Guiana Shield has acted as a stable core area in which many ancestral species persist (Lim 2012), thus playing an important role in the mammalian biodiversity of the South American domain. The Central Brazil and Atlantic shields are frequently considered to be a single unit, when they are referred to as the Brazilian Shield. In the present chapter, however, the two shields were considered to be distinct geological units (Fig. 1). The Central Brazil Shield is covered with Phanerozoic sedimentary rocks, which are associated with basalts up to a number of hundred meters thick, in central and western Brazil, extending west into Bolivia and part of Paraguay (Hasui and de Almeida 1985). The Central Brazil Shield has two sectors, distinguished by their lithology and structure: the eastern sector – the Tocantins structural province – and the western sector, which includes the southern Amazon sedimentary basin and the Tapajós province (Hasui and Almeida 1985). The Tocantins province is covered predominantly by savannah, with local forest, and the lowlands of the Pantanal also belong to this province, whereas the Tapajós province is covered with dense tropical forest (Almeida et al. 1981). Despite the lack of studies that focus on the Central Brazil Shield, a number of studies have evaluated the mammalian fauna of the Cerrado, Pantanal, or the forested regions of these shields (e.g., Brandão de Oliveira

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et al. 2019; Carmignotto et al. 2011; Tomás et al. 2017) and have reported considerable diversity in this region. The Atlantic Shield is composed of mobile, long, and sinuous Proterozoic (Brazilian) granulite-rich belts (Goodwin 1996). This tectonically complex shield comprises three structural provinces, the São Francisco, Borborema, and Mantiqueira provinces, as well as São Luís craton, which is part of the São Francisco craton, in the north, and the Luiz Alves craton in the south (Goodwin 1996, Albert et al. 2018; Fig. 1). Some authors also include part of the Rio de la Plata craton here, although the exact limits of this craton are not subject to a general consensus (Rapela et al. 2011). The Atlantic shield is covered primarily by Atlantic Forest, which extends from eastern Brazil to Paraguay and Misiones Province, in Argentina, in addition to Caatinga dry scrub and transitional areas with the Cerrado savanna (Fig. 1). The majority of the studies on the mammalian fauna of this region have focused on the Atlantic Forest (e.g., Bovendorp et al. 2017), although there are also some studies of the Caatinga and Cerrado (e.g., Carmignotto et al. 2011), which have shown a high diversity. The western Amazon region encompasses a number of sub-Andean sedimentary basins (Hurtado et al. 2018). It is separated from the Llanos basin, to the north, by the Vaupés Arch, and from the basin of the upper Madeira, to the south, by the Fitzcarrald Arch (Albert et al. 2018; Fig. 1). The western Amazonian lowlands are a unique biogeographic region, which is one of the world’s richest biological hotspots (Bush 1994; Adams 2009; Hoorn et al. 2010). The complex geomorphological history of this region, including evidence of two major marine incursions, has contributed to the diversity of its flora and fauna (D’Apolito 2016). The region of the eastern Amazonian lowlands is poorly studied, and its exact limits are not well defined. As defined here, this region includes the area east of Purus arch, between the lower Madeira and Tocantins rivers, south of the Amazon River, extending southward to the foothills of the Central Brazil Shield, and northward to the lowlands north of the lower Amazon (Fig. 1). Part of this region has been studied and is known to have a considerable mammalian species richness (Stone et al. 2009). The landscape of this region is relatively flat, with extensive floodplains traversed by multiple small rivers. It is also one of the most impacted sectors of the Amazon basin, with extensive deforestation, logging, bushfires, and cattle ranching (Stone et al. 2009). While this ecoregion has a diverse biota, in particular, of birds and bats, it is not as rich as that of other areas within the Amazon basin (WWF 2020). The principal sector of these lowlands is the floodplain of the lower Amazon, which includes the Marajó archipelago, and extensive geological formations established between the Tertiary and the Holocene (Rossetti and de Toledo 2006). The area to the east of the Tocantins River is the most densely populated part of the Brazilian Amazon region and likely represents the future scenario of the rest of the eastern Amazonian lowlands (Stone et al. 2009). The mammalian diversity of the western Amazonian lowlands (e.g., Carvalho 1957; Voss and Emmons 1996; Patton et al. 2000; Bernarde and Machado 2008; Nunes-Lavocat et al. 2015; Abreu-Júnior et al. 2016; Voss et al. 2019) and the Guiana Shield (Beebe 1919; Tate 1939; Handley 1976; Voss and Emmons 1996;

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Voss et al. 2001; Engstrom and Lim 2002; Rossi et al. 2016) has been surveyed extensively. Relatively much fewer studies have focused on the mammals of the Central Brazil Shield and the eastern Amazonian lowlands (Stone et al. 2009). Phylogeographic research is a powerful tool for the elucidation of the current geographical patterns of the different subdivisions of a taxon and the comparison of the phylogeographic patterns of multiple co-distributed taxonomic groups. Comparative phylogeography is even more appropriate for testing hypotheses on the factors determining contemporary patterns of biodiversity (Arbogast and Kenagy 2001). The geographic regions that are the focus of the present chapter offer a valuable opportunity to test hypotheses on the historical affinities and diversity of the marsupial order Didelphimorphia, an ancient South American mammalian lineage. The present chapter represents a preliminary investigation of the phylogeographic patterns of this group, based on mitochondrial cytochrome b sequences. The chapter focuses on the species richness and composition, and the geographic structuring of eight didelphimorphian genera: Didelphis, Gracilinanus, Marmosa (Micoureus), Marmosops, Metachirus, Monodelphis, Philander, and Thylamys, including the most diverse genera of the subfamily Didelphinae.

Methods Cytochrome b (mt-Cytb) sequences of specimens of the genera Didelphis, Gracilinanus, Marmosa (Micoureus), Marmosops, Metachirus, Monodelphis, Philander, and Thylamys were obtained from the database of the authors’ laboratory and from GenBank (Table 1). In the case of such samples, sequences with less than 750 base pairs were not considered for analysis except when they were the only material available for a given species or region. The country acronyms used in the figures are based on the ALPHA-3 codes (IBAN 2020). The phylogeographic patterns of these didelphimorphian were analyzed in relation to five geographic regions: the Guiana, Central Brazil, and Atlantic shields, and Western and Eastern Amazonian lowlands, following Albert et al. (2018), Hurtado et al. (2018), and Roddaz et al. 2005), in order to compare their species composition and analyze their connections. The most appropriate nucleotide substitution models for the phylogenetic reconstructions and the maximum likelihood (ML) analyses were selected and run in MEGA X (Kumar et al. 2018). The branch support for the ML topologies (based on the best tree) was obtained using the bootstrap procedure (1000 pseudoreplicates). Two models were selected for the ML mt-Cytb datasets. The General Time Reversible + gamma distribution and invariable sites model was selected for the analysis of Didelphis, Gracilinanus, Marmosa (Micoureus), Marmosops, Metachirus, Monodelphis, and Thylamys, while the Tamura Nei (TN93) model + gamma distribution model was selected for Philander. Additional GenBank sequences, including outgroups, were combined with the data for the phylogenetic analyses (Table 1). The median-joining (MJ) network (Bandelt et al. 1999) was reconstructed in the Network program (version 4.5.1.6; available at http://www.fluxus-engineering.com).

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Table 1 List of the mt-Cytb sequences included in the molecular analyses presented in this chapter, with the GenBank accession number Didelphis D. aurita GU112879–112885. D. albiventris JF280991, KM071410, KT447516–447520, JF280983–280990, JF281003. D. imperfecta AJ487004. D. marsupialis HM589701–589702, JF280998–280002, KJ129895, KT447521, MG491975, U34665. D. virginiana HM589699–589700, KJ129896 Gracilinanus G. aceramarcae HQ622162. G. agilis HQ622149, HQ622153, KF313925, KF313935, KF313940, KF313942, KF313948, KF313950, KF313953, KF313955, KF313958, KF313964, KF313967, KF313970, KF313978, KF313981, KM066014, KM066021. G. emiliae KU171192, KR190439, KR190441. G. marica KU171193. G. microtarsus JF281020, KF313982, KT952216, KT952229, KT952232, KT952237, KT952250, KT952239. G. peruanus KM066026–066029, KU171195 Marmosa (Micoureus) M. alstoni JN887133. M. rapposo HM106368–106369, JN887136, MK496187, MK496189. M. constantiae EF587309, JF281084–281086, GU112917, HM106375, MK496184–496188, MK496190, MK496192–496196, MK496210, MK496212, MK496200-496201, MK496208, MK496213–496214, MW088886–088890, MW088892–088902. M. demerarae AJ606434–606437, AJ606440–606441, AJ606443–606444, AJ606447, EF587290–587291, JF281070, U34674. M. domina EF587295-587300, JF281071–281079, JF281081–281083, JF281099-281092, GU112916, GU112918, MK496181. M. limae EF154230, EF587292–587294, KF619579, MK496183, JF281088–281089. M. paraguayana EF587288-587289, ef587301-587303, EF587305–587308, GU112919–112924, HM106372-106373, JF281069, JN887137887140. M. rutteri HM106370, U34675, MW088903–088912, MW088914 Marmosops M. bishopi, KT437838-437839, KT437844, KT4378177847, KT437863, MW088848–088851. M. carri KT437721.

Out group Caluromys philander KJ129897, C. derbianus JF489138, C. lanatus U34664

Out group Caluromys lanatus U34664

Out group Marmosa (Marmosa) HM106343, HM106385, HM106397, HM106401, Caluromys philander KJ129897, C. lanatus KJ129898, C. derbianus JF489138

Out group Monodelphis emiliae KM071607, Monodelphis domestica EF154205 (continued)

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Table 1 (continued) M. caucae KT437694, KT437757, KT437859–437860, MW088852-088854. M. creightoni KT437722, KT437740. M. fuscatus KT437706, KT437763. M. handleyi KT437745. M. incanus GU112904, KC954771, KF313983, KT437713, KT437783, KT437787, KT437789–437790, KT437792, KT437805, KT952152–952164, KT952166, KT952168952176, KT952177, KT952180–952182, KT952184-952190, KT952191, KT952193, KT952196–952198, KT952201, KT952203, KT952204–952207, KT952208–952209, MW088856. M. noctivagus KT437812KT437827, KT437829, KT437831–437832, KT437834–437837, KT437845–46, KT437849, KT437851–54, KT437861, KT437864–437865, U34669–34670, MW088865–088869. M. ocellatus KT437810, KT437813, KT437821, KT437824, KT437848, KT437850, MW088872–088881. M. pakaraimae KC954770. M. parvidens AJ606427–606428. M. paulensis KC954772, KT437720, KT437761, KT437795–437796, KT437814, KT437880, MW088882–088883. M. pinheiroi AJ606431, AJ606433 Metachirus M. myosuros AJ628365, GU112909–112914, JF281094, KJ129889, KU171196, MK817273–817275, MK817277–817292, MK817296–817299, U34671–34672. M. nudicaudatus MK817294–817295, MK817301 Monodelphis M. adusta HM998564, KM071398. M. americana MW088821–088824. M. arlindoi KM071462. M. dimidiata EF154221, HQ651777, KM071337, KM071357, KM071385, KM071388, KM071562–071563. M. domestica HQ651771, HQ651773. M. emiliae DQ385832–385835, KJ129900, KM071383, KM071602–071607, MW088831. M. gardneri KM071565, M. glirina MW088834–088841. M. maraxina HM998559, KM071375, KM071536–071543, KM071545–071546, KM071548–071554. M. handleyi DQ386631–386632, KM071400. M. iheringi KM071389, KM071561. M. kunsi KM071558, HM998582–998584, KM071336,

Out group Caluromys philander KJ129897, C. lanatus KJ129898, C. derbianus KU171185

Out group Didelphis albiventris KT447517, Gracilinanus microtarsus KF313982

(continued)

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Table 1 (continued) KM071340, KM071344, KM071346, KM071352, KM71559-071560. M. osgoodi KM071401. M. peruviana DQ386615, DQ385840, HM998589-998590, KJ129901, KM071405-071407, KM071409, U34676, BankIt MW088842–088846. M. reigi FJ810210–810211. M. sanctaerosae KM071527. M. scalops KM071598. M. touan KM071524–071525 Philander P. andersoni MG491896, JF281033, MG491892–491894. P. canus JF281034–201040, KT153573, KM188487–188488, MG491902–491909, MW088809–088814. P. pebas MG491957–491958, MG491960, KM88489. P. mcilhennyi AJ628366, JF201031, JQ388613–388614, MG491914–491921, MW088815–088816. P. melanurus MG491923, MG491926, MG491928. P. opossum AJ628367, KJ129894, KU508546, MG491930, MG491937–491939. P. pallidus MG491942–491952, MG491954–491955. P. quica JF201030, JQ778969, GU112936–112937, GU112939–112942, KU171197, MG491962 Thylamys T. citellus HM583374, GQ911594–911595. T. elegans HM583376, KF164533, HM583378–583379, KP994529. T. karimii HM583381, EF051700. T. macrurus HM583382–583383. T. pallidior HM583407–583411. T. puchellus KF164558–164559. T. pusillus HM583415–583419. T. sponsorius HM583426–583427, HM583429, HM583431, KF16456. T. tatei HM583449, KF164556–164557. T. venustus HM583482–583484, HM583488–583489, HM583499. T. velutinus HM583450-583451. Thylamys sp. HM583420, HM583423

Out group Caluromys philander KJ129897, MK817325, C.derbianus KU171185, C. lanatus U34664

Out group Caluromys philander KJ129897, C. derbianus KU171185, C. lanatus KJ129898

The population structure and geographic distribution patterns were evaluated excluding any sites with missing data. Geographic population structure is important for the multiplication of species and transformation (Wright 1951), and the absence of any structuring in a population may reflect the occurrence of gene flow. On the other hand, the presence of geographic structuring implies that gene flow is infrequent or absent and that each population may be evolving independently, given that the absence of gene flow is one of the principal components of the speciation process (Slatkin 1987).

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Results In the maximum likelihood (ML) analyses, all the species of each genera analyzed (which had more than one haplotype) proved to be monophyletic. The ML analysis of Didelphis included 40 sequences representing 38 haplotypes. This analysis divided the genus into two groups, one containing Didelphis virginiana and the second containing all the other species, some of which were subsequently assigned to subclades (Fig. 2). The median-joining (MJ) topology of Didelphis albiventris is consistent with the results of the ML and separated the Central Brazil Shield haplogroups from the remaining specimens by at least 26 nucleotide substitutions and one median vector. The MJ topology of Didelphis marsupialis is also consistent with the ML, revealing distinct population structuring, with specimens from North America lineages separated from those from South American by 32 and 24 nucleotide substitutions, and more than one median vector (Fig. 2).

Fig. 2 The maximum likelihood (ML) topology of Didelphis, showing the haplotype number per species, museum and/or field or tissue-sample numbers, localities, and the numbers of the collecting localities (in parentheses) shown on the map. The black circles represent the 80–100% bootstrap values, the black squares represent bootstrap values of 70–79%, and the white squares, bootstraps of 60–69%. The map shows the Didelphis collecting localities, the western and eastern Amazonian lowlands, and the three shields (color-coded on the map, and in the ML and MJ analyses). In the median-joining network of D. albiventris and D. marsupialis, the circles represent the haplotypes, and their size is proportional to the number of shared sequences, while the numbers refer to the haplotypes in the ML analysis. The black circles represent the median vectors, and the numbers on the lines are nucleotide substitutions

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The ML analysis of Gracilinanus was based on 37 sequences, which represented 37 haplotypes. This analysis also divided the genus into two groups, one containing Gracilinanus emiliae, and the other containing all the other species, some of which were also assigned to subclades (Fig. 3). The ML analysis also indicated differences between the G. emiliae clades from the western Amazonian lowlands and the Central Brazil Shield, and G. agilis from the Central Brazil and Atlantic shields (Fig. 3). The ML analysis of Marmosa (Micoureus) included 128 sequences representing 103 haplotypes (Fig. 4). The genus was divided into two major lineages, one containing Marmosa (Micoureus) rutteri and Marmosa (Micoureus) rapposa, and the second with all the other species and additional subclades (Fig. 4). The results of the network analysis of this genus are consistent with those of the ML (Fig. 5). This analysis also revealed population structuring in the samples of M. constantiae and M. limae from the different regions, i.e., the shields and lowlands (Figs. 4 and 5). The ML analysis of Marmosops was based on 151 sequences, with 112 haplotypes. Once again, all the Marmosops species with more than one haplotype were monophyletic, and the genus was divided into two major lineages, one containing Marmosops bishopi, Marmosops pinheiroi, Marmosops pakaraimae, and Marmosops parvidens and the other containing all the other species and subclades. This genus is distributed primarily on the Atlantic Shield and in the western Amazonian lowlands, and to a lesser extent, on the Guiana Shield (Figs. 6 and 7).

Fig. 3 Maximum likelihood topology of Gracilinanus showing the museum and/or field or tissuesample numbers, localities, and the numbers of the collecting localities (in parentheses), as shown on the map. The black circles represent the 80–100% bootstrap values, and the white squares, bootstrap values of 60–69%. The map shows the Gracilinanus collecting localities, the western and eastern Amazonian lowlands, and the three shields (color-coded on the map and in the ML and MJ analyses)

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Fig. 4 The maximum likelihood (ML) topology of Marmosa (Micoureus) showing the museum and/or field tissue-sample numbers, as well as the numbers of the collecting localities (in parentheses) shown on the map. The black circles in ML represent the 80–100% bootstrap values, and the black squares, bootstrap values of 70–79%. The map shows the Micoureus collecting localities, the western and eastern Amazonian lowlands, and the three shields (colorcoded on the map and in the ML and MJ analyses)

The ML analysis of Metachirus included 51 sequences representing 49 haplotypes (Fig. 8). Metachirus was divided into two major lineages, one containing Metachirus nudicaudatus, and the other with the remaining species and respective subclades, all with high support values (Fig. 8). The network analysis of this genus is consistent with the results of the ML analysis (Fig. 9). The ML analysis of Monodelphis included 98 sequences, with 89 haplotypes (Figs. 10 and 11), and all the Monodelphis species with more than one haplotype were shown to be monophyletic. This genus was divided into three major lineages, with a number of subclades (Figs. 10 and 11). The network analysis is consistent with the results of the ML analysis and revealed geographic structuring between the two M. emiliae populations from the Amazonian lowlands, between the M. domestica haplogroups from the Atlantic and Central Brazil shields, and between the M. kunsi populations (Fig. 12). The maximum likelihood (ML) analysis of Philander included 78 sequences, with 67 haplotypes. This genus has three lineages with a number of subclades

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Fig. 5 The median-joining network of Marmosa (Micoureus) constantiae, M. demerarae, M. domina, M. limae, Marmosa (Micoureus) sp., and M. esmeraldae. The circles represent the haplotypes (color-coded by region, as in the map, with white circles referring to regions not coded on the map), with their size being proportional to the number of shared sequences, while the numbers refer to the haplotypes shown in the maximum likelihood topology in Fig. 4). The black circles represent the median vectors, and the numbers adjacent to the lines are the nucleotide substitutions. The map shows the Micoureus collecting localities, the western and eastern Amazonian lowlands, and the three shields (color-coded on the map and in the ML and MJ analyses)

(Fig. 13). The network analysis of this genus is consistent with the results of the ML analysis, with Philander opossum in a central position (Fig. 14). The ML analysis of Thylamys included 42 sequences and 41 haplotypes and confirmed the monophyly of all the species with more than one haplotype. This genus had two lineages, one containing T. karimii and the other with the remaining species and subclades, located only on the Central Brazil Shield and in southwestern South America (Fig. 15).

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Fig. 6 Part I of the maximum likelihood topology of Marmosops showing the museum and/or field tissuesample numbers, and the numbers of the collecting localities (in parentheses) are shown on the map. The black circles represent 80–100% bootstrap values; the black squares, values of 79–79%; and the white squares, values of 60–69%. The map shows the collecting localities, the western and eastern Amazonian lowlands, and the three shields (color-coded on the map and in the ML and MJ analyses)

Discussion The classification of the marsupial taxa of the order Didelphimorphia should be considered with caution. The ample geographic ranges of many of the extant lineages have led to intensive research into the origins of the morphological diversity of the order, which has resulted in the description of a number of new species (Nascimento et al. 2015; Díaz-Nieto and Voss 2016; Pavan et al. 2017; Voss et al. 2018), and also the formulation of several alternative taxonomic arrangements (e.g., Voss et al. 2012; Lima-Silva et al. 2019). The present chapter did not aim to provide a comprehensive review of the order, but rather, to evaluate the differences in the species composition, distribution patterns, and phylogeographic relationships of the target didelphimorphian genera of the different regions analyzed here, that is, the Precambrian shields and the Amazonian lowlands.

Didelphis Didelphis has radiated throughout Central and South America, and neighboring parts of southern North America, and it is thus the most widespread didelphimorphian genus. The origin and diversification of this relatively ancient lineage are probably

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Fig. 7 Part II of the maximum likelihood topology of Marmosops showing the museum and/or field tissue-sample numbers, and the numbers of the collecting localities (in parentheses) shown on the map. The black circles represent 80–100% bootstrap values; the black squares, values of 79–79%; and the white squares, values of 60–69%. The map shows the collecting localities, the western and eastern Amazonian lowlands, and the three shields (color-coded on the map and in the ML and MJ analyses)

related primarily to the environmental changes that occurred during the PlioPleistocene (Dias and Perini 2018). This taxon is traditionally divided into six species, including one, D. virginiana (Kerr 1792), that ranges as far north as the Nearctic region. The other five species can be divided into two groups, the blackeared opossums – D. marsupialis Linnaeus, 1758, and Didelphis aurita WiedNeuwied, 1826 – and the white-eared opossums, D. albiventris Lund, 1840; Didelphis imperfecta Mondolfi and Pérez-Hernández, 1984; and Didelphis pernigra Allen, 1900 (Dias and Perini 2018). Only one of these species (D. pernigra) was not represented in the maximum likelihood analysis, which confirmed the validity of all the other species, in addition to detecting two distinct lineages in D. albiventris, one in Cerrado and another in the southern Atlantic Forest and the Paraguayan Chaco (Fig. 2). In South America, the Precambrian shields (areas with long-term habitat stability) and the Amazonian lowlands (where habitats have changed continuously over the past 4 Ma) are considered to have played an important role in the present-day distribution of these taxa (Bicudo et al. 2019). Some species, such as Didelphis aurita (found only on the Atlantic Shield and adjacent areas in the Paraná basin), have restricted distributions, while others, such as D. albiventris, occur on more than

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Fig. 8 Maximum likelihood (ML) topology of Metachirus showing the museum and/or field or tissue-sample numbers, and the numbers of the collecting localities (in parentheses), as shown on the map. The black circles in the ML represent the 80–100% bootstrap values and the white squares, bootstrap values of 60–69%. The map shows the Metachirus collecting localities, the western and eastern Amazonian lowlands, and the three shields (color-coded on the map and in the ML and MJ analyses)

one shield, with highly structured populations (see Nascimento et al. 2015). In the specific case of D. albiventris, the populations of the Central Brazil and Atlantic shields are well differentiated, with high bootstrap support (Fig. 2). These results are consistent with those of Nascimento et al. (2019), who used cytochrome c oxidase subunit I as a molecular marker and identified two distinct (southern and northeastern/southeastern) South American D. albiventris lineages. In this chapter, in addition, the D. marsupialis population from the western Amazonian lowlands formed a separate cluster from that of the Central Brazil Shield and the Central American lineages (Fig. 2). Despite the presence of distinct molecular lineages in some Didelphis taxa, the external characters are highly polymorphic, and it is virtually impossible to diagnose genetic lineages based only on morphological cues (Lavergne et al. 1997), which reinforces the need for more extensive, integrative research, to better understand the diversity of this genus.

Gracilinanus The radiation of the genus Gracilinanus was associated with the distribution of forest formations in South America, including those of the Cerrado ecoregion, as

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Fig. 9 The median-joining network of Metachirus, in which the circles represent the haplotypes, and their size is proportional to the number of shared sequences, while the numbers refer to the haplotypes in the maximum likelihood analysis (Fig. 8). The black circles represent the median vectors, while the numbers adjacent to the lines are nucleotide substitutions (color-coded on the map and in the MJ analyses)

reflected in the distribution of its present-day species (Brandão de Oliveira et al. 2019). This genus includes seven species (Creighton and Gardner 2008; Semedo et al. 2015) – Gracilinanus aceramarcae (Tate, 1931), Gracilinanus agilis (Burmeister, 1854), Gracilinanus dryas (O. Thomas, 1989), Gracilinanus emiliae (O. Thomas, 1909), Gracilinanus marica (O. Thomas, 1989), Gracilinanus microtarsus (J.A. Wagner, 1842), and Gracilinanus peruanus (Tate, 1931). Only one of these (G. dryas) was not represented in the maximum likelihood analysis, which indicated the presence of two G. emiliae lineages, located in the western Amazonian lowlands and Central Brazil Shield (Fig. 3). One species (G. microtarsus) was restricted to the Atlantic Shield and another, G. agilis, was structured, with one population on the Atlantic Shield and a second on the Central Brazil Shield (Fig. 3).

Marmosa (Micoureus) Marmosa (Micoureus) has speciated throughout all the major regions of South America, with the exception of its southernmost extreme. The subgenus Micoureus Lesson, 1842, has eight species (de la Sancha et al. 2012; Lima-Silva et al. 2019; Voss et al. 2020) – Marmosa (Micoureus) alstoni (J.A. Allen, 1990); M. (Micoureus) constantiae Thomas, 1904; M. (Micoureus) demerarae (Thomas 1905); Marmosa

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Fig. 10 Part I of the maximum likelihood (ML) topology of Monodelphis showing the museum and/or field or tissue-sample numbers, and the numbers of the collecting localities (in parentheses) shown on the map. The black circles in ML represent 80–100% bootstrap values and the open squares, values of 60–69%. The map shows the Monodelphis collecting localities, the western and eastern Amazonian lowlands, and the three shields (color-coded on the map and in the ML and MJ analyses)

(Micoureus) limae; Marmosa (Micoureus) paraguayana (Tate, 1931); Marmosa (Micoureus) phaea (Thomas, 1899); Marmosa (Micoureus) rapposa; and M. (Micoureus) rutteri (Thomas, 1924). The molecular phylogeny of the subgenus, presented here, includes all the species except M. (Micoureus) phaea, and the ML was consistent with the results of the previous studies (Dias et al. 2010; de la Sancha et al. 2012). Voss et al. (2020) considered M. budini Thomas 1920 to be a junior synonymous of M. rapposa Thomas 1899, and M. limae and M. parda Tate 1931 to be valid species. More recently, three other forms of the subgenus Micoureus, Marmosa germana Thomas, 1904; Marmosa parda Tate, 1931; and Marmosa perplexa Anthony, 1922, were recognized provisionally as valid species (Voss et al. 2020; Astúa et al. 2021). The analysis presented here confirmed the species status of M. alstoni, M. rapposa, M. constantiae, M. paraguayana, and M. rutteri, as suggested by Lima-Silva et al. (2019) and Voss et al. (2019, 2020). Gardner and Creighton (2008) recognized five M. demerarae subspecies – M. demerarae areniticola (Tate 1931), M. demerarae demerarae (Thomas 1905), M. demerarae domina (Thomas 1920), M. demerarae esmeraldae (Tate 1931), and M. demerarae meridae

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Fig. 11 Part II of the maximum likelihood (ML) topology of Monodelphis showing the museum or field tissue-sample numbers, and the numbers of the collecting localities (in parentheses) shown on the map. The black circles represent the 80–100% bootstrap values; the black squares, values of 79–79%; and the open squares, values of 60–69%. The map shows the Monodelphis collecting localities, the western and eastern Amazonian lowlands, and the three shields (color-coded on the map and in the ML and MJ analyses)

(Tate 1931) – and the current results indicate that at least three of these lineages (domina, esmeraldae, and demerarae) are in fact valid species (Figs. 3 and 4). Gardner and Creighton (2008) found evidence that the populations of Central Brazil and Atlantic shields were partly associated with the name domina. Voss et al. (2020) considered Marmosa (Micoureus) esmeraldae to be a junior synonym of M. demerarae, although the current analyses indicated that M. esmeraldae deserves full species status (Fig. 3). These authors also considered domina to probably be a “. . .synonym [. . .] of constantiae.,” but they offer no details other than the fact that the analyses were “. . .based on our examination of type material. . ..” The current ML and network analyses also identified parts of the population of Central Brazil and Atlantic shields as three distinct groups, which further supports the specific status of Marmosa (Micoureus) sp., M. limae, and M. domina and restricts the geographic distribution of this latter taxon to Central Brazil (Figs. 4 and 5). The phylogenetic tree also recuperated a clade that included samples from the Brazilian Amazon and Venezuela, which was a sister group of the other M. demerarae samples from the Guiana Shield and part of eastern Amazonian lowlands. The authors consider this population to belong to Marmosa (Micoureus) esmeraldae (Tate,

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Fig. 12 The Median-Joining network of Monodelphis domestica, Monodelphis emiliae, Monodelphis glirina, Monodelphis maraxina, and Monodelphis kunsi. The circles represent the haplotypes, and their size is proportional to the number of shared sequences, while the numbers refer to the haplotypes in the Maximum Likelihood topology (Figs. 10 and 11). The black circles are the median vectors and the numbers adjacent to the lines are the nucleotide substitutions (color-coded on the map, and in the MJ analyses)

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Fig. 13 The maximum likelihood (ML) topology of Philander showing the museum and/or field or tissue-sample numbers, as well as numbers of the collecting localities (in parentheses) shown on the map. The black circles in the ML represent the 80–100% bootstrap values; the black squares, values of 79–79%; and the open square bootstrap values of 60–69%. The map shows the Philander collecting localities, the western and eastern Amazonian lowlands, and the three shields (colorcoded on the map and in the ML and MJ analyses)

1931), which is distributed on the southern Guiana Shield and adjacent areas of the western Amazonian lowlands (Figs. 3 and 4). The median-joining analysis confirmed this arrangement, in particular, by differentiating the population from the Negro basin and adjacent parts of Venezuela (M. esmeraldae) from the other Guiana Shield samples (M. demerarae), while also separating part of the samples from the Central Brazil and Atlantic shields (M. domina), based on the number of median vectors and nucleotide substitutions (Fig. 4). These results are consistent with those of the previous studies that indicated the existence of a Micoureus species complex in the Amazonian lowlands (Voss et al. 2019). The other population from the western Amazonian lowlands was identified previously as M. regina, although here, Voss et al. (2019) is followed, who rejected this proposal and allocated the western Amazonian populations to Marmosa (Micoureus) rutteri Thomas, 1904. In fact, the present data show that M. demerarae is found primarily on the Guiana Shield and in the adjacent areas,

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Fig. 14 The median-joining network of Philander, in which the circles represent the haplotypes, and their size is proportional to the number of shared sequences, while the numbers refer to the haplotypes in the maximum likelihood topology (Fig. 13). The black circles represent the median vectors, and the numbers adjacent to the lines are the nucleotide substitutions. The map shows the western and eastern Amazonian lowlands, and the three shields (color-coded on the map and in the MJ analyses)

while M. domina is found on the Central Brazil and Atlantic shields and in the eastern Amazonian lowlands, with M. paraguayana on the Atlantic Shield, M. rapposa on the Central Brazil Shield and adjacent areas of Bolivia, and M. constantiae on the Central Brazil Shield, northward to the Amazonian lowlands, and in adjacent areas of Peru (Fig. 3).

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Fig. 15 The maximum likelihood (ML) topology of Thylamys showing the museum and/or field tissue-sample numbers, and the numbers of the collecting localities (in parentheses) shown on the map. The black circles in the ML topology represent 80–100% bootstrap values; the black squares, values of 79–79%; and the white squares, the bootstrap values of 60–69%. The map shows the Thylamys collecting localities, the western and eastern Amazonian lowlands, and the three shields (color-coded on the map and in the ML and MJ analyses)

Marmosops Marmosops also radiated throughout the major regions of South America, except for its southernmost extreme. The molecular phylogeny of Marmosops revealed two clades with species from the western Amazonian lowlands in both groups (Figs. 6 and 7). Overall, four Marmosops species are found in the western Amazonian lowlands, two on the Atlantic Shield, and three on the Guiana Shield. The taxonomy of this genus is not well defined (Gardner and Creighton, 2008; Nascimento et al. 2015; Díaz-Nieto et al. 2016; Díaz-Nieto and Voss 2016), and a total of 19 taxa were considered valid in the present chapter, including M. bishopi (Pine, 1981); Marmosops carri (J.A. Allen and Chapman, 1887); Marmosops caucae (Thomas, 1900); Marmosops chucha Díaz-Nieto and Voss, 2016; Marmosops creightoni Voss, Tarifa, and Yesen, 2004; Marmosops fuscatus (Thomas, 1896); Marmosops handleyi (Pine 1981); Marmosops incanus (Lund 1840); Marmosops invictus (Goldman, 1912); Marmosops juninensis (Tate, 1931); Marmosops magdalenae Díaz-Nieto and Voss, 2016; Marmosops noctivagus (Tschudi, 1845); Marmosops ocellatus (Tate, 1931); Marmosops ojastii Garcia et al. 2014; M. pakaraimae Voss et al. 2013; M. parvidens (Tate, 1931); Marmosops paulensis (Tate, 1931); M. pinheiroi (Pine, 1981); and Marmosops soinii Voss, Fleck, and Jansa, 2019. Six of these species were not included in the present analysis, however. Otherwise, species of this genus are widespread in the western Amazonian lowlands and also on the Atlantic and Guiana shields, but not on the Central Brazil Shield (Figs. 5 and 6).

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The geographic structuring of the M. bishopi populations detected in the present chapter was consistent with the results of Díaz-Nieto et al. (2016), who concluded that the Marmosops mtDNA haplogroups were genetically independent, despite their broad morphological similarities. The present results are consistent with this, showing profound structuring in the M. bishopi samples, with the sample from Peru being well separated from those from Brazil and Bolivia (Fig. 6). A similar pattern of geographic structuring was detected in M. ocellatus, with three distinct lineages, one from Peru, one from central Bolivia, and one from western Amazonia, as well as in M. caucae, with three lineages (western Amazonian lowlands, Venezuela, and Ecuador), and M. noctivagus (western Amazonian lowlands and northern Peru), M. paulensis (Serra do Mar and Serra da Mantiqueira), and M. incanus (northern and southern Atlantic Forest), each with two lineages (Fig. 5).

Metachirus The Metachirus radiation also occurred throughout the major regions of South America, except for its southernmost extreme. This genus is traditionally considered to be monospecific, with its single species, Metachirus nudicaudatus (É. Geoffroy, 1803), having a number of subspecies (Gardner and Dagosto 2008). In an unpublished thesis, Vieira (2006) recognized three of these subspecies as valid species – Metachirus colombianus (J.A. Allen, 1900); Metachirus tschudii J.A. Allen, 1900; and Metachirus modestus (Thomas, 1923) – and Voss et al. (2019) also supported the species status of Metachirus myosuros (Temminck, 1824). These studies highlight the need for a thorough review of this genus. The present molecular phylogeny of Metachirus separates the genus into two clades, one containing M. nudicaudatus and the other with the remaining taxa (Fig. 8), which is consistent with the results of previous morphological studies, which restricted the geographic distribution of M. nudicaudatus to the Guianas and eastern Amazonian lowlands (Vieira 2006) or to the Guiana Shield alone (Voss et al. 2019). The M. nudicaudatus populations analyzed here include localities on the Guiana and Central Brazil shields (Fig. 8). The second clade was subdivided into five haplogroups, which coincide partially with the original subspecies (Gardner and Dagosto 2008) and the species recognized by Vieira (2006), but not with the taxonomic arrangement proposed by Voss et al. (2019). The eastern Amazonian clade, denominated Metachirus sp. here, appears to be an undescribed species. The western Amazonian lowland clade, which includes samples from Peru and the Brazilian Juruá and Purus basins (Figs. 8 and 9), is assigned here to Metachirus sp., based on its morphological attributes. Vieira (2006) described a number of diagnostic morphological traits for these populations (in specimens identified as M. tschudii), such as the dark midline on the back and a pronounced rusty tone on the hip. However, the name M. myosuros tschudii, which type locality is Guayabamba in northwestern Peru, is here attributed to the population of north Peru and Ecuador. The results of the present chapter thus suggested the presence of two unnamed

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lineages, Metachirus sp. from western Amazonian lowlands and Metachirus sp. from the eastern Amazonian lowlands (Fig. 8). The Metachirus clade from the Atlantic Shield (including the samples from eastern Brazil) supports the species status of Metachirus myosuros, as proposed by Vieira (2006) and Voss et al. (2019), and differs from Gardner and Dagosto (2008), who classified this taxon as a subspecies. Metachirus myosuros myosuros is found along the whole eastern Brazilian coast (Patton et al. 2000; Costa 2003, Gardner and Dagosto 2008). Despite the considerable geographic distance, M. myosuros myosuros from the Atlantic Shield is more closely related to Metachirus sp. from the western Amazonian lowlands, and Metachirus sp. from the eastern Amazonian lowlands, than to the taxa found in the northeastern Central Brazil Shield (Fig. 8), as reported by Costa (2003). These results reflect the historical importance of the central Brazilian forests that once connected the marsupial populations of the Amazon and Atlantic forests and their importance for the understanding of the evolutionary history of the present-day fauna of the lowland Amazon rainforest (Costa 2003). The other clade recovered in the molecular analyses (Fig. 8) corresponded to M. myosuros colombianus with samples from Panamá and type locality in Colombia, sister clade of M. myosuros tschudii.

Monodelphis Monodelphis radiated throughout the major regions of South America, except for its southernmost extreme. This is a speciose genus, with many recently described species (Pine and Handley Jr 2008; Pavan et al. 2012, 2017; Pavan 2019), although there is no current consensus on the taxonomic status of some lineages, such as M. maraxina. The species considered valid in the present chapter include Monodelphis adusta (O. Thomas, 1897); Monodelphis americana (Muller, 1776); Monodelphis arlindoi Pavan et al., 2012; Monodelphis brevicaudata (Erxleben, 1777); Monodelphis dimidiata (J. A. Wagner, 1847); M. domestica (J. A. Wagner, 1842); M. emiliae (O. Thomas, 1912); Monodelphis gardneri Solari et al. 2012; Monodelphis glirina (J. A. Wagner, 1842); M. handleyi Solari, 2007; Monodelphis iheringi (O. Thomas 1888); Monodelphis kunsi Pine 1975; Monodelphis maraxina O. Thomas, 1923; Monodelphis osgoodi Doutt, 1938; Monodelphis palliolata Osgood, 1914; Monodelphis peruviana (Osgood, 1913); Monodelphis pinocchio Pavan, 2015; Monodelphis reigi Lew and Perez-Hernández, 2004; Monodelphis ronaldi S. Solari, 2004; Monodelphis saci Pavan et al., 2017; Monodelphis sanctaerosae Voss et al., 2012; Monodelphis scalops (O. Thomas, 1888); Monodelphis touan (Shaw, 1800); Monodelphis unistriata (J. A. Wagner, 1842); and Monodelphis vossi Pavan, 2019. The analysis of Monodelphis confirmed the monophyly of all the species represented by more than one haplotype, in an arrangement that is consistent with those presented in the previous studies (Caramaschi et al. 2011; Voss et al. 2012; Pine et al. 2013; Pavan et al. 2014). This genus has a number of endemic lineages in the regions analyzed in the present chapter (Figs. 10 and 11), in particular the

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Atlantic Shield (e.g., M. dimidiata, M. scalops, M. americana, and M. iheringi), but also in the western Amazonian lowlands (e.g., M. adusta, M. glirina, M. peruviana, and M. gardneri), Central Brazil Shield (e.g., M. maraxina, and M. sanctaerosae), Guiana Shield (e.g., M. reigi and M. touan), and eastern Amazonian lowlands (M. arlindoi). Other species, such as M. domestica, with two lineages (Caatinga and Cerrado), and M. kunsi, with three (north Argentina + South Bolivia, Central Brazil Shield, and Atlantic Shield), occur in more than one region and have geographically structured populations. These results highlight the importance of these regions in the phylogeography of the species, and of the genus, in general. The ML analysis divided M. emiliae into two clades, one in the western Amazonian lowlands and the other in the eastern lowlands, which is designated Monodelphis sp. here (Fig. 10). The MJ analysis revealed a similar pattern, with the two haplogroups being separated by 113 nucleotide substitutions, which reinforce the existence of two quite distinct lineages (Fig. 12). The population from the eastern Amazonian lowlands is thus considered here to be an undescribed species, Monodelphis sp. The MJ analyses also indicated that M. glirina from the western Amazonian lowlands and Central Brazil Shield is connected directly to M. maraxina in Central Brazil (Fig. 12). In the case of M. maraxina, there is a clear separation between the Alta Floresta haplotype (01) and all the other haplotypes (Fig. 12). The M. glirina and M. maraxina haplogroups are separated from each other by at least 66 nucleotide substitutions and two median vectors (Fig. 12), which supports the proposal of Bezerra et al. (2018) and disagrees with Pavan (2019), who considered the glirina and maraxina lineages to be a single species. The latter paper was based on a morphological analysis of the different lineages but lacked an adequate sample from the western lowlands, which may account for its conclusions (Pavan 2019). The distribution of M. maraxina, as proposed here, would include the eastern Xingu basin, Marajó Island, and the southern Amazon basin as far west as the Tapajós-Madeira interfluve (Fig. 11). The present chapter also revealed the occurrence of Monodelphis peruviana in the Brazilian state of Acre, in the municipality of Porto Acre.

Philander Philander radiated throughout the principal regions of South America, except for its southernmost extreme. This genus has 10 species, including a number that have recently been described or revalidated or considered as junior synonymous (Patton and da Silva 1998; Voss et al. 2018; Voss et al. 2020): Philander andersoni (Osgood, 1913); Philander canus (Osgood, 1913); Philander deltae Lew, Perez-Hernández, and Ventura, 2006; Philander mcilhennyi Gardner and Patton, 1972; Philander melanurus (Thomas, 1899); P. nigratus (Thomas, 1923); P. opossum (Linnaeus, 1758); Philander vossi Gardner and Ramírez-Pulido, 2020; Philander pebas Voss et al., 2019; and Philander quica (Temminck, 1824). The analysis of Philander also confirmed the monophyly of all its species, in an arrangement that is consistent with those presented in previous studies (Voss et al. 2018). The MJ analysis allocated P. opossum from the Guiana shield and the eastern

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Amazonian lowlands to a central position, connected directly to two species from the western lowlands (andersoni and mcilhennyi) and a third (canus) found in both the western Amazonian lowlands and the Central Brazil Shield (Fig. 13). This indicates the occurrence of multiple incursions into the western Amazonian lowlands (Fig. 14). Philander mcilhennyi, P. pebas, and P. andersoni are the western lowland lineages (Figs. 12 and 13). In the MJ, the majority of P. canus samples from the western Amazonian lowlands formed a distinct cluster from those of the Central Brazil Shield, except for some samples collected in neighboring areas and HPc08 (locality 42) from the southern part of the shield (Figs. 12 and 13).

Thylamys The Thylamys radiation is restricted to the subequatorial region of South America, with three species occurring on the Central Brazil Shield (Fig. 15). This genus is thought to have originated from peripheral isolates of the ancestral lineage in the foothills of the eastern Andes (Palma et al. 2002). This genus is speciose, with a number of undescribed lineages and valid species (Creighton and Gardner 2008; Martin 2009; Giarla and Voss 2010; Palma et al. 2014; ▶ Chap. 4, “Taxonomic Checklist of Living American Marsupials”): Thylamys bruchi (Thomas, 1921), Thylamys cinderella (O. Thomas, 1902), Thylamys citellus (O. Thomas, 1912), Thylamys elegans (Waterhouse, 1839), Thylamys karimii (Petter 1968), Thylamys macrurus (Olfers, 1818), Thylamys pallidior (O. Thomas, 1902), Thylamys pulchellus (Cabrera, 1934), Thylamys pusillus (Desmarest, 1804), Thylamys sponsorius (O. Thomas, 1921), Thylamys tatei (Handley, 1957), Thylamys velutinus (J.A. Wagner, 1842), and Thylamys venustus (O. Thomas, 1902). In the present chapter, species of this genus were found only on the Central Brazil Shield, which was expected, given that this genus occurs typically in semi-xeric habitats (Flores et al. 2000). The results of the analysis confirmed the monophyly of all the Thylamys species, in an arrangement that is consistent with those presented in previous studies (Carvalho et al. 2009; Palma et al. 2014).

Marsupial Lineages and Geographic Patterns Considering all the didelphimorphian genera analyzed in the present chapter, the highest species richness was recorded in the western Amazonian lowlands, in comparison with the other regions, that is, the eastern lowlands, and the Guiana, Central Brazil, and Atlantic shields (Fig. 16). Overall, 15 of the 21 species that occur in the western Amazonian lowlands are exclusive to this region, including one Marmosa (Micoureus), four Marmosops, two Metachirus, five Monodelphis, and three Philander species. These results are consistent with those of a number of previous studies, which indicated that the western Amazonian lowlands is a unique region in South America and possibly the world’s richest biological hotspot (Bush 1994; Hoorn et al. 2010).

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Fig. 16 Maps showing the western and eastern Amazonian lowlands and the three shields, with the species (circles) recorded in each region during the present chapter. The internal coloration of the circles is coded by region of occurrence, white circles are species from outside the five sampled regions. Species distributed in more than one region are shown as two or more circles (one in each region), connected by arrows

The Atlantic Shield presented the second largest number of species (n ¼ 17), of which 12 are endemic to this region, including one Didelphis, one Gracilinanus, two Marmosa (Micoureus), two Marmosops, one Metachirus, four Monodelphis, and one Philander species. The vegetation of the Atlantic Shield is composed primarily of Atlantic Forest, which is considered to be one of the hottest of the 36 global biodiversity hotspots (Rezende et al. 2018). However, the Atlantic Shield also includes a considerable area of Caatinga vegetation and some tracts of Cerrado. The gallery forest of the Cerrado has also played an important role in the connectivity of this domain with the Atlantic Forest, given that many of the taxa found in the Atlantic Forest in the gallery forests of the Cerrado (Silva 1996). The Caatinga also has a number of enclaves of humid cloud forest (“brejos de altitude”) set in the semi-arid landscape, which are sustained by orographic precipitation (Galindo-Leal

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and Câmara 2003) that may be relicts of a more ample Atlantic Forest at some time during the Pleistocene. Thirteen species are found on the Guiana Shield, of which seven are endemic, including one Didelphis, one Marmosa (Micoureus), three Marmosops, and two Monodelphis species. The Guiana highlands are known for their endemism (Catzeflis 2021) of both flora and fauna species (Hollowell and Reynolds 2005), although the number of endemic mammals is low overall. The Central Brazil Shield also had an intermediate number (n ¼ 8) of endemic didelphimorphians, including one Gracilinanus, two Marmosa (Micoureus), two Monodelphis, and three Thylamys species. The vegetation of this shield is dominated by the open formations of the Cerrado ecoregion, including extensive areas of grassland (“campo limpo”) and marsh (“campo úmido”), with herbaceous vegetation only (Eiten 1972), although the Amazon ecoregion is dominant in some areas. The diversity of the terrestrial lineages (Monodelphis and Thylamys), which are able to use open habitats, was thus expected for this region. The eastern Amazonian lowlands, the smallest of the sampled region, had a total of eight species, with three endemic forms, including one Metachirus and two Monodelphis species (Fig. 16). The connection between the Central Brazil and Atlantic shields is suggested by the distribution of four species (D. albiventris, G. agilis, M. kunsi, and M. domestica) which occur exclusively in these two regions. In this context, it is important to note that the western portion of the Atlantic Shield is covered with the Cerrado vegetation that also dominates the Central Brazil Shield. However, the analyses presented here show a clear division between the D. albiventris, G. agilis, and M. domestica populations from the two shields, which is consistent with the presence of more than one evolutionary lineage. These results are consistent with the available data on D. albiventris, which indicate a potential difference between the southern and northeastern population (Nascimento et al. 2019), the Rio São Francisco and Serra Geral de Goiás as geographic barriers to gene flow between the G. agilis populations (Faria et al. 2013), and the existence of two M. domestica lineages, one in the Cerrado + Pantanal and the other in the Caatinga (Caramaschi et al. 2011). The connection between the Central Brazil Shield and the western Amazonian lowlands was supported by the exclusive occurrence of P. canus in these two regions. A number of studies (e.g., Costa 2003; Batalha-Filho et al. 2012) indicate the existence of a corridor of dispersal for birds and mammals along the western edge of the Central Brazil Shield during much of the Miocene, which extended from the north of the present-day Chaco, in the Brazilian state of Mato Grosso, west into Bolivia and Paraguay, and north to the Brazilian state of Rondônia, creating a corridor of forest linking the Atlantic Forest (in the region of the Brazilian state of Paraná) to the Amazon Forest. The connections between the Guiana Shield and both the Central Brazil Shield and the western Amazonian lowlands were less evident, however, with a single species, M. nudicaudatus, connecting the first, and two, M. esmeraldae and M. caucae, in the latter. However, M. esmeraldae and M. caucae from the Guiana Shield and the western Amazonian lowlands, and the Metachirus nudicaudatus

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populations from the Guiana and Central Brazil shields, were structured conspicuously, which indicates that they represent more than one evolutionary lineage. These connections had already been documented by Hasui and Almeida (1985), who also postulated that, due to its location and its relative stability during the Miocene and Pliocene, the Guiana Shield played an important role in the diversification of the mammals of the Neotropical region, with the Guiana plateau both promoting endemism and acting as a geographic barrier (Lim 2012). The eastern Amazonian lowlands appear to represent an important biogeographic region, with at least three endemic species including Monodelphis arlindoi and two undescribed species of the genera Metachirus and Monodelphis. This region shares one species with the Atlantic and Central Brazil shields (Marmosa (Micoureus) limae), one (P. opossum) with the Guiana and Central Brazil shields, one (M. constantiae) with the western Amazonian lowlands and Central Brazil Shield, and two species (Didelphis marsupialis and Gracilinanus emiliae) with the western Amazonian lowlands and the Guiana and Central Brazil shields. This highlights the potential importance of this region, which has been widely overlooked in biogeographic studies. Two potential dispersal corridors linking the Atlantic Forest and the eastern Amazonian lowlands have been proposed, one along the coast of northeastern Brazil, and a second, further inland, linking the cloud forest enclaves of the Caatinga (Costa 2003; Batalha-Filho et al. 2012).

Conclusions The regions analyzed in the present chapter comprise an intricate mosaic that encompasses four major ecoregions (i.e., the Atlantic Forest, Amazon, Caatinga, and Cerrado) and a diversity of vegetation types, including forest formations, open savannas, and wetlands. The marsupial taxa and lineages analyzed here are also highly diverse and have arisen at different times since the Miocene. The earliest lineages, including Monodelphis (26.1 MYA) and Metachirus (ca. 20.2 MYA), appeared during the early Miocene, followed by lineages that arose during the middle Miocene, such as Marmosops (ca. 17.0 MYA), Marmosa (Micoureus), ca. 14.3 MYA, and Gracilinanus (ca. 13 MYA), and Thylamys (ca. 17 MYA), and the more recent lineages, such as Philander and Didelphis, from the late Miocene (Steiner et al. 2005). Jansa et al. (2013) provided a slightly different interpretation of the evidence, placing the radiations of Thylamys, Didelphis, and Philander in the Pliocene. These species also vary in their habits, with Gracilinanus, Marmosa (Micoureus), and Marmosops being arboreal and Monodelphis and Thylamys velutinus terrestrial, while the other taxa, such as Didelphis and Philander, are found in both types of habitat. These differences in habitat preferences and divergence times have led to the distinct phylogeographic patterns observed in the present chapter. Arboreal species appear to disperse less widely than terrestrial ones, with their dispersal probably being limited by the discontinuity of the canopy, as well as their type of locomotion. As habitat specialists are dependent on specific types of habitat and are thus less

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likely to traverse areas containing other habitats, they tend to disperse over shorter distances than more generalist species (Santini et al. 2012). Overall, the present results are consistent with the known contribution of landscape-level oscillations to the diversification patterns of Neotropical vertebrates (Albert et al. 2018). These oscillations are the result of the major changes that have occurred in the river drainages of northern South America, which shaped mega-wetlands over the past 15 MYA (i.e., floodplains, wetlands, and seasonally flooded savannahs) until establishing the present-day landscape (Albert et al. 2018). The results of the present chapter also indicate that the distributions of a number of species of Marmosops, Monodelphis, and Thylamys are restricted to only one of the five sampled regions, in contrast with the other genera, whose species typically have a much wider distribution. Didelphis marsupialis and Gracilinanus emiliae, for example, occur in four of the sampled regions, while Marmosa (Micoureus) limae and M. constantiae occur in three regions. All the genera, except Thylamys, have some species distributed in at least two of the sampled regions (Fig. 15), with structured populations being observed in many cases (Figs. 1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13 and 14). This emphasizes the need for further taxonomic studies to determine whether these populations are just structured geographically or do, in fact, belong to distinct evolutionary lineages.

Cross-References ▶ Taxonomic Checklist of Living American Marsupials Acknowledgments Fieldwork and laboratory analyses were supported by grants from the IOC–Fiocruz/IFAC institutional agreement, CNPq, and FAPERJ to Dr. CR Bonvicino (CNPq 304498/2014-9 and FAPERJ E26/201.200/2014 from the Oswaldo Cruz Institute), Dr. Elder Morato and Dr. Marcus Silveira (PPBio/CNPq 457540/2012-5), and Paulo S. D’Andrea (CNPq 439208/2018-1 and FAPERJ E-26/210.245/2018).

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Marsupials in the Guiana Region (Northeastern Amazonia): Diversity and Endemism

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Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Marsupials (Opossums) Occurring in the Guiana Region: An Overview . . . . . . . . . . . . . . . . . . . . . . Caluromys (Woolly Opossums) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Chironectes minimus (Water Opossum) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cryptonanus Sp. (Dwarf Opossum) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Didelphis (Common Large Opossums) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Glironia venusta (Bushy-Tailed Opossum) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Gracilinanus emiliae (Emilia’s Gracile Opossum) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Hyladelphys kalinowskii (Kalinowski’s Gracile Opossum) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Lutreolina crassicaudata (Lutrine Opossum) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Marmosa (Mouse Opossums) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Marmosops (Slender Mouse-Opossums) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Metachirus nudicaudatus (Brown Four-Eyed Opossum or Pouchless Four-Eyed Opossum) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Genus Monodelphis (Short-Tailed Opossums) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Genus Philander (Gray Four-Eyed Opossums) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Abundance of Opossums in Forested Habitats . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . The Three Small Reddish-Brown Opossums in French Guiana . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Opossums in Savannas: The Generous Contribution of the Barn Owl . . . . . . . . . . . . . . . . . . . . . . . . Opossums in Isolated Inselbergs and Elevated Rocky Outcrops . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Endemism of Didelphidae in the Guianan Shield . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cross-References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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François Catzeflis died before publication of this work was completed. François Catzeflis: deceased. F. Catzeflis (*) Emeritus Researcher. CNRS and University of Montpellier. Institute of Evolutionary Sciences, University of Montpellier, Montpellier, France e-mail: francois.catzefl[email protected] © Springer Nature Switzerland AG 2023 N. C. Cáceres, C. R. Dickman (eds.), American and Australasian Marsupials, https://doi.org/10.1007/978-3-031-08419-5_15

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Abstract

The Guiana Region occupies the northeast quadrant of Amazonia and encompasses primarily lowland rainforest, but with minor components of other habitats (e.g., savannas, marshes, and montane forests). This bioregion has an area of approximately 2.5 million km2, and its core area is composed of the Guianas sensu stricto (Guyana, Suriname, and French Guiana), the northern Brazilian states such as Amapá and Roraima, and the Venezuelan states of Amazonas and Bolívar. To date, a total of 26 species of marsupials is known from this region, ranking third in diversity after bats (ca. 150 species) and rodents (ca. 60 species). The marsupials of the Guiana Region include members of all four extant didelphid subfamilies: one species each of Glironiinae and Hyladelphinae, two species of Caluromyinae, plus 22 species of Didelphinae. By combining the results of fieldwork from four forested localities in French Guiana, an overview of species-specific abundances is based on 811 captures representing 14 species. For nonforested areas, such as savannas, opossums represented less than 10% of the remains of 642 vertebrates found exclusively in owl pellets, and most of them (35 out of 57) were the small Guianan dwarf opossum (Cryptonanus sp.). Keywords

Geographic distribution · Inselberg mountains · Pantepui endemism · Species richness · Cryptonanus · Hyladelphys

Introduction For the aims of this chapter, the Guiana Region covers an approximate area of 2.5 million km2 and is located roughly between the main channels of the Orinoco and Amazon rivers. In geopolitical terms, it includes the French overseas department of Guyane (“French Guiana”), Suriname, Guyana, Venezuela south of the Orinoco River (Bolívar and Amazonas states), and Brazil north of the Rio Negro and the lower Amazon River (northeastern Amazonas, Roraima, northern Pará, and Amapá states; Fig. 1). This area was first recognized as a biogeographic zone by Wallace (1852), and it has been consistently recognized with the same geographic limits by most subsequent zoogeographers, such as Voss and Emmons (1996) and Silva et al. (2005). The Guiana Region has one of the largest remaining tracts of intact tropical rainforest on Earth, and it has an exceptionally low human population density, with most people inhabiting the coastlines and riverine margins. Research including Didelphimorphia inhabiting the Guiana Region is fortunately sustained and continuously bringing new data on taxonomy and biodiversity of opossums. The last review by Lim (2016) listed 21 species of Didelphidae in the Guianan countries, and this chapter considers five additional taxa discovered or redefined during the 10 preceding years.

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Fig. 1 Map of the Guianan Region comprising the Guianan countries: Guyana (G), Suriname (S), French Guiana (F), and Brazilian Amapá (A). The Guiana Region as traditionally delimited by the Orinoco, the Rio Negro, and the lower Amazon amounts to ca. 2.5 million km2. The dotted line is a more restricted “Guianan subregion” east to the Rio Caura – Rio Branco and north of the Amazonian floodplain, amounting to ca. 2 million km2

Marsupials (Opossums) Occurring in the Guiana Region: An Overview Caluromys (Woolly Opossums) According to Malcolm (1990), Lim (2012), and Brito et al. (2015), sympatry of the brown-eared woolly opossum (Caluromys lanatus) with the more common and widespread bare-tailed woolly opossum (C. philander) occurs in few areas of the Guiana Region, such as in southern Guyana, near Manaus, and in the Venezuelan states of Bolivar and Amazonas. Outside of the Guiana Region, C. lanatus and C. philander are broadly sympatric in northern and central Brazil (Mato Grosso, Goiás, and Minas Gerais states), as well as in eastern Bolivia (Gardner 2007). Caluromys lanatus was the famous “micouré second ou micouré laineux” of Azara (1801), which has a very large distribution from Paraguay to Ecuador, including most of western Amazonia (Cáceres and Carmignotto 2006). A recent phylogeographic study (using the mitochondrial cytochrome-b gene) of genetic samples from widely scattered populations indicates almost no geographic structure

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for C. lanatus as opposed to some noteworthy genetic heterogeneity in C. philander (Voss et al. 2019). In the Guiana Region, both species of woolly opossums have been trapped mostly in the forest canopy and subcanopy, at heights of 5–35 m above the ground (Voss et al. 2001; Catzeflis, unpublished), and both occur in dense multistratal rainforest (mainly terra firme), as well as in mature secondary forests. Both C. lanatus and C. philander have been found infested with Trypanosoma cruzi in Guianan Venezuela and/or in French Guiana (WHO 2002). Caluromys philander has been observed to be kept as pets (mascota in Spanish) by the Sanema tribe of Amerindians along the Caura valley (Bolivar VZ: Ochoa et al. 2009). Whereas there is no published study of the ecology of C. lanatus in the Guianas, there are a few studies of C. philander, whose life traits have been examined in both secondary and primary forests in French Guiana (Atramentowicz 1995; JulienLaferrière 1997 and references therein).

Chironectes minimus (Water Opossum) The water opossum (Chironectes minimus) occurs throughout the whole of the Guiana Region, and a recent molecular (cytochrome-b gene) study by Voss and Jansa (2019) has suggested extensive gene flow and/or recent range expansion across all of the South American landscapes currently occupied by this semiaquatic species. This is in contrast with recent published evidence of population divergence from comparative analyses of craniodental morphology (Damasceno and Astúa 2016; Cerqueira and Weber 2017). The IUCN repartition map (Pérez-Hernandez et al. 2016a, b) indicates a continuous distribution throughout all four Guianan countries. Notice that in French Guiana the water opossum is the sole species of Didelphidae which is strictly protected by the law (Hansen and Richard-Hansen 2007).

Cryptonanus Sp. (Dwarf Opossum) A still undescribed species of Guianan dwarf opossum (genus Cryptonanus) is to be found in nonforested areas such as savannas, either grassy savannas or savannas intermixed with bushes and/or isolated trees. Recent collecting efforts in the savannas of Amapá and French Guiana have discovered the presence of this tiny and still-undescribed species (da Silva et al. 2013; Baglan and Catzeflis 2016). Thanks also to the examinations of owl pellets from coastal French Guiana, this elusive taxon was found in nine localities characterized by a cerrado-like environment, living together with the few other small nonvolant mammals found in that threatened habitat (Stier et al. 2020). The discovery of Cryptonanus north of the Amazon River considerably expands its known distribution; the nearest known

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samples of the species C. agricolai are some 1200 km to the south, in the Brazilian state of Tocantins (Bezerra et al. 2009).

Didelphis (Common Large Opossums) The two species of Didelphis inhabiting the Guiana Region are the common and widespread northern black-eared opossum (Didelphis marsupialis Linné, 1758) and the less abundant Guianan white-eared opossum (D. imperfecta Mondolfi and PérezHernández, 1984). Until recently, the Guianan smaller-sized white-eared opossum was known as D. albiventris albiventris, as in the publications of Adler et al. (2006), Catzeflis et al. (1997), or Voss et al. (2001). However, D. imperfecta was split from D. albiventris based on morphological data analyzed by Lemos and Cerqueira (2002) and Ventura et al. (2002). Both taxa have been found sympatrically in primary rainforests in a few sites throughout the Guiana Region, but D. imperfecta seems to be the less abundant species based on the numbers of individuals encountered during a faunal-rescue operation in French Guiana, where only 41 D. imperfecta were captured as compared with 200 D. marsupialis from February 1994 to March 1995 (Catzeflis et al. 1997). Also, in Brazilian Pará, D. imperfecta seems less abundant than sympatric D. marsupialis (Faria and Melo 2017). In Suriname, 40 Didelphis individuals from 12 localities preserved as skins all had “intensely black ears” (Husson 1978: pages 32 and 33). Although often found in lowland habitats, specimens of D. imperfecta have been caught at elevations as high as 2550 m in Cerro Marahuaca, in the Venezuelan state of Amazonas (Faria and Melo 2017). As elsewhere in the rainforested lowland Neotropics, populations of Didelphis can undergo fluctuations in numbers and occur at very low abundances in some areas at certain times. A fortuitous example concerns D. imperfecta in French Guiana: at Paracou (near the town of Sinnamary), none was caught or observed during four long and intense field sessions from 1991 to 1994 (Voss et al. 2001), whereas a few years later a field team sampling during 4 months in 2001 (Adler et al. 2006) caught both species of Didelphis at almost the same frequency (44 D. imperfecta and 39 D. marsupialis).

Glironia venusta (Bushy-Tailed Opossum) The bushy-tailed opossum (Glironia venusta) ranges across much of Amazonia, but it remains known from only a few specimens (Ardente et al. 2013; Voss et al. 2019). In the Guiana Region, there is only a single recent observation (documented with convincing photographs) from the southern part of French Guiana (Mont Itoupé: Sant and Catzeflis 2018). Either G. venusta is extremely rare in the Guianas, or else this species does not enter traps set on the lower canopy, unlike other arboreal opossums, such as the similar-sized Marmosa demerarae, with more than 150 captured specimens from four French Guianan localities (see Table 1).

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Table 1 Numbers of opossums caught in four forested localities in French Guiana. Species are listed by alphabetical order; see details in the text. Sampling effort is the product of traps x nights and of buckets x nights (for pitfalls used at Paracou and at Nourages). Forest type is indicated. Total mammals caught is for all small nonvolant (907 rodents and 811 opossums) mammals. Percent (%) Didelphidae with regard to “total mammals caught.” Marmosa lepida is indicated by (x) for Paracou, as it is present at that locality but was neither caught by Voss et al. (2001) nor by Adler et al. (2012)

Sampling effort Total mammals caught Caluromys philander Chironectes minimus Didelphis imperfecta Didelphis marsupialis Gracilinanus emiliae Hyladelphys kalinowskii Marmosa demerarae Marmosa lepida Marmosa murina Marmosops parvidens Marmosops pinheiroi Metachirus nudicaudatus Monodelphis touan Philander opossum % Didelphidae

Paracou (Sinnamary; primary) 30,347 494 19 3 50 60 1 2 60 x 10 10 19 16 1 18 54.5

Tigre (Cayenne; secondary) 15,636 566 17

Nouragues (Regina; primary) 27,607 395 16

Cacao (Roura; secondary) 16,662 263 1

78

32

15

62 146

4 67 66.1

2 16 1 14 5 4 13 1 16 30.4

14 1 3 8 1 5 18.3

Gracilinanus emiliae (Emilia’s Gracile Opossum) The attractive G. emiliae is an uncommon tiny marsupial with a very wide distribution in Amazonian Brazil and Peru (Voss et al. 2019). Gracilinanus emiliae is known from ten localities throughout the Guianan countries: two locations in Amapá, three in Guyana, three in French Guiana, and two in Suriname. As an anecdote, five out of the six animals collected in French Guiana have been caught by hand when spotted by naturalists along concrete roads (the sixth animal was shot perching in dense secondary growth at Paracou: Voss et al. 2001).

Hyladelphys kalinowskii (Kalinowski’s Gracile Opossum) Hyladelphys kalinowskii has a large and highly contrasted black mask, extending behind the eyes to the base of the ears, and a completely self-white ventral pelage: its portrait is almost unmistakable, as illustrated in an animal caught near a wooden lodge in French Guiana (Fig. 2). With the recent study of Catzeflis (2018), H. kalinowskii is known in 15 localities of the Guiana Region: 1 in Guyana, 11 in French Guiana, and 3 in Amapá (IEPA collections at Macapá). In French Guiana,

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Hyladelphys has been found in various habitats, from pristine primary forests to highly degraded secondary forests – most animals (16 out of 18 individuals) have been observed and/or caught opportunely by hand, and only two have been caught in traps (pitfall traps: Voss et al. 2001). There are at least three observations of Hyladelphys occurring in a human habitation, the most astonishing being in the folded hammock of an Amerindian in the Wayampi village of Trois-Sauts (upper Oyapock).

Lutreolina crassicaudata (Lutrine Opossum) The lutrine opossum (L. crassicaudata; also known as the thick-tailed opossum) is known from very few localities in the central and western parts of the Guianan Shield: see map in Flores and Martin (2016). Lutreolina crassicaudata has a disjunct distribution in South America occupied by two subspecies. In the Guiana Region, the lutrine opossum is only known from Guyana, the Venezuelan states of Bolivar and Delta Amacuro, and Suriname. In Guyana, L. crassicaudata is only found in savannas (llanos), tropical grasslands, and dry pastures, and it is almost always noted near water courses, riparian vegetation, and gallery forests.

Marmosa (Mouse Opossums) According to the classification of Voss et al. (2014), in which Micoureus is ranked as a subgenus, the genus Marmosa includes four species that occur in the Guiana Region: M. demerarae, M. lepida, M. murina, and M. tyleriana.

Fig. 2 Portrait of a Kalinowski’s gracile opossum (Hyladelphys kalinowskii), which was caught by the domestic cat of a lodge in suburban secondary forest near Cayenne (French Guiana), on 15 March 2016. (Thanks to Loïc Epelboin (owner of the cat) and to Christian Marty (photographer) for this delightful portrait)

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Tyler’s opossum M. tyleriana is one among only seven mammals endemic to the Pantepui Highlands (Lew and Lim 2019), and it is known from just three highland localities spanning 1300–2100 m above sea-level; M. tyleriana is the sister taxon to a clade of three species from the surrounding Amazonian and Guianan lowlands (Gutiérrez et al. 2010). The little rufous mouse opossum (M. lepida) has been found in a dozen localities of the Guiana Region. Marmosa lepida is either very rare or reluctant to enter traditional traps, as exemplified by the Paracou (French Guiana) case: Voss and colleagues never caught this species despite abundant sampling efforts from 1991 to 1993: ca. 6000 trapnights by conventional trapping and ca. 2700 bucket-nights by pitfall trapping (Voss et al. 2001); Adler et al. (2012) spent a considerable effort (9700 trap-nights) with appropriate-sized Sherman traps in 2001 and caught 70 small-sized opossums representing five species, but no M. lepida. Ironically, three individuals of M. lepida had been caught at the very same locality of Paracou in March 1989 and June 1990 by G. Dubost and O. Henry (specimens in the Paris museum, MNHN), making this locality the only one known to us throughout the Guianas with all three taxa of small, reddishbrown opossums: G. emiliae, H. kalinowskii, and M. lepida. Marmosa demerarae (previously known as M. cinerea demerarae) and M. murina are quite common species with a very large distribution throughout the Guiana Region. The woolly mouse opossum M. demerarae and the murine opossum M. murina occur in sympatry across most of their range throughout the Guiana Region; however, they are generally not syntopic in that M. demerarae is more abundant in the canopy of primary and secondary forest, whereas M. murina is scansorial and appears to be more abundant in lower forest strata and/or in secondary forests. A study by Byles et al. (2013) of the composition of helminth endoparasites in these two taxa living in eight localities of French Guiana indicated (a) a rather high species richness (12 and 14 species of helminths) and (b) a sharing of 12 species of endoparasites, suggesting that the differences in foraging behavior and habitat between M. demerarae and M. murina were not so large as to prevent sharing of most (86%) of their endoparasites.

Marmosops (Slender Mouse-Opossums) Four species of slender mouse opossums (Marmosops) are known in the Guiana Region: M. caucae, M. pakaraimae, M. parvidens, and M. pinheiroi. Neblina’s slender opossum (Marmosops caucae: a name replacing M. neblina, which is a junior synonym) has an isolated locality on Cerro Neblina (Amazonas, Venezuela). With regard to the general distribution of M. caucae, the Cerro Neblina locality is a remarkable outlier, some 850 km east from the nearest localities in the Cordillera Oriental, Colombia: see map on Fig. 1 in Díaz-Neto et al. (2016:923). The Marmosops taxon with the smallest distribution is certainly the Pantepui slender opossum M. pakaraimae (recently described by Voss et al. 2013), known from five localities, of which three are in the Pakaraima Highlands of western Guyana and two are in the adjacent highlands of eastern Venezuela. Recorded elevations at these localities range from 800 to about 1500 m above sea level. As

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shown through molecular studies, M. pakaraimae is the sister species to Marmosops parvidens from the immediately adjacent Guianan and eastern Amazon lowlands (Voss et al. 2013; Díaz-Neto et al. 2016). The delicate slender opossum M. parvidens and Pinheiro’s slender opossum M. pinheiroi are from the Guianan lowlands, where they are both widely distributed. In French Guiana and Suriname, six localities are known where more than three individual slender mouse opossums have been caught, and five of these localities document both species in sympatry. For these two countries, M. parvidens appears more common than M. pinheiroi, with respectively 55 and 31 specimens in collection. The abundance of both Marmosops is still better known in Brazilian Amapá: there are ten forest localities where at least three Marmosops individuals have been caught (pers. comm. of Claudia Regina da Silva: 21 February 2020), and nine of these localities have evidenced both species in sympatry. And, still in forested locations of Amapá, M. parvidens (130 collected specimens) seems much more abundant than M. pinheiroi (61 specimens) in lowland rainforests.

Metachirus nudicaudatus (Brown Four-Eyed Opossum or Pouchless Four-Eyed Opossum) Brown four-eyed opossums M. nudicaudatus are quite common terrestrial didelphids in forested areas throughout the Guiana Region. A recent phylogeographic survey (Voss et al. 2019) suggests that M. nudicaudatus is endemic to northeastern Amazonia (French Guiana, Guyana, Surinam, and Brazilian Amapá) whereas other geographic samples of Metachirus from southwestern Amazonia, northwestern Amazonia, and the Atlantic Forest belong to another species, namely, M. myosuros (Temminck, 1824).

Genus Monodelphis (Short-Tailed Opossums) There has been much taxonomic change in Monodelphis during the 20 previous years, and four species are today recognized throughout the Guiana Region. Their general relationships and distribution are appropriately addressed by Pavan et al. (2012; see also ▶ Chap. 15, “Short-Tailed Opossums Genus Monodelphis: Patterns of Phenotypic Evolution and Diversification,” by Pavan, this volume). Arlindo’s short-tailed opossum Monodelphis arlindoi is a poorly known species recently described from central-south Guyana and in southeastern Roraima to eastern Amazonas and northern Pará (Brazilian regions north of the Amazon River; Pavan et al. 2012). The Guianan short-tailed opossum Monodelphis brevicaudata was previously thought to be the sole species in the Guiana Region (as per Solari 2010) although Voss et al. (2001) emphasized the variability of external characters in Guianan Monodelphis, and suspected that M. touan might be a separate species, pending

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further examinations; M. brevicaudata occurs in northern Guyana and in the Venezuelan state of Bolivar. The red-legged short-tailed opossum Monodelphis touan, also recently resurrected from synonymy with Monodelphis brevicaudata by Pavan et al. (2012) based on molecular and morphological analyses, is to be found in French Guiana, Brazilian Amapá, and eastern and southeastern Pará (on the right – southern – bank of the Amazon River). The fourth species of short-tailed opossum is Reig’s opossum M. reigi, which is only known from two localities in Guyana and one locality in Venezuela; thus, M. reigi is restricted to the Pakaraima Highlands and immediate vicinity. Pavan et al. (2016) showed that M. reigi diverged during the early Pleistocene (2.4 million years ago) from its sister species Monodelphis adusta and other closely related taxa from the western Amazonian lowlands; thus, its sister taxa are not any of the three Guianan species (M. arlindoi, M. brevicaudata, or M. touan). Monodelphis brevicaudata, M. arlindoi, and M. touan belong to the same phylogenetic clade and are distributed in adjacent lowland rainforest of northern Brazil and of the Guianan Shield, as shown in the map on Fig. 6 in Pavan et al. (2012: 201). Thus, these 3 taxa are allopatric or, at most, parapatric.

Genus Philander (Gray Four-Eyed Opossums) A recent revision of Philander has been published by Voss et al. (2018), and it appears that three species occur in the Guiana Region. Of these, Anderson’s foureyed opossum Philander andersoni (Osgood, 1913) and the gray four-eyed opossum P. canus (Osgood, 1913) (which includes P. mondolfii Lew et al., 2006, a junior synonym) are found in sympatry in the Venezuelan state of Amazonas, whereas the common four-eyed opossum P. opossum (Linnaeus, 1758) is the sole species of the genus in Guyana, French Guiana, Suriname, Amapá, and northern Pará. Note that P. mondolfii (one of several junior synonyms of P. canus: see above) was known from two separate areas: (1) northeastern and northwestern sectors of the piedmont hill systems that are found between the Venezuelan Guiana Shield border and the Orinoco River; (2) the foothills on the eastern slopes of the Cordillera Oriental of Colombia, and foothills of northern and southern slopes of Cordillera de Mérida (Venezuela) (Lew et al. 2006; IUCN 2016).

Abundance of Opossums in Forested Habitats In French Guiana, a few field sessions with comparable sampling designs have been made by various students, and this chapter uses these data to allow a contrast to be made between four forested localities. The four localities are the following: Paracou (municipality of Sinnamary), as described by Simmons and Voss (1998) and Voss

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et al. (2001), being mainly primary well-drained rainforests; Camp du Tigre (municipality of Cayenne), a peri-urban hill of mature secondary forests, similar to the Cabassou locality described by Julien-Laferrière and Atramentowicz (1990); Nouragues (municipality of Regina), being mostly primary rainforests around the scientific station, as per the description of Charles-Dominique (2001); and Cacao (municipality of Roura) with mostly well drained old secondary forests, bordering an agricultural landscape. Samplings were done with more or less standard methods and equipment (Sherman and Tomahawk live traps deployed at ground level, wiremeshed traps set on trees at 2–3 m heights; pitfalls in well-drained terra firme forests in the localities of Paracou and Nouragues). The numbers of encountered species of Didelphidae range from 14 (Paracou) to 6 (Camp du Tigre), and the two localities where pitfalls have also been used (Paracou and Nouragues) have more species than the two localities with only traps in use (Table 1). Six taxa have been caught in all four localities: Caluromys philander, Didelphis marsupialis, Marmosa demerarae, M. murina, Monodelphis touan, and P. opossum, whereas four species have been encountered in only one locality: Chironectes minimus, Didelphis imperfecta, Gracilinanus emiliae at Paracou, and Marmosa lepida at Nouragues. The most abundant(a) species is Didelphis marsupialis, well represented in each locality. Then Marmosa murina and M. demerarae are also abundant but notice that M. murina is extremely abundant in only one locality (Camp du Tigre, a mature secondary forest bordering the city of Cayenne). Thus, the three most abundant species altogether comprise 63% of all 14 species of encountered Didelphidae (811 specimens). Philander opossum is the fourth well-represented taxon (13%), followed by Caluromys philander (7%). The sixth ubiquitous species, Monodelphis touan, is rarely caught (from one to four individuals per locality). As suggested by Voss et al. (2014:19), the genus Marmosa appears to be the dominant clade of small insectivorous-frugivorous arboreal opossums throughout most of the forested Neotropical lowlands, and this is also the case in the four French Guianan forested localities. The interpretation of “abundance” necessitates some caution as current numbers are based on specimens collected in traps, not on actual census results. Therefore, it is not possible to distinguish abundance from trappability, being alluded in the text that quite a few species of opossums (such as G. venusta, G. emiliae, M. lepida . . .) might be trap-reluctant.

(a)

As a member of a larger guild of small (up to 2 kg) nonvolant mammals (including rodents – sigmodontines, echimyids, and sciurids –), the opossums comprise between 18% (Cacao) and 66% (Camp du Tigre) of all nonvolant small mammals having entered the traps and/or pitfalls in those four localities.

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The Three Small Reddish-Brown Opossums in French Guiana Among the small marmosines, there are three superficially similar species in the Guiana Region, all of which are very small (850 mm, which generally means higher altitudes (Jones et al. 2003). In Tasmania, however, Spotted-tailed Quolls occupy a wide range of rainfall zones and vegetation types, from 450 mm on the east coast to 3000 mm in the southwest, and actually reach their highest densities in open grassy woodlands and fragmented lowland farmland (Hamer et al. 2022). The threatening force driving this mainland – Tasmanian difference may be a combination of direct predation of quolls and competition for medium-sized native and invasive (European Rabbit Oryctolagus cuniculus) prey by the invasive European Red Fox which is widespread on the mainland and absent in Tasmania.

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Another classic relictual species on mainland Australia is the Mountain Pygmy Possum Burramys parvus, now restricted to boulderfields at altitudes >1400 m in three separate alpine and sub-alpine regions of south-eastern Australia. Based on fossil evidence of several species of Burramys inhabiting wet forest environments in the Pleistocene, it is hypothesized (Broome et al. 2012) that during one of the four interglacial warm periods, rainforests, with populations of ancestral Mountain Pygmy Possums, extended to the highest altitudes in south-eastern Australia. With the onset of the next cold and dry glacial interval, the rainforest contracted into the warmer, wetter lowlands leaving behind stranded populations of the Mountain Pygmy Possum. As the high-altitude rainforest vegetation in New South Wales and Victoria subsequently changed to cold-adapted open woodlands and shrublands, the open framework of the boulder piles in these areas enabled the resilient possums to survive the retreat of the rainforest and the onset of an alpine climate. Their current ability to hibernate to survive the wintry conditions is inherently present in burramyids in general. Subfossil material found in lowland cave deposits indicates a formerly much wider distribution. The limited available habitat has consequently restricted numbers of the Mountain Pygmy Possum to less than 2000 adult individuals across its entire distribution. Some bioregions, such as the Jarrah Forest in southwest Western Australia, harbor multiple species with relictual niches, possibly because these areas still provide sufficient structurally complex habitat to allow species persistence in the face of invasive predators and other threats. The Jarrah Forest is located east of the Swan Coastal Plain on an inland plateau with the Darling scarp forming the western boundary and at the southeastern end includes the Blackwood Plateau and further east the Stirling Ranges. The bioregion is divided into two sub-regions, Northern Jarrah Forest (1,898,799 hectares), and Southern Jarrah Forest (2,610,275 hectares). The region is dominated by Jarrah Eucalyptus marginata and Marri Corymbia calophylla. Wetland vegetation in the southeast is dominated by paperbarks and the eastern forest is predominantly wandoo woodland, of Wandoo Eucalyptus wandoo. While upland areas are species-rich, the drier inland is less so. Heath is a common understorey of the Jarrah forest in the north and east. Jarrah Forest bioregion supports 29 mammal species including marsupials such as the Numbat, Gilbert’s Potoroo, Western Quoll, Brush-tailed Bettong, Tammar Wallaby, Western Ring-tailed Possum, Common Brush-tailed Possum, Quenda, and Red-tailed Phascogale Phascogale calura. Most of these were once widespread but are now limited to the fragmented portions of Jarrah Forest (Burrows and Christensen 2002).

Isolation Slows but Does Not Eliminate Declines The island state of Tasmania has been separated from the continental mainland of Australia since rising sea-levels about 13,000 years ago flooded the Bassian Plain linking Tasmania with the southern mainland of Victoria (Lambeck and Chappell 2001). This island “moat” has functioned to keep out some threats that have caused extinctions on the Australian continent, notably the Dingo and the European Red

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Fox. All of the extant and recent mammal fauna of Tasmania have, or previously had, distributions that included the temperate southeastern mainland. The Thylacine and the Tasmanian Devil became extinct on the mainland around 3000 years ago possibly resulting from a synergy of declines consequent to a protracted period of El Nino drought, the introduction of the Dingo which was similar in size to the mainland Thylacine, and proposed increased competition from increasing human density (Brüniche-Olsen et al. 2018). The approximately simultaneous extinction of both species on the mainland was associated with a sharp decrease in genetic diversity, strongly supporting a role for climate (Brüniche-Olsen et al. 2018; White et al. 2017). The Thylacine is officially classified as Extinct, with the last confirmed wild individual killed in 1933. Causes are still debated, with persecution facilitated by a bounty for accused sheep killing probably representing a sustainable harvest rather than a causation, and a hypothesis of a distemper-like disease that was also reported in the early 1900s to decimate quoll populations unconfirmed (McCallum and Dobson 1995). Other species, which are now considered to be Tasmanian “endemics” are actually the remaining extant populations from once wider distributions including Tasmania and the mainland. These species, Eastern Quoll, Rufous-bellied Pademelon, and Eastern Bettong, disappeared from mainland Australia probably mostly due to fox predation over the first 150 years of European occupation (Woinarski et al. 2014). Tasmania has not escaped mammal species declines and a possible extinction, though, the most notable being the now 80% total population decline of the Tasmanian Devil from a novel transmissible cancer, which arose in the late 1980s and has now spread across most of the species island-wide range (Cunningham et al. 2021) (Fig. 4). The Devil is listed as Endangered at state and IUCN levels although studies demonstrate rapid evolution in response to the extreme selection pressure placed upon the species by high mortality from the disease, with genomic changes relevant to fighting cancer (Epstein et al. 2016). No populations have become extinct and population decline is expected to at least level out in the next decade (Cunningham et al. 2021) as the disease has now transitioned from being an epidemic to an endemic disease (Patton et al. 2020). The only likely mammal extinction in the main island of Tasmania in the last 200 years, aside from the Thylacine, is a rodent, the New Holland Mouse Pseudomys novaehollandiae, with surveys failing to reveal this species since about 2000 (Lazenby 2009), although it has recently been found on Flinders Island. Species which are showing ongoing decline are those with distributions in the drier eastern part of Tasmania that occupy open grasslands and grassy woodlands where cat density is extremely high, among the highest in Australia (Hamer et al. 2021). Of most concern are the Eastern Quoll (Cunningham et al. 2022) and Eastern Barred Bandicoot Perameles gunnii. Causes of declines of these species could be a combination of warming and drying climate and loss of structurally complex low vegetation important as refuge from cats, which have increased particularly with the decline of Tasmania’s top predator, the Tasmanian Devil (Fig. 4).

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Fig. 4 Case study: Emerging Infectious Disease causes severe top predator loss and triggers community-wide changes in the Tasmanian marsupial fauna. The severe disease caused population decline of Tasmanian Devils (a), the top predator and scavenger (b) in Tasmanian ecosystems, has triggered community-wide changes in the behavior and abundance of Tasmanian marsupials. Devils are demonstrated to effectively suppress populations of two of the world’s most destructive invasive alien species, the feral Cat and the Black Rat. With the effective loss of the functional role of devils at 90% local declines, cat abundance has increased and is contributing to decline in bandicoots (c) and Eastern Quolls (d) (Cunningham et al. 2020). Experiments in which carcasses were placed in the landscape across the devil decline gradient show that the alien cat behaviorally avoids devils when they are at high density but carrion feeding by the native spotted-tailed quoll, which has coevolved with devils, is affected only by the amount of carrion that the large and more dominant devil first removes. Quolls and some native herbivores also alter the time of night of their peak activity to avoid devils at high density and relax to become active earlier in the night when devils are declined. In the absence or low density of devils, the arboreal brushtail possums forage on the ground much further from the protection of trees, which would influence plant growth and seedling recruitment. (Images: Menna Jones (a, b, d) and Bridgette Barnden (c))

Management Stems Loss and Improves Retention of Marsupial Species The Upper Warren region, 300 km south of Perth, between Manjimup, Bridgetown, and Lake Muir, includes 140,000 ha of eucalypt forest and woodland and is notable for its retention of many threatened mammal species including 15 marsupials that have undergone broad-scale and severe declines elsewhere (e.g., Numbat, Western Ring-tailed Possum, Brush-tailed Bettong, and Tammar Wallaby), but some mammal species were locally extirpated (e.g. Greater Bilby, and Burrowing Bettong) in the twentieth century (Ian Wilson pers. comm., Abbott 2001).

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Long-term monitoring (>40 years) of mammals since 1974 has been conducted in the region (Wayne et al. 2017). During the late 1970s and 1980s, numbers of Brush-tailed Bettongs increased steadily after a translocation within the region and the start of fox-baiting for fauna conservation in targeted areas in 1977 (Burrows and Christensen 2002). Most other native mammals were uncommon until fox control was greatly increased in frequency and extent between 1992 and 1996. However, after 1995 six native marsupial species declined severely and successively, with dunnarts (Sminthopsis spp.) and Brush-tailed Phascogale declining from 1995, Quenda from 1996, Western Ring-tailed Possum from 1999, Brush-tailed Bettong from 2000, and Western Brush Wallaby from 2006 (Wayne et al. 2017). Three species increased: Common Brush-tailed Possum since 2000, Western Quoll since 2003, and Tammar Wallaby since 2006, with the latter increase due mostly to translocations within the area. The declines are of particular concern given that the area is in conservation reserves, in which many threats (notably habitat loss and hunting) that have affected mammal assemblages elsewhere in Australia and the world are excluded. Furthermore, the area has had management aimed at the control of some putative threatening factors. There is a strong role of predation by European Red Fox in driving species’ declines, with evidence of at least temporary increases of some native mammals following fox control (Possingham et al. 2004). There was no apparent association with fire regimes for the Brush-tailed Bettong or other species. Although climate impacts were found, e.g., drought impacts on Brush-tailed Phascogale (Rhind and Bradley 2002), no recovery has been evident in subsequent wetter years. Vegetation degradation due to P. cinnamomi was not highly significant; although present it was limited in extent within the study area where declines have been more pervasive. There was evidence of impacts of timber harvesting on sensitive species such as Western Ring-tailed Possum (Wayne et al. 2006) and Brush-tailed Phascogale (Rhind 2004) but not the Brush-tailed Bettong (Wayne et al. 2016); however, little of the study area was exposed to this factor. Predation by the Domestic Cat is hypothesized as the most likely common or primary cause behind many of the recent declines in the Upper Warren. The integrated reduction of both cats and foxes, conducted within an experimental framework, is the most direct and definitive action to test this and deliver the greatest practical conservation outcomes.

Changing Climate Australia is already experiencing the impacts of climate change (CSIRO and BOM 2022). Since 1910, Australia’s climate has warmed by approximately 1.4  C, leading to an increase in the frequency of extreme heat events. Warming has occurred in all months, with temperatures increasing for both day- and night-time, and there is a greater frequency of very hot days in summer. The warmest year on record was 2019, and the 7 years from 2013 to 2019 among the 9 warmest years. Long-term trends in rainfall are evident in some regions with the southwest and southeast experiencing

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drier conditions, with more frequent years of below average rainfall, especially in the cool months of April to October. There has been an increase in extreme fire weather and in the length of the fire season across large parts of Australia since the 1950s. Climate change is contributing to these changes in fire weather by affecting temperature, relative humidity, and associated changes to the fuel moisture content. Considerable year-to-year variability in fire weather also occurs and La Niña years are associated with wet and cool climate anomalies and a lower number of days with high fire index values. There is a significant trend in southern Australia towards more days with weather conditions conducive to extreme bushfires. The impacts of climatic change are demonstrated in a variety of ecosystems and communities around the world (Hughes 2000). The changes to the Australian climate pose significant threats to vulnerable marsupial species, especially in fragmented ecosystems. Climate change can affect species both directly and indirectly. Climatic conditions such as temperature may act directly by exceeding a species’ physiological tolerance range (St. Clair and Gregory 1990). Conditions may limit food resources or disrupt reproduction and completion of life cycles (Parmesan et al. 2000). Long-term changes in climatic conditions can gradually lead to decoupling of feeding and reproduction cycles (Winder and Schindler 2004) and shifts or reductions in species’ distributions and abundances (Foden et al. 2007).

Bioclimatic Niche and Susceptibility A suite of traits that makes a species vulnerable to disturbance generally will also dispose them to risk from climate change (Steffen et al. 2009). Species most at risk include: (a) species with narrow physiological tolerance to factors such as temperature or water availability; (b) specialized species with narrow habitat requirements such as reliance on particular abiotic or habitat features; (c) geographically localized species including those that have been reduced to small, isolated habitats; (d) genetically impoverished species with low genetic variability that are less likely to have the genetic diversity; (e) species with a poor ability to disperse, with long generation times, time to sexual maturity, or complex life histories (e.g., male “die-off ” in Antechinus spp. and Phascogale spp.); (f) populations located on the periphery of the range of a species that contracts in response to climate change; and (g) montane and alpine species, typically composed of small and isolated populations and possibly with nowhere to migrate as their habitats retreat uphill in response to climatic warming. Some of the earliest work on climate change impacts in south-eastern Australia examined the potential effect of climate change on the distribution of fauna species considered most at risk in the forests and heathlands of the major Victorian bioclimatic regions. These species included five threatened marsupial species (Swamp Antechinus, Southern Brown Bandicoot, Leadbeater’s Possum, Long-footed Potoroo, and Mountain Pygmy Possum) (Brereton et al. 1995). Information regarding faunal distributions and predictive models for bioclimatic ranges was used in

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conjunction with the accepted enhanced greenhouse climate scenarios for 1990. Species in near-coastal habitats were identified as sensitive to climate change. The bioclimate of the Mountain Pygmy Possum’s range is very sensitive and would not persist with a 1  C rise in temperature. The response of the Swamp Antechinus in coastal western Victoria and south-eastern South Australia was significant, with the bioclimatic range declining by 90–100% at +2  C. In comparison, the bioclimate of the Southern Brown Bandicoot appeared to be more tolerant of climate change, persisting to +3  C with a decline of 51–89%. For Leadbeater’s Possum, the least area of bioclimatically suitable habitat occurred under a scenario which takes into account changes in the seasonality of rainfall and is more complex and hence less reliable to predict. A recent species-level assessment of climate change vulnerability for a sample of Australia’s threatened species mapped the distributions of species affected by main factors driving climate change vulnerability: low genetic variation, dependence on a particular disturbance regime, and reliance on a particular moisture regime or habitat (Lee et al. 2015). Climate change vulnerability index values for the species assessed ranged from 11.3 (extremely vulnerable) for the Mountain Pygmy Possum to 5 (low vulnerability) for the Western Quoll. The Mountain Pygmy Possum is the only Australian mammal confined to the Australian Alps bioregion and is dependent on winter snow cover and cool temperatures (Broome et al. 2012). It has undergone a significant range contraction since the last glacial maximum when it occurred throughout most of southeastern Australia and is now further threatened by habitat loss, habitat degradation, predation by invasive cats and foxes, small population sizes and loss of genetic diversity, and climate change. The Mountain Pygmy Possum has a specialist diet predominantly consuming Bogong Moths Agrotis infusa, a long-distance seasonal migrant, and seeds of Podocarpus lawrencei (Gibson et al. 2018). Analyses of the diet revealed strong seasonal and climatic influences on these dominant food resources, providing further evidence of the species’ susceptibility to climate change. Selective foraging for the lipid-rich Bogong Moths and Podocarpus seeds suggests that they provide important health and survival benefits for these pygmy possums. It has been proposed that given their dependence on cooler, higher-elevation aestivation sites, Bogong Moths may experience reduced survival in a warmer world. Further, climate change across the vast migratory route of the moth is likely to further affect its survival and availability for consumption by the Mountain Pygmy Possum (Gibson et al. 2018). There have been recent observations of population crashes of the Bogong Moths linked to climate change and recent droughts in areas where the moths breed. These declines have put extra pressure on the endangered Mountain Pygmy Possum. Alpine species and habitats in general may be more at risk because of the limited options for adjustment of the geographic distribution in response to a changing climate. The early bioclimatic modelling of Brereton et al. (1995) predicted extinction of the Mountain Pygmy Possum with a 1  C rise in temperature, and given the species’ current restricted distribution, it remains to be seen whether the species will survive in coming decades (Gibson et al. 2018).

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At the other end of the vulnerability scale is the Western Quoll, a generalist species in its dietary and habitat requirements. Despite a severe range contraction because of habitat clearance and predation from introduced feral species, the Western Quoll has a high dispersal capacity and the greatest genetic variation of all quoll species (Gibson et al. 2018). Lee et al. (2015) found that climate change vulnerability increased greatly as geographic range size declined. This can be due to threatened species already having been impacted by habitat loss restricting them to small fragments of their former range, population declines, and low genetic variation. Alternatively, some life history traits associated with high climate change vulnerability are also related to narrow geographic range size. Identification of species most vulnerable to climate change can assist prioritization for urgent actions to protect and assist these species (Lee et al. 2015).

Species Affected by Temperature Changes Southern Greater Glider The Southern Greater Glider, Australia’s largest gliding marsupial, is widely distributed along the eastern coast, but has recently experienced drastic declines in population numbers. It has a strong association with hollow-bearing trees, used for nesting, and the availability of hollows is reduced by fires and timber harvesting (Wagner et al. 2020). The species has, however, disappeared from areas that have experienced neither. The Southern Greater Glider has a unique physiology and strict diet of Eucalyptus foliage that makes it vulnerable to high temperatures and low water availability. It has been suggested that climatic conditions may be significant for habitat selection, and recent climatic trends may be contributing to the observed declines (Wagner et al. 2020). Analyses of the influence of climatic, topographic, edaphic, biotic, and disturbance variables on occupancy and habitat suitability of the Southern Greater Glider found that climatic variables, particularly those related to aridity and extreme weather conditions, such as number of nights warmer than 20 C, were highly significant predictors of Southern Greater Glider occurrence (Wagner et al. 2020). Climate and habitat suitability have changed over time, with increasing aridity across much of the species southern distribution closely associated with observed population declines. In some areas at higher elevation, conditions have become wetter, and the Southern Greater Glider is still recorded at high densities. These areas will become increasingly important as climatic refugia in the coming decades (Wagner et al. 2020). Western Ring-Tailed Possum The Western Ring-tailed Possum is a medium-sized arboreal marsupial that is critically endangered (Environment Protection and Biodiversity Conservation Act 1999) and has retracted to habitat fragments in the Swan Coastal Plain bioregion. The species has experienced a dramatic decline in numbers and range in recent

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decades due to factors such as habitat destruction and fragmentation and the impact of introduced predators (Yokochi et al. 2016). Cooper et al. (2020) examined the physiological tolerance to environmental conditions of the Western Ring-tailed Possum. Basal metabolic rate and other standard physiological variables measured at an ambient temperature of 30  C corresponded to values for other marsupials. At lower temperatures, body temperature decreased slightly, and metabolic rate increased significantly at 5  C. The species experienced mild hyperthermia at higher temperatures, and increased evaporative heat loss by licking. Their point of relative water economy ( 8.7  C) was more favorable than other possums. It was predicted that Western Ring-tailed Possums should tolerate low ambient temperatures and be more physiologically tolerant of hot and dry conditions than other possums. The species should physiologically tolerate the climate of habitat further inland than their current distribution, and withstand moderate impacts of climate change in the south-west of Western Australia (Cooper et al. 2020).

Species Affected by Declining Rainfall Low rainfall has been shown to have a significant influence on the abundance of small marsupials in forests, woodlands, and heathlands including the Brush-tailed Phascogale (Rhind and Bradley 2002) and Honey Possum (Bradshaw et al. 2007) in south-western Australia. There is also recent evidence that low rainfall and drought have severe impacts on the abundance of species such as Agile Antechinus, Swamp Antechinus, and Eastern Quoll in south-eastern Australia (Fancourt et al. 2015; Parrott et al. 2007; Sale et al. 2008).

Swamp Antechinus The Swamp Antechinus is a small terrestrial dasyurid that has a restricted, fragmented, coastal distribution in south-eastern Australia and is listed as Vulnerable (Environment Protection and Biodiversity Conservation (EPBC) Act 1999; https://www.dcceew.gov. au/environment/epbc). It favors damp habitat, particularly dense heathlands and woodlands, tussock grasslands, sedgelands, and gullies (Menkhorst 1995), often in landscape settings with little exposure to the sun (Gibson et al. 2004). Significant population declines of the species have been recorded during periods of below-average rainfall and drought (Sale et al. 2008), especially during the “millennium drought” (1996–2010) where much of the southeast of Australia experienced persistent drought (CSIRO and BOM 2022). Major declines of the species were recorded in the eastern Otways, (2013–2017). Assessment of long-term changes found that high-density populations occurred after above-average rainfall, and both low- and high-density populations collapsed after wildfire, after low rainfall, and in fragmented habitat. While low rainfall was proposed as a likely factor contributing to declines in Swamp Antechinus populations in the eastern Otways (Wilson et al. 2001), there is now strong evidence from several sites that rainfall does have major impacts on population dynamics (Sale et al. 2008). Maximum population densities occurred following the

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highest total annual rainfall (901 mm) recorded for two decades, and density declines were measured during periods of below-average rainfall and drought (2001–2007). The impact of rainfall on the species is considered to result from bottom-up increases or declines in productivity of vegetation and associated dietary resources, particularly moth larvae and beetles (Sale et al. 2008). The observed increase in survival of females into the breeding season, of juveniles after weaning, and of overall body weight following peak annual rainfall has been related to increased productivity, while lower rainfall and drought result in decreased productivity with consequential population declines. Declining rainfall during the “millennium drought” (1996–2010), and exceptionally low rainfall in 2014 (498 mm) and 2015 (448) appear to have impacted Swamp Antechinus across the landscape. High rainfall in July 2016 followed by high spring rainfall was expected to result in increased survival and recruitment. There was no increase in locations or trap success in 2017, providing no evidence of such responses. This indicates that recovery may require longer periods of increased rainfall. The species may now be restricted to very small populations in refuges such as coastal dunes, and predicted low rainfall and increased burning frequency pose major threats to the species’ survival (Wilson et al. 2017).

Eastern Quoll The endangered Eastern Quoll is a medium-sized carnivorous marsupial that now survives in the wild only in the island state of Tasmania. It has recently undergone a rapid and severe population decline in Tasmania, with no sign of recovery (Cunningham et al. 2022). Spatially and temporally explicit weather modelling suggested that the proximate cause of decline was a prolonged period of unfavorable weather during 2001–2003 (Fancourt et al. 2015). The environmental suitability for Eastern Quolls was negatively associated with precipitation, with the highest predicted suitability in areas of very low precipitation, and the minimum winter temperature was negatively related to quoll occurrence at temperatures above 0  C, indicating that quolls do better in dry years with cold winters. Although these two variables explained over 75% of variation in quoll abundance, the mechanisms behind weather-driven fluctuations in abundance are not understood. It was hypothesized that the weather variables may influence prey availability (Fancourt et al. 2015). Analyses of diet found contraction of dietary niche during winter (July) and early spring (September) when insect larvae were the bulk of quoll diet, making the species vulnerable to weather-related fluctuations in food availability at that time (Fancourt et al. 2018). Current and historic dietary composition exhibited large differences with a marked shift from insect larvae to mammals, mainly due to a reduction in corbie (Oncopera intricata) larvae (Fancourt et al. 2018). Quoll abundance is positively related to corbie larva abundance during winter, and the abundance of both appear negatively related to winter rainfall. The lower contribution of insects at sites with low quoll densities suggests that insects represent an important food item for Eastern Quolls during winter, when dietary niche is narrowest and energy demands are highest. The findings suggest that weather-induced fluctuations

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in quoll abundance, including the significant state-wide decline during 2001–2003, are potentially driven by weather-induced fluctuations in corbie larva abundance.

Fire Impacts Fire is the dominant terrestrial, landscape-scale disturbance factor globally (Bowman et al. 2009), and studies using a range of climate models predict a more fire-prone future in most terrestrial ecosystems (Moritz et al. 2012). It has been estimated that at least 4400 IUCN-listed threatened species are being adversely affected by contemporary fire regimes; i.e., changes to the frequency, timing, intensity, and extent of fire events (Kelly et al. 2020). The majority of these are threatened by increasing, rather than decreasing, fire frequency or intensity (Kelly et al. 2020). Fire regimes encompass a sequence of fire events and are determined by major factors such as frequency, intensity, season and type (Gill and Catling 2002), and spatial and temporal arrangement of fire regimes (Bradstock et al. 2005; Parr and Andersen 2006). Inappropriate fire regimes such as long periods of fire exclusion, or sustained frequent burning, may lead to local extinctions of flora and fauna and result in a loss of biodiversity over time (Burrows and Wardell-Johnson 2003). Faunal species differences in fire responses and recovery have been studied extensively in Australia and are related to differences in the ability of animals to escape or shelter from fire, to survive in post-fire environments, together with differences in habitat and resource specificity, fecundity, and dispersal capacity (Nimmo et al. 2021). Ecological fire regimes appropriate for fauna can thus be based on life history strategies, post-fire succession patterns, and habitat requirements (Driscoll et al. 2010). Impacts of fire regimes, particularly frequency and extent, have had strong impacts on marsupials in the forests and heathlands of Australia. In southern heathlands and heathy woodlands, some marsupial species increase in abundance in habitat regenerating after fire, and may reach maximum abundance about 2–8 years after fire (Wilson et al. 2017). The rate of recovery of vegetation, not time per se, is considered the most important factor (Fox and Monamy 2007) and is strongly dependent on rainfall patterns post fire. A succession of species occurs when their particular requirements are met, for example, the Agile Antechinus and the White-footed Dunnart are early to mid-succession species, whereas the Swamp Antechinus occurs late in succession due to its dependence on thick, complex vegetation structure (Wilson et al. 2017). In forest communities, differences in fire severity play a major role in determining post-fire survivorship and habitat use for arboreal marsupials (Banks et al. 2011). Fires of high intensity and severity can make habitat unsuitable by depleting critical food and shelter resources. For example, the abundance of Southern Greater Gliders declined after severe wildfires removed hollow-bearing trees and incinerated foliage, leading to scarcity of food and cover (Chia et al. 2015). Inappropriate fire regimes such as long periods of fire exclusion, sustained frequent burning, or large intense fires have had serious impacts on threatened

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marsupials, particularly those with small population sizes. Large and intense fires have severely impacted terrestrial species such as Gilbert’s Potoroo, Swamp Antechinus and Quokka, and arboreal species such as Leadbeater’s Possum, the Koala, Western Ring-tailed Possum, and Red-tailed Phascogale. Inappropriate fire regimes have led to local extinctions of flora and fauna and result in a loss of biodiversity over time (Woinarski et al. 1999). Although there is much information on fire impacts on marsupials, there is limited or no information on the fire responses of most species in relation to intense megafires such as occurred through the south-eastern Australian coastal forests in the spring and summer of 2019–2020 (Jolly et al. 2022).

Megafires Climate change impacts on fire regimes include the increased frequency of large fires of extreme intensity (megafires). The 2009 “Black Saturday” wildfires in Victoria were among Australia’s worst bushfire disasters with 173 human deaths and 450,000 ha burnt. In south-eastern Australia, the wet decades of the 1950s and 1970s were followed by the significant “millennium drought” (1996–2010) (CSIRO and BOM 2022). The Black Saturday fires occurred during extreme bushfire weather conditions: one week before the fires, a significant heatwave affected south-eastern Australia. From 28–30 January, temperature records were broken with areas experiencing three consecutive days above 43  C (109  F), with the temperature peaking at 45.1  C (113.2  F) on 30 January 2009. An unparalleled sequence of megafires between September 2019 and March 2020 followed the driest year on record in Australia. In 2019, national annual rainfall was 40% lower than the long-term average and maximum temperatures were, on average, 2.1  C above the long-run average maxima. The forest fire index in December 2019 was the highest on record for almost all of eastern Australia. This sequence of megafires burnt more than 100,000 km2 of native vegetation in eastern and southern Australia during a fire season of longer duration, and fires of severity and extent greater than ever recorded for these temperate and subtropical regions (Collins et al. 2021). Over 20% of Australia’s eucalypt forests burned, 10-times higher than the annual average for these biomes (Boer et al. 2020). Early estimates were that the area would have contained almost 800 million (Dickman and McDonald 2020) updated to 3 billion native vertebrates affected by the fires when their full extent was understood. Rapid desktop assessments showed that the megafires overlapped with the distributions of hundreds of vertebrate species and thousands of invertebrate species, including numerous threatened species (Ward et al. 2020). Significant analyses of impacts of the fires on animal species, and prioritization of species for management response, were prepared in 2020–2021 along with an assessment of the conservation impacts of population loss and recovery (Legge et al. 2022). This work estimated the proportion of each of 173 taxa whose distributions substantially overlapped the fire extent. Using expert elicitation, the local population responses to fires of varying severity were estimated. The spatial and

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elicitation data were then combined to estimate overall population loss and recovery paths. This information was employed to indicate potential eligibility for listing as threatened, or uplisting, under Australian legislation (EPBCA 1999). The megafires caused, or contributed to, population declines that may make 70–82 taxa eligible for listing as threatened; and another 21–27 taxa may be eligible for uplisting. The largest estimated population losses at 10 years/3 generations for marsupials were the Northern Long-nosed Potoroo (Potorous tridactylus tridactylus) the Yellow-bellied Glider, Koala (listed population), the Southern Greater Glider (Petauroides volans volans) (30% declines); the Southern Long-nosed Potoroo (Potorous tridactylus trisulcatus), Long-footed Potoroo, and Kangaroo Island Dunnart Sminthopsis fuliginosa aitkeni (50% declines). Marsupials identified as now probably eligible for listing include the Yellowbellied Glider, Long-nosed Bandicoot, Parma Wallaby Notamacropus parma, and Mainland Dusky Antechinus Antechinus mimetes. The taxa likely to be eligible for uplisting included the Northern Greater Glider (Petauroides volans minor), Koala (listed population), Southern Greater Glider, Northern Long-nosed Potoroo, Southern Long-nosed Potoroo, Long-footed Potoroo, and Kangaroo Island Dunnart. The study predicted that the marsupial taxa assessed as eligible for listing or uplisting will not recover to pre-fire population size within 10 years/three generations. Of the 91 taxa recommended for listing/uplisting consideration, 84 are now under formal review through national processes. The Greater Glider (southern and central subspecies) and the Koala (combined populations of Queensland, New South Wales and the Australian Capital Territory) have been uplisted to Endangered, the Yellowbellied Glider and southern Long-nosed Potoroo have been listed as Vulnerable.

Priorities for Conserving Diversity of Australia’s Temperate and Sub-Tropical Marsupials It is not the intention of this section to cover conservation strategies in detail as these are covered in dedicated chapters in Part IV Conservation (see ▶ Chaps. 49, “Multiple Threats Affecting the Marsupials of Australasia: Impacts and Management,” ▶ 50, “Novel Conservation Strategies to Conserve Australian Marsupials,” and ▶ 41, “Conservation Biogeography of Modern Species of Australasian Marsupials”). Rather, we will briefly identify the key priorities for conserving marsupial species in Australia’s temperate and subtropical forests, woodlands, and heathlands. The threats to marsupials in these more southern parts of Australia are the big global change drivers: climate warming, habitat and landscape fragmentation and degradation from an expanding footprint of human activity, invasive alien species and emerging infectious diseases. These drivers are synergistic and multifactorial and present a complex problem for conservation managers. Two abiding principles are to conserve diversity at multiple taxonomic levels (Family, Species, Subspecies and local adaptation) and to conserve ecological and evolutionary processes (Bennett et al. 2009).

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A key challenge is to facilitate wildlife to live in the same landscape as feral predators, Domestic Cats and Red Foxes, for which eradication is not feasible. Developing effective conservation approaches “outside the fence,” outside of islands and invasive predator-fenced reserves, has the potential to greatly enhance restoration of species, communities, and ecosystem function. Lethal management tools such as broad-scale aerial delivery of poison baits are effective for foxes, with positive outcomes for conservation in Western Australia and Victoria. Cats are more difficult to control at scale, although advances in new baits (e.g., Eradicat) and target-specific devices such as the Felixer, which can be deployed at local scale, allow targeted control (Moseby et al. 2021; Read et al. 2019). An increasing focus is on harnessing natural ecological interactions and evolutionary selective forces to shift ecosystems in favor of native species and to disadvantage invasive predators (Cunningham et al. 2019). Ecological levers include restoring top predators which suppress invasive mesopredators (Cunningham et al. 2020; Gordon et al. 2015), restoring low, dense vegetation which provides refuge for native marsupials to evade predation by cats and foxes, and using mechanical destruction of rabbit warrens to drastically reduce the abundance of rabbits which support high densities of invasive predators (Berman et al. 2011). Rabbit biocontrol measures, such as the release of caliciviruses which cause Rabbit Hemorrhagic Disease, are effective at greatly reducing rabbit density at very large scales (Pedler et al. 2016) but are perpetually limited by coevolutionary arms races between rabbits and pathogen, with the need to find new agents. Evolutionary approaches include training animals to recognize invasive predators and low-level exposure to neutered cats in a controlled environment to trigger natural evolution of behaviors and morphologies that confer resistance to predation (Blumstein et al. 2019; Moseby et al. 2016). These approaches are efficient, effective, and enduring at large scale in unfenced landscapes and their development and implementation are a priority for future conservation. For the many species that are vulnerable to climate warming, either because they are insufficiently mobile or their habitat is small or isolated, translocations need to be considered (Braidwood et al. 2018). The plant pathogen Phytophthora cinnamomi is recognized as one of the world’s most significant invasive alien species and the epidemic of P. cinnamomi “dieback” is a major concern in Australian heathland, woodland, open forest, and rainforest communities (O’Gara et al. 2005). A number of marsupial species (e.g., Honey Possum, Yellow-footed Antechinus, Swamp Antechinus, Agile Antechinus) and mammal communities have been found to be impacted by severe degradation of habitat, resulting in loss of susceptible flora species such as grasstrees Xanthorrhoea spp., major disruption to vegetation structure, reduction in ecosystem primary productivity and biomass. All conservation management needs to be approached through the lens of climate change which increases wildfire and is exacerbated by the destruction of natural habitat to support the ever-growing human need to grow food, fiber, and wood. A clear message is the need to transition agricultural and forestry production to sustainable and also restorative practices; regenerative agricultural practices at catchment scale and certification of sustainable forestry practices including selective logging and plantations. Clearfell harvesting of wet forests and industrial extractive agriculture needs to end. A holistic approach to landscape management across all

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land use classes is needed to make human landscapes functional for wildlife and imbed these in a network of high quality habitat, with a goal of retaining at least 30% natural habitat (CBD 2021).

Concluding Remarks The subtropical and temperate forest, woodlands, and heathlands in Australia support a broad diversity of marsupials with many endemic lineages, including within the three main regions where geographic barriers have meant a long history of evolutionary isolation. Species population declines and extinctions have been ongoing since European contact and introduction of alien invasive predators and the full extent of loss may never be known. Key threats are ongoing, operate synergistically, and include loss and fragmentation of habitat due to increasing human land use, invasive species particularly predators such as foxes and cats, inappropriate fire regimes, and the increasing threat of climate change which exacerbates habitat loss and the threat of megafires. A holistic and global approach to conservation and restoration is needed to mitigate and reverse the risk of widespread marsupial loss and extinctions (Figs. 2, 3 and 4).

Cross-References ▶ Conservation Biogeography of Modern Species of Australasian Marsupials ▶ Diversity and Endemism of the Marsupials of Australia’s Arid Zone ▶ Diversity and Endemism of the Marsupials of Australia’s North-Eastern Tropics ▶ Diversity and Endemism of the Marsupials of Australia’s Top End and Kimberley ▶ Impact of Habitat Loss and Fragmentation on Assemblages, Populations, and Individuals of Australasian Marsupials ▶ Multiple Threats Affecting the Marsupials of Australasia: Impacts and Management ▶ Novel Conservation Strategies to Conserve Australian Marsupials

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Wayne AF, Wilson BA, Woinarski JCZ (2017) Falling apart? Insights and lessons from three recent studies documenting rapid and severe decline in terrestrial mammal assemblages of northern, southeastern and southwestern Australia. Wildl Res 44:114–126 White LC, Mitchell KJ, Austin JJ (2017) Ancient mitochondrial genomes reveal the demographic history and phylogeography of the extinct, enigmatic thylacine (Thylacinus cynocephalus). J Biogeogr 45:1–13 Wilson BA, Garkaklis MJ (2020) Patterns of decline of small mammal assemblages in vegetation communities of coastal south-east Australia: identification of habitat refuges. Aust Mammal 43: 203–220 Wilson BA, Robertson D, Moloney DJ et al (1990) Factors affecting small mammal distribution and abundance in the eastern Otway Ranges, Victoria. Proc Ecol Soc Aust 16:379–396 Wilson BA, Aberton J, Reichl T (2001) Effects of fragmented habitat and fire on the distribution and ecology of the swamp antechinus (Antechinus minimus maritimus) in the eastern Otways, Victoria. Wildl Res 28:527–536 Wilson BA, Kinloch J, Sonneman T et al (2009) Distribution and impacts of Phytophthora cinnamomi. In: Wilson BA, Valentine LE (eds) Biodiversity values and threatening processes of the Gnangara Groundwater System, vol. Chapter nine. Gnangara Sustainability Strategy and Department of Environment and Conservation, Perth Wilson BA, Bleby K, Valentine LE et al (2010) Impacts of fire on biodiversity of the Gnangara groundwater system. Department of Environment and Conservation, Perth Wilson BA, Valentine LE, Reaveley A et al (2012) Terrestrial mammals of the Gnangara Groundwater System, Western Australia: history, status, and the possible impacts of a drying climate. Aust Mammal 34:202–216 Wilson BA, Zhuang-Griffin L, Garkaklis MJ (2017) Decline of the dasyurid marsupial Antechinus minimus maritimus in south-east Australia: implications for recovery and management under a drying climate. Aust J Zool 65:203–216 Winder M, Schindler DE (2004) Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85:2100–2106 Woinarski JCZ, Brock C, Fisher A et al (1999) Response of birds and reptiles to fire regimes on pastoral land in the Victoria River District, Northern Territory. Rangel J 21:24–38 Woinarski JCZ, Burbidge AA, Harrison PL (2014) The action plan for Australian mammals 2012. CSIRO Publishing, Melbourne Wooller RD, Russell EM, Renfree MB (1984) Honey possums and their food plants. In: Smith A, Hume I (eds) Possums and gliders. Australian Mammal Society, Sydney, pp 439–443 Yokochi K, Kennington WJ, Bencini R (2016) An endangered arboreal specialist, the Western Ringtail Possum (Pseudocheirus occidentalis), shows a greater genetic divergence across a narrow artificial waterway than a major road. PLoS One 11:e0146167

Part IV Ecology and Conservation

Population Dynamics of Neotropical Marsupials

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Rosana Gentile, Maja Kajin, and Helena Godoy Bergallo

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Life-History Strategies and Population Dynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Population Growth, Reproduction, and Population Density . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Limiting Factors and Population Regulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Metapopulation Dynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Animal Movements and Spatial Dynamics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Examples of Studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Demography and Population Modeling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Applications and Perspectives . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cross-References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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In this chapter, the most important aspects related to the population dynamics of Neotropical marsupials are reviewed. Each topic includes some theoretical information and examples of field studies. First, the theme is introduced, providing some general information about what population dynamics are and its aims. Next, the following topics are discussed: life-history strategies and population R. Gentile (*) Laboratory of Biology and Parasitology of Wild Reservoir Mammals, Oswaldo Cruz Institute, Oswaldo Cruz Foundation – FIOCRUZ, Rio de Janeiro, Brazil e-mail: rgentile@ioc.fiocruz.br M. Kajin Ecology and Environment Conservation, Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia Department of Zoology, University of Oxford, Oxford, UK H. G. Bergallo Department of Ecology, Institute of Biology Roberto Alcantara Gomes – IBRAG, Rio de Janeiro State University – UERJ, Rio de Janeiro, Brazil © Springer Nature Switzerland AG 2023 N. C. Cáceres, C. R. Dickman (eds.), American and Australasian Marsupials, https://doi.org/10.1007/978-3-031-08419-5_18

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dynamics, growth, reproduction and density, limiting factors and population regulation, metapopulation dynamics, and demography and population modeling. Finally, the application and perspectives of population dynamics studies are discussed. Throughout the chapter, the most important publications carried out in the Neotropical region related to the issues discussed are referenced and compiled. Keywords

Demography · Density feedback · Life-history · Metapopulation · Population models · Parental Investment

Introduction Populations are one of the most studied and important levels of ecological organization. A population can be defined as a set of individuals of a given species that occupies a certain area where individuals reproduce (Mayr 1970). Populations are commonly studied and understood by means of a series of attributes called population parameters, such as number of individuals, birth rate, survival rate, mortality rate, fecundity rate, and migration rate, among others. Understanding temporal variations of these attributes, as well as the causes for these variations, is called population dynamics, and is one of the central points of Population Biology. The boundaries of a population may be natural, when local geography imposes limits on a susceptible habitat for a species, or they may be arbitrary when defined according to the interest of a study. The processes acting in a population involve births, deaths, and movement of individuals. Thus, a population is not constant, neither in space nor in time; that is, the number of individuals varies from one area to another and from moment to moment. The first population studies and demographic censuses were carried out in human populations a long time ago and were fundamental in economic and social planning. As early as in Ancient Greece and Rome, people were amused by abundance increases of pest species, like rats and grasshoppers, which directly affected the quality of their lives. However, the causes of such pest outbreaks at that time were considered divine intervention, mysterious and impossible to explain. In 1662, Graunt established the first version of what was later called by Halley a life table and became an important tool for insurance calculations. Such perceptions and calculations provided the basis for modern population-dynamics studies. An outstanding publication on population biology was the book An Essay on the Principle of Population as it Affects the Future Improvement of Society, published by Thomas Malthus in 1798. He argued that the growth of a population would always outrun its ability to feed itself, so that population sizes would rise not arithmetically but geometrically, whereas food production would increase arithmetically, consequently resulting in famine and misery. Modern interest in the population ecology of wildlife and plants began in the early twentieth century, when the field of study that would be

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called population dynamics was firstly delimited by Charles Elton (Elton 1927). Around that time, mathematical models started to be used to study population dynamics by people, like Elton himself, Raymond Pearl, Alfred Lotka, and Vito Volterra, to quantify populations and understand their variations, becoming widely used in studies of population biology. Study of the population dynamics of a species aims to relate the numerical variation of the various population parameters to their causes (Begon et al. 2006). These factors can be intrinsic, that is, attributes of the population itself, such as population density and reproductive rate, or extrinsic, like environmental factors, which also includes the populations of other species in a community. Birth, death, immigration, and emigration are parameters that affect population size and are the proximate causes of population variation. These parameters are affected by environmental factors, which are considered the final causes. Thus, to understand the variation in population size, it is necessary to understand the variations in its cause; that is, how environmental factors influence birth, death, immigration, and emigration. An example of an intrinsic factor is an increase in the density of individuals in an area, which would lead to food shortages and, consequently, an increase in mortality, resulting in a decrease in the number of individuals in the population. These intrinsic factors also include the spatial structure of the population, i.e., how individuals are distributed in a certain area, social interactions, reproduction components (litter size, gestation, and lactation periods, reproductive season, mating system, sex ratio), and physiological responses to stress. Regarding environmental or extrinsic factors, the amount of rainfall, temperature, air humidity, vegetation productivity, and food resources can be taken as examples (Ricklefs 1990). Among the most important ecological characteristics of organisms are demographic strategies. Some species have fast population turnover rates, while others show slow turnover along a gradient of variation. Demographic strategies are part of the life history of a species. These can be considered as a set of responses to biotic and abiotic environmental conditions that exert selection pressure on individuals. Thus, these strategies are among the most important ecological characteristics in species differentiation and evolutionary processes (Begon et al. 2006). Considering the marsupials of the New World, didelphids stand out as the most diverse and widely studied family in relation to population dynamics. Opossums of the genera Didelphis, Philander, Metachirus, Monodelphis, and Marmosa are the most frequently studied among Neotropical marsupials. Despite the high species richness of didelphid marsupials in the Neotropical region, they have relatively similar population dynamics, based mainly on regional climate predictability (Gentile et al. 2012). Local or regional climatic conditions and resource availability are determining factors in the population dynamics of these species, commonly resulting in seasonal cycles. The purpose of this chapter is to address various aspects related to the population dynamics of New World marsupials, including theoretical information and examples of case studies. The following topics are discussed: demographic aspects, such as growth, density, and population regulation; aspects of life history strategies;

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metapopulation issues, including spatial and colonization-extinction dynamics; and finally, a brief topic about the application and perspectives of population dynamics studies.

Life-History Strategies and Population Dynamics Life-history strategies refer to a set of a species’ adaptive responses accumulated over evolutionary time (Wilbur et al. 1974). Life-history strategies include demographic (e.g. youth and adult mortality schedules, reproductive life span), energy (e.g., diet, metabolic strategies), and behavioral (e.g., space use, social organization) characteristics (Fleming 1979). The main reproductive strategy that distinguishes marsupials (Metatheria) from placental mammals (Eutheria) is the short gestation period with little investment in fetuses (12–38 days) but a long lactation period (2–11 months) (Sharman 1973). Even though the litter size is high on average (6.7
2.8 neonates, ranging from 2 to 12), the percentage of litter mass at birth to mother mass for didelphids does not exceed 0.86
0.87% (median ¼ 0.52%, lower and upper hinge from 0.16% to 1.67%, N ¼ 8) (Fig. 1a, data obtained in Jones et al. 2009). In terms of comparison, small eutherians, such as rodents, have a ratio of litter mass at birth to mother mass, for example, of 17% for Nectomys squamipes and 30% for Cerradomys goytaca (Martins-Hatano et al. 2001). Considering data of rodents and lagomorphs of some species of Neotropical families (Jones et al. 2009), the fetuses’ investment of these orders is much higher (11.65
1.97% for lagomorphs and 23.22
11.65% for rodents). There is a tendency for larger species, regardless of the Order, to have a smaller ratio of litter mass to adult mass (Fig. 1). However, this picture changes at weaning, when parental investment, as measured by litter mass expressed as a percentage of maternal mass (Russell 1982), is quite high for didelphids (117.85
110.50%, median ¼ 76.21%, lower and upper hinge from 41.56% to 164.10%, N ¼ 8). Although there may be large variation in parental investment, weaning litter mass is proportional to adult mass in didelphid marsupials (r2 ¼ 0.93, F ¼ 39.14, p ¼ 0.0008, N ¼ 8, Fig. 2). As the components of life history interact, they cannot be considered in isolation (Stearns 1992). In periods of food shortage, interrupting lactation, which leads to the death of the young but ensures female survival for future reproduction, may be an adaptive strategy for some species of Macropodidae marsupials, such as the red kangaroo, Osphranter rufus (Low 1978). For this species, this effort is not high, as they usually produce one puppy at a time, have nonseasonal reproduction, facultative embryo diapause and anestrus, uninterrupted uterine cycle, and postpartum estrus. In addition, at the end of pregnancy, the weight of the puppy represents about 44% of the mother’s weight (Russell 1982). Conversely, if environmental conditions are not favorable, the loss of an entire litter can be dramatic for didelphid females. The reproductive effort of females during lactation is so high that their mortality rate is higher after the reproductive period, as their energy reserves have been suppressed (Dickman and Vieira 2006). Thus, the didelphids’ strategy, in

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Fig. 1 Relationship between the ratio of neonate litter mass per mother body mass and logarithm of adult body mass for Neotropical species of the orders Didelphimorphia (red dots and line), Lagomorpha (blue dots and line), and Rodentia (green dots and line). Data obtained in Jones et al. (2009)

Fig. 2 Relationship between litter mass at weaning (g) and adult body mass (g) for didelphid marsupial species. Data obtained in Jones et al. (2009)

general, is to start breeding in the dry season, with less food resources, so that lactation and independence of the young occur in the season with highest resource availability, ensuring the success of the effort undertaken (Bergallo and Cerqueira 1994). The body size of a species is also a life-history trait that influences its population dynamics. For mammals, species with smaller body size have higher metabolic rates

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(Eisenberg 1980). Thus, body size can be inversely related to the population density of the species, due to the flow of energy in the body, which in turn, influences the growth rate of a species (McNab 1986). However, this relationship is not clear in Neotropical marsupials (Table 1 - r2 ¼ 0.206, p ¼ 0.158, N ¼ 48) because it also depends on the type of diet and kind of environment in which the populations occur. Carnivorous species, for example, are expected to have lower population densities than herbivores with the same body size. This can be attributed to the fact that carnivores are at higher trophic levels and, therefore, their food items occur in less abundance than the food items of herbivores, which are at lower trophic levels (Robinson and Redford 1986). However, most species of Neotropical marsupials present omnivorous diet, with a tendency for frugivory, insectivory, or carnivory (Santori and Astúa de Moraes 2006), which makes it difficult to observe the relationship between these characteristics of diet and body size with population density (Table 1). Regarding the influence of the type of environment, Didelphis aurita, for example, is found at low densities in preserved areas but at higher densities in more disturbed areas (Gentile et al. 2012), which can be attributed to the low population density of its predators (Fonseca and Robinson 1990).

Population Growth, Reproduction, and Population Density Population growth rate is one of the most important features to be studied to understand a population’s dynamics. It can be broken down into two fundamental parameters: number of individuals born minus the number of individuals dead during a certain time interval, characterizing a closed population (where no new individuals arrive or leave the area). The population growth rate can be further broken down to include the number of individuals that immigrated from and/or emigrated to neighboring areas during a certain time interval, characterizing an open population (where individuals enter and leave the area) (e.g., Gotelli 2007). Such a representation sets the population growth rate as a discrete measure, as opposed to a continuous one, representing a certain finite time interval, most commonly, a year. A year is the most logical unit for quantifying population growth rate because of the climate season cycle and, consequently, the reproductive cycle. Obtaining reliable estimates of local population abundance requires an account of the uncertainty regarding imperfect detection (Mackenzie et al. 2006). This means that the probability of capture, which is 10 months old) in a population in Tennessee (Ladine 1997). Differences might have been due to seasonal influences or the presence of raccoons (Procyon lotor), which could have caused opossums to forage at more varied times. No such difference was observed in other two populations in Florida (Ryser 1995) and in Tennessee (Carver et al. 2011), evidencing the plasticity in time of activity among different populations. Seasonal Variation: Nightly Air Temperature and Food Availability Nightly air temperature strongly influences the amount, duration, and distribution of activity in marsupials (Ryser 1995; Harmon et al. 2005; Kanda et al. 2005; Franco et al. 2011; Vieira et al. 2017). Reduced activity in winter is considered an adaptation to cold stress and has been noted in species in northern and southern latitudes (Gillette 1980; Franco et al. 2011). Didelphis virginiana reduces activity drastically when temperatures dropped below freezing, remaining in the den for several days (Fitch and Shirer 1970; Gillette 1980; Franco et al. 2011). Gillette (1980) observed that no opossum went over 15 m from its den’s entrance when temperatures were between 10  C and 15  C at sunset. However, at some point, they were forced to forage during the day, as a way to escape the high thermoregulation requirements forced by the freezing temperatures during the night. A similar behavior was observed in a population at the northernmost part of its range (Kanda et al. 2005). When temperature averaged 2  C or higher, opossums would forage for up to 6–9 hours a night. When temperature reached values between 6  C and 2  C, maximum foraging for the night was 1.5 hours, while at 6  C activity was reduced to as low as 15 minutes (Kanda et al. 2005). Given the high energy demands, reducing activity during winter can yield considerable energy savings for opossums. Thermal constraints also limit activity of D. gliroides, a small (16–32 g), microbiotheriid marsupial living in temperate rainforests of Chile and Argentina. When

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nightly air temperatures were relatively constant, D. gliroides remained active for longer periods than during nights with more variable temperatures (Franco et al. 2011; di Virgilio et al. 2014). To survive in this challenging environment, monito del monte exhibits daily torpor and hibernation (multiday torpor, Geiser 1994). This strategy helps energy storage during winter by saving 40–60% of their total daily energy needs by maintaining a decreased core temperature (Geiser 1994). Nightly air temperature not only exerts a considerable influence on activity in the field but also affects the proportion of time devoted to various types of behavior (McManus 1971). Didelphis virginiana studied in an outdoor enclosure showed pronounced reduction in activity during autumn and winter, nevertheless devoting nearly twice as much time to feeding and nest construction or maintenance (compared with spring and summer). Decrease in activity and in time devoted for certain activities at low temperatures is a consequence of increase in energy expenditure and, at the same time, decrease in foraging success, leading to a negative energy balance (Ryser 1995). This behavioral adjustment allows opossums to avoid severe temperature stresses by denning, since its pelage has relatively poor insulative properties (Scholander et al. 1950). Response to variation in nightly air temperature may also differ between populations. A study investigating geographic variation in activity patterns between two populations of G. agilis in two dry-woodland areas of the tropical savanna registered a decrease in activity at low temperatures in only one population: the southern population where the winter is more severe (Vieira et al. 2017). Gracilinanus agilis was active between 2 and 4 hours after sunset in the population at southeastern Brazil, while in central Brazil, activity was constant through the night and not affected by nightly air temperature. The decrease in temperature possibly forced G. agilis to be active only at certain hours of the night to avoid energy loss through thermoregulation. Apart from the temperature-dependent variation in activity patterns, time and duration devoted to foraging behavior also vary between seasons in New World marsupials (Atramentowicz 1982; di Virgilio et al. 2014; but see Ferreira and Vieira 2014; Marques and Fábian 2018). In French Guiana, 12 individuals (5 ♀ and 7 ♂) of C. philander were monitored for 50 nights in both abundant and scarce seasons (Atramentowicz 1982). When mature fruits were abundant, movements lasted only part of the night (55 to 75% of the night used), with females returning most often to the shelter before 04:00. However, activity of females with suckling young (> 5 weeks old) was 20% greater when compared with non-lactating females or females with pouch young less than 5 weeks old, which was explained by their increased dietary needs due to high milk production. In the scarce seasons, all females, lactating or not, foraged more than 9 hours per night (78 to 90% of the night used). In spite of this, all females lose weight, and production of young was strongly affected by the seasonal food shortage, as shown by an increased pouch young mortality in the second litter (Charles-Dominique et al. 1981). Laboratory studies evaluating activity during food deprivation periods have shown contrasting responses. When C. derbianus was put on food deprivation for 1 to 2 days, they double their activity levels (Hunsaker Don II and Shupe 1977). On

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the other hand, when males of D. virginiana were exposed to a 50% reduction in food availability, foraging activity was shortened by 2 to 3 hours, and 48% of activity was concentrated within 3 hours after dark (Angermeier et al. 1986). These different responses may be related to differences in time allocated to each period, as observed in D. gliroides. In full-moon nights, D. gliroides consumed more fruits of the mistletoe per visit, even though individuals were less active (di Virgilio et al. 2014). Thus, marsupials can adopt different strategies regarding time allocation and feeding behavior when facing severe periods. Food patchily distributed in space and time also attracts and leads to an increase in marsupial activity. Activity patterns of D. gliroides varied considerably between months, which was related to both resource abundance and distribution in temperate forests of Argentina and Chile (di Virgilio et al. 2014; Fontúrbel et al. 2014). The monito del monte is omnivorous, consuming preferably arthropods and fruits, including the mistletoe Tristerix corymbosus (Wilson and Mittermeier 2015). In both areas D. gliroides increased activity with increase fleshy fruit availability (di Virgilio et al. 2014; Fontúrbel et al. 2014). In the tropical savanna, Pseudobombax tomentosum, a deciduous tree typically found along the edges of gallery forest, blooms in the dry season (Gribel 1988). Flowers open between 18:20 and 18: 40, being functional for one night only. Caluromys lanatus was observed active at this same time, visiting several flowers during the same night (Gribel 1988). The same behavior was observed in the Mexican mouse opossum (Marmosa mexicana). Mouse opossums fed on inflorescences of the Neotropical palm Calyptrogyne ghiesbreghtiana right after nightfall (18:00–19:00) and from 23:00 to 01:00. Assuming a 90% assimilation efficiency of sugar and 46 g of body mass, M. mexicana would have to visit nine flowering plants in order to cover its daily energetic needs (Sperr et al. 2009). Moonlight Nighttime illumination varies through the moon cycle, and several nocturnal marsupials are known to alter their activity patterns in relation to moon phase; some suppress activity in bright moon nights to avoid predators (lunarphobia), while others increase activity to improve foraging efficiency (lunarphilia, Prugh and Golden 2013). The lunarphobic behavior was recorded in at least five New World marsupials (e.g., Julien-Laferrière 1997; Moraes Jr 2003; di Virgilio et al. 2014; Fontúrbel et al. 2014; Albanesi et al. 2016; Table 1). In D. gliroides, moonlight intensity affects activity, feeding patterns, and time allocation (di Virgilio et al. 2014; Fontúrbel et al. 2014). Individuals are more active during new and first-quarter moon nights, when visibility in the forest is considered low (Fontúrbel et al. 2014), and visit and consume higher quantities of the mistletoe fruits during shorter visits in bright moon nights, as a way to reduce exposure to predators (di Virgilio et al. 2014). As in the D. gliroides, an increase in activity was significantly associated with periods of low luminosity in both Andean white-eared opossum (Didelphis pernigra; Barrera-Niño and Sánchez 2014) and the whiteeared opossum (Didelphis albiventris; Albanesi et al. 2016), indicating that foragers perceive decreased predation risk. Norris et al. (2010) also documented later periods of activity during the night in lunar phases of greater luminosity for D. marsupialis.

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However, the authors do not conclude if the opossum decreases its activity, nor if it increases it, but that it postpones the beginning of activity to latter hours of the night. Three primary hypotheses have been proposed underlying the effects of moonlight on the activity patterns of prey species: the predation risk hypothesis, the visual-acuity hypothesis, and the habitat-mediated predation risk hypothesis (Prugh and Golden 2013). The first one states that if predators are more effective in capturing preys in bright moon nights, preys would respond by shifting their activity patterns to evade predation. The second, the visual-acuity hypothesis, states that if preys rely on vision as their primary sensory system, activity would equally increase, and not be affected by predators. The third, the habitat-mediated predation risk hypothesis, states that if moonlight increases predation risk, the suppressive effect of moonlight on prey activity should decrease as habitat cover increases. Camera trap studies evaluating the relationship between moonlight and nightly activity patterns of predators and some potential marsupial preys showed no support for the first hypothesis. In the humid Chaco, D. albiventris is more active in bright moon nights as its potential predator, the ocelot (Leopardus pardalis), while gray four-eyed opossums (Philander opossum) show similar activity patterns across all moon phases (Huck et al. 2016). Likewise, in primary lowland Amazonian forest, D. marsupialis is more active on both full and new moon, while P. opossum is the only fully nocturnal species, besides the ocelot, with a uniform distribution across the moon cycle (Pratas-Santiago et al. 2016). No conclusion can be reached regarding the validity of the habitat-mediated predation risk hypothesis since both studies found similar results for closely related species in both open and forested habitats. Contrary to what was recently found in a meta-analysis on the effect of moonlight on predation risk in mammals (Prugh and Golden 2013), the variability in responses of marsupials to moonlight suggests a high plasticity in timing of activity. While a population of D. albiventris shows lunarphobic behavior in a Piedmont forest in northwestern Argentina (Albanesi et al. 2016), a second population increases activity in bright moon nights in the Argentinean Gran Chaco (Huck et al. 2016, 2017). Other species which showed different responses to moonlight variation was the common opossum, D. marsupialis. The opossum shows no response to changing levels of luminosity (Harmsen et al. 2011; Parodi 2015) and was equally active at full and new moon (Rutherford and Foon 2016). Finally, differences between sexes to moonlight illumination is also observed in C. philander (Julien-Laferrière 1997). The bare-tailed woolly opossum does not shift their activity to the parts of the night with low moonlight intensities, but males are more active in nights with no or low moonlight than in nights with medium to high moonlight. The same response was not observed in females which had a constant, low level of activity, independent of moon phase. However, no female was monitored at full moon. Anthropogenic Factors Marsupials as any other species are subjected to varying levels of human disturbance in the environment. Daily activity patterns can be affected by habitat loss and fragmentation, invasive alien species, and increased

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hunting pressure (Norris et al. 2010; Silva et al. 2018; Carvalho et al. 2019). It is therefore surprising that its influence on marsupial activity has remained relatively unexplored. Habitat conversion prevails in tropical and temperate biomes, and several marsupials persist and even thrive in these altered landscapes (Cáceres and MonteiroFilho 2001; Norris et al. 2010; Silva et al. 2018). Across a fragmented Amazonian forest landscape, D. marsupialis is active later with increasing forest patch size (Norris et al. 2010). No significant difference in activity was observed between native temperate rainforests and exotic eucalyptus plantations or in areas under different levels of human activity for both D. gliroides (Fontúrbel et al. 2014) and D. virginiana (Wang et al. 2015), respectively. Thus, other factors may facilitate the persistence of these species following human perturbation. Although the importance of habitat loss and fragmentation is recognized, hunting is often implicated as the main driver of defaunation and can have profound effects on species activity patterns. In the Western and Central Brazilian Amazonia, nocturnal and cathemeral species (including the nocturnal marsupials D. marsupialis and M. myosuros) are detected relatively more frequently in areas near human communities (a proxy for the intensity of hunting) with low proportion of primary forest (Abrahams et al. 2017). For the authors, concentrated activity in the night minimizes direct contact with humans. According to interviews with local residents, both marsupials are not prime targets in hunted sites. However, in other forested areas, species of the genus Didelphis are important source of protein for human communities (Barros and Azevedo 2014). According to reports of locals, the best times to hunt the common opossum is early in the morning, when they are resting in burrows, or at night, when individuals are foraging (between 20:00 and 2:00; Barros and Azevedo 2014). Despite high conservation concern and commonness in both rural and protected areas, few studies so far have investigated the potential effects of alien species such as dogs and cats (domestic or feral) on the activity pattern of New World marsupials (Zapata-Ríos and Branch 2016; Silva et al. 2018; Carvalho et al. 2019). Zapata-Ríos and Branch (2016) compared the activity of D. pernigra and other ten mammal species in areas with and without feral dogs in the Andes. Three species significantly altered their activity in areas with feral dogs, but the Andean opossum was not one of them. While feral dogs were active at dawn and dusk, D. pernigra was nocturnal, and the overlap in activity between species in the beginning of the night did not change its behavior. The authors suggested that this might be explained by physiological constraints of D. pernigra that preclude shifts in activity patterns, prey naiveté, or existence of effective mechanisms for reducing interference and predation from dogs, such as arboreality. A low overlap in activity patterns is also recorded for D. aurita and domestic dogs in two Atlantic Forest areas (Silva et al. 2018; Carvalho et al. 2019). While differences in activity between the two dog populations were observed (mainly diurnal, Silva et al. 2018; cathemeral, Carvalho et al. 2019), D. aurita was mainly nocturnal in both areas. When encountering a potential predator is inevitable, two potential anti-predator behaviors can be adopted

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by some opossums: thanatosis, also known as tonic immobility, death feigning, or even “playing possum” (Francq 1969), and the secretion of a pungent-smelling substance which may be deposited with feces or urine or separately (Russell 1984). Thanatosis is mostly recorded in species of the genus Didelphis (Francq 1969), while paracloacal gland secretion occurs in several marsupial families (Russell 1984). Competition and Predation: Time as a Niche Dimension Sympatric species are often thought to reduce competition through differential use of available resources (e.g., space, food, and time) (Schoener 1974a). Although temporal partitioning has been proposed as a mechanism that promotes stable coexistence (Kronfeld-Schor and Dayan 2003), the time dimension is assumed not to be as common as is space or food (Schoener 1974a,b). The first major effort evaluating resource partitioning among species from various taxa was made by Schoener (1974a). He reviewed evidences of resource partitioning in three niche dimensions (habitat, food, and time) in 81 studies. He concluded that “habitat dimensions are important more often than food-type dimensions, which are important more often than temporal dimensions.” However, when estimating species segregated by two or more dimensions, 41% were separated in some degree by time. For the author, “the amount of resource competition required to cause an animal to drop certain periods of time from its activity should be considerably greater” (Schoener 1974b). The rarity of temporal partitioning has been attributed to the rigidity of timekeeping mechanisms, to different physiological and morphological adaptations required to be active at different times of the day, and to phylogenetic constraints that might restrict shifts in activity patterns (Kronfeld-Schor and Dayan 2003; Roll et al. 2006). Since Schoener’s review, there is a growing body of evidence that temporal partitioning might facilitate coexistence between species, including several studies on small mammals (e.g., Dickman 1991; Vieira and Baumgarten 1995). In order to avoid direct confrontation (interference competition) or reduce resource overlap (resource competition), temporal segregation would be expected to occur mainly among species occupying the same vertical strata and sharing similar food preferences. In a high-elevation grassland field, the small mammal community composed by the shrewish orange-sided opossum Monodelphis dimidiata and three other rodents is mostly diurnal and terrestrial, feeding mainly on invertebrates (Vieira and Paise 2011). In this environment, food availability varies according to two seasons (“scarcity” and “abundance”). If the low invertebrate availability affected the use of time through competition in the scarcity season, a reduction in niche breadth and the overall overlap in time use among species would be observed. Contrary to predictions, the temporal niche segregation under conditions of low resource availability was not observed; both niche breadth and overall overlap in time increased. The authors suggested that for the studied community, time dimension was not relevant for helping species coexistence through reduction in competition. Indeed, that diurnal small-mammal community could have converged upon a

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preferable period of the day, with higher resource availability and reduced exposure to low nocturnal temperatures. Similarly, other field studies examining temporal segregation among marsupials and other mammals found no strong, significant evidence (Marmosa paraguayana and D. albiventris, Oliveira-Santos et al. 2008; P. opossum, D. marsupialis, the armadillo Dasypus novemcinctus, and the paca Cuniculus paca, Hernández Hernández et al. 2018). One study in particular evaluated the ecological segregation in space, time, and diet of two sympatric, close related opossums, D. aurita and D. albiventris. Activity throughout the night was very similar and opossums differed in the use of space, with adult females of D. aurita occupying mainly the forest interior and stream sides, while D. albiventris females were mostly restricted to forest edges or open areas (Cáceres and Machado 2013). Assessment of temporal partitioning is not an easy task, even for well-studied species. Didelphis virginiana and P. lotor are nocturnal mammals that co-occur in large areas of their geographic distribution. Two studies evaluating temporal partitioning between species found contrasting results (Ladine 1997; Carver et al. 2011). Ladine (1997) observed that D. virginiana forages at different times of the night and suggests that the two taxa partition resources through foraging time differences. During the study, intraspecific differences in activity between sexes and among age classes of D. virginiana were also detected, and the author hypothesized that differences might have been due to seasonal influences or that the presence of raccoons could have increased intraspecific variation in activity among opossums. A second study on temporal partitioning verified the lack of temporal differences in diel foraging patterns (Carver et al. 2011). Although a degree of avoidance between species might exist, other possible factors may also play a role. Despite no strong evidence of shift or restriction in temporal activity among potential competitors in New World marsupials, many studies conducted under controlled laboratory conditions with dasyurid marsupials have proven that spatiotemporal partitioning can indeed facilitate coexistence among ecologically related species (e.g., Moss and Croft 1988; Righetti et al. 2000). A series of controlled introduction and removal experiments in a terrarium showed that both Planigale gilesi and Planigale tenuirostris were active throughout the night without the presence of the larger dasyurid, Sminthopsis crassicaudata (Moss and Croft 1988). However, after the introduction of S. crassicaudata, both species exhibited behavioral changes such as a strong bimodal pattern of activity. Similarly, Righetti et al. (2000) revealed differences in activity patterns and interactions within and among three dasyurids (Antechinus swainsoni, Antechinus stuartii, and Sminthopsis murina). Avoidance behavior between the two Antechinus species, and from the smaller competitor, S. murina, toward the larger one, A. stuartii, may enable coexistence. Most studies on resource partitioning in ecological communities have focused on how potential competitors coexist rather than on predators and their prey (KronfeldSchor and Dayan 2003). By choosing a specific time of the day for activity, the spectrum of potential predators is also chosen. While foraging for preys, nocturnal marsupials are exposed to several predators such as carnivore mammals, snakes, and owls. In this way, they must balance between the costs of predator avoidance with

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the adequate foraging time. A series of studies in a fragmented landscape in the Santa Cruz Mountains in west-central California have examined the impacts of human disturbances (e.g., exurban housing development and recreational activities such as biking, hiking, and dog walking) on spatial and temporal patterns of apex predators (puma and coyote) and mesopredators (e.g., D. virginiana and P. lotor) and their consequences throughout the ecological community (Wang et al. 2015). Didelphis virginiana were found more often at sites occupied by pumas, while coyote and raccoon detection probabilities were negatively associated with pumas (Wang et al. 2015). Temporal overlap between pumas and opossums also increased at high human use locations (Wang et al. 2015). The authors suggested that opossums may have benefited from suppressed activity of coyotes (predator) and raccoons (competitor) in sites occupied by pumas, even the opossum being a relative common item in pumas’ diet (Wang et al. 2015). High overlap in activity patterns between opossums (D. marsupialis and D. aurita) and potential predators (puma, ocelot, and jaguar) suggests that Didelphis species do not adjust activity to avoid predators (Weckel et al. 2006; Harmsen et al. 2011; Carvalho et al. 2019). However, in two of these studies, D. marsupialis and D. aurita were not considered as part of predators’ diet (Weckel et al. 2006; Harmsen et al. 2011), despite being part of the diet in other areas (e.g., Pratas-Santiago et al. 2016). It is important to consider that pumas, ocelots, and jaguars have a diverse diet and will rarely drive their hunting effort to one specific prey (Weckel et al. 2006; Harmsen et al. 2011). In fact, synchronous activity of prey species and their predators is another possible strategy that may reduce the chances of being captured – the dilution effect (Halle and Stenseth 2000). Thus, the effect of potential predators on the temporal activity of preys should also be evaluated considering the entire local community. So far, what most studies on temporal segregation in New World marsupials have searched for is a major shift or a remarkable restriction in activity. However, a change in activity is restricted to the preferred time window and will be detected only by detailed data collection in the field or by experiments conducted in enclosures. With the advent of wildlife camera traps, researchers are now able to give an in-depth examination of possible changes in temporal activity in the entire community of potential competitors, predators, and their prey, while considering activity timing of conspecifics and possible confounding factors. Finally, as pointed out by Schoener (1974a), in each community, “the species separate according to various mixtures of differences in vertical, horizontal habitat, and food type.” In this way, studies should focus on more than one niche dimension and interaction between them when evaluating resource partitioning in ecological communities.

Conclusion and Future Directions Knowledge on activity patterns of most New World marsupials is still limited to a coarse description. In sum, New World marsupials concentrate activity at night, most frequently in a single daily peak of activity soon after sunset. For some species, a

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second peak of activity is also registered and has been related to food availability, predation risk, and weather conditions, however an endogenous origin cannot be ruled out. Diurnal activity is limited to Monodelphis species and has been associated with cold, open areas (Roll et al. 2006; Vieira and Paise 2011). The proportion of diurnal and crepuscular species can be even higher since only 20% of the genus Monodelphis has some record (anedoctal) of activity (Wilson and Mittermeier 2015). Temporal plasticity in the clade is evident; marsupials vary activity in response to changes in environment, and individual variation is also observed in some species. However, contrary to observed in some Australasian marsupials, no study has demonstrated a switch in activity (e.g., from day to night) and changes occur within a limited time window. Several studies have focused on the effects of moonlight on suppressing activity of potential preys, probably as an influence of studies conducted with desert rodents in the last decades. Results are inconclusive, since some species reduce activity in bright moon nights, while other have shown an increase or no response to changes in moon illumination. The effect of seasonality in food availability and temperature were also highly investigated, both in the field and in indoor enclosures. Overall, marsupials increase activity in periods of reduced food availability and avoid exposure to cold environments by reducing it. Nonetheless, in the latter, most studies were conducted with species living at higher latitudes, where temperature variation is high. Several other factors remain largely unexplored like the effect of vegetation cover, rainfall, parasites, and individual condition on temporal activity. Future studies should focus on the variability in response to environmental factors among populations. This latter will be dependent on a joint effort of researchers to gather data from different regions. Activity data gathered in the field have been gleaned as a by-product of ecological studies focusing on questions related to population and community ecology (e.g., Alves and Andriolo 2005; Behnke 2015; Hernández-Pérez et al. 2015; Hernández Hernández et al. 2018). One of the first employed methods was live trap checks in pre-defined intervals (Vieira and Baumgarten 1995; Cáceres and Monteiro-Filho 2001). Latter, a variety of methods have been proposed to estimate activity in the field such as digital timing device (e.g., Graipel et al. 2003; Ferreira and Vieira 2014; see a method for correction the data in Graipel et al. 2003), radiotelemetry (e.g., Galliez et al. 2009), data-logging sensors (e.g., Kanda et al. 2005), and camera traps (e.g., Oliveira-Santos et al. 2008). Camera trap studies, in particular, have produced considerable insights into the activity patterns of several species. One of the most valuable contributions of camera trapping is the continued recording of activity of the entire community for several months. However, camera traps can show bias favoring data on larger animals such as Didelphis species (Cole Burton et al. 2015), because of increased detection range and day range (Rowcliffe et al. 2014). Camera traps also do not give detailed information on individuals such as sex, age, body mass, and reproductive condition. Hence, the method employed should be linked to the study question. Despite the many advances for describing and quantifying activity patterns, only recently ecologists have delineated studies modeling the degree to which biotic and abiotic factors affect activity and temporal niche partitioning in marsupials (e.g.,

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Norris et al. 2010; di Virgilio et al. 2014; Ferreira and Vieira 2014; Wang et al. 2015). To address this gap, Frey et al. (2017) suggest a coordinated distribution of experiments to capture sufficient camera trap data across a range of anthropogenic stressors and community compositions, which would facilitate a standardized approach to assessing the impacts of multiple variables on species’ activity. New methodologies should also be employed in studies on temporal activity such as the use of kernel functions to fit activity data (e.g., Oliveira-Santos et al. 2013; Rowcliffe et al. 2014; Henning et al. 2017). The use of kernel functions allows the identification of periods of concentrated activity, avoiding problems associated with the arbitrariness of the timescale categorization, adequately fitting either a bimodal or a multimodal pattern (Oliveira-Santos et al. 2013). These new methodologies open new possibilities for investigations of activity patterns and for testing hypotheses concerning the response of marsupials to changes in the environment and in experimental treatments.

Cross-References ▶ Movement, Habitat Selection, and Home Range of American Marsupials ▶ Positional Behavior and Locomotor Performance of American Marsupials: Links with Habitat and Substrate Use

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Daily Torpor, Hibernation, and Heterothermy in Marsupials

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Fritz Geiser and Christine E. Cooper

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . American Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Didelphimorphia: Opossums . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Paucituberculata: Shrew Opossums . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Microbiotheria: Monito del Monte . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Australasian Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Dasyuromorphia: Insectivorous/Carnivorous Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Notoryctemorphia: Marsupial Moles . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Diprotodontia: Possums . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Heterothermy in Large Marsupials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . How Many Marsupials Express Torpor? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Ecological Aspects of Torpor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Concluding Remarks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cross-References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

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Abstract

Most marsupials are small, and because they are endothermic and have high metabolic rates when active, they lose substantial amounts of energy and water. To deal with such challenges many marsupials are not permanently homeothermic, but rather they are heterothermic and can enter a state of torpor during which metabolic rate (MR), water loss, body temperature (Tb), and other Dedicated to the memory of Francisco (Pancho) Bozinovic F. Geiser (*) Centre for Behavioural and Physiological Ecology, Zoology, University of New England, Armidale, NSW, Australia e-mail: [email protected] C. E. Cooper School of Molecular and Life Sciences, Curtin University, Perth, WA, Australia © Springer Nature Switzerland AG 2023 N. C. Cáceres, C. R. Dickman (eds.), American and Australasian Marsupials, https://doi.org/10.1007/978-3-031-08419-5_43

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physiological functions are temporarily reduced. Torpor is used by both American and Australasian marsupials, including species from nine families ranging in body mass from ~5 g to 1000 g. Daily torpor with a reduction of metabolism and water loss by ~70% and Tb by ~10–20  C for several hours, typically interrupted by daily foraging, is most common. Multiday torpor (hibernation) is known to occur in the Microbiotheriidae, Burramyidae, and Acrobatidae, which can reduce MR by >90% and Tb by ~30  C to a few degrees above 0  C. Hibernating marsupials can remain torpid for several days up to a month before periodically rewarming, perhaps because of the need to drink. As torpor saves so much energy and water it has profound effects on the ecology and biology of many marsupials. Torpor permits survival under adverse seasonal environmental conditions and periods of food and water shortages as well as persisting and reproducing in resource-poor habitats. Torpor can facilitate extreme longevity and assists survival after natural disasters via reduced energy and water demands, which permits reduced foraging and thus predator avoidance. Thus, torpor is a crucial part of the biology and ecology of many marsupial species. Keywords

Adverse conditions · Daily torpor · Hibernation · Long-term survival · Thermal energetics · Water conservation

Introduction Extant mammals comprise three groups, the egg-laying mammals (Monotremata, ~5 species), the pouched mammals (marsupials or Metatheria, ~345 species), and the placental mammals (Placentalia or Eutheria, >6000 species). Endothermic mammals evolved from ectothermic reptiles around 200 Mya, which required a many-fold increase in metabolic rate and therefore food requirements (Withers et al. 2016; Lovegrove 2019). The oldest subclass, the egg-laying mammals, diverged from the line leading to the therian subclass about 190 Mya, while marsupials and placental mammals diverged around 140–160 Mya (Bininda-Edmonds et al. 2007; O’Leary et al. 2013). Consequently, the three mammalian lineages must have separately survived the Cretaceous-Paleogene (K-Pg) extinction of dinosaurs and many other terrestrial organisms at around 65 Mya (O’Leary et al. 2013; Lovegrove 2019). The use of heterothermy and torpor, the topic of this chapter, provides a functional avenue as to how endothermic mammals could survive this calamity (e.g., Lovegrove 2019) and how they continue to live and reproduce under adverse conditions. Consequently, torpor is an important aspect of the ecology, distribution, and abundance of marsupials. Of the ~345 extant marsupial species, most (~225) are found in Australia and New Guinea and the rest (~120) are mainly in South and Central America. Extant marsupials are classified into seven orders, the Didelphimorphia and Paucituberculata (American marsupials; Ameridelphia), as well as the

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Microbiotheria from the Americas, and the Dasyuromorphia, Peramelemorphia, Notoryctemorphia, and Diprotodontia from Australia and New Guinea. The Microbiotheria are considered to be potential ancestors of Australian marsupials as they belong to the Australidelphia along with the Australian orders, although they occur only in South America (see Riek and Geiser 2014; Withers et al. 2016). Several biological factors predispose marsupials to the use of heterothermy to balance their energy and water budgets. Marsupials differ from the much more diverse placental mammals in their reproductive biology. The neonates of marsupials are very small, weighing only between ~5 and 900 mg or 1 day, often lasting for weeks, with minimum Tb typically decreasing to 6 months is probably the main reason they survive over winter under snow. Burramys remain in subnivean hibernacula until spring food sources are available and therefore highly seasonal torpor is more beneficial than for other pygmy-possums (Körtner and Geiser 1998). Interestingly, Burramys bred in captivity and raised under warm thermal conditions did not fatten and never hibernated, although they were held under identical conditions as wildcaught individuals, which did fatten and hibernated for months (Geiser et al. 1990). This developmental plasticity complicates reintroduction of the species to the wild where hibernation is crucial for winter survival. More recently, however, mothers

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and young were held under thermal conditions similar to those in the wild and offspring released to the wild survived and have successfully bred (Parrott et al. 2017). Torpor patterns of Burramys are strongly temperature-dependent, with the lowest TMR and the longest TBD occurring at Ta of ~2  C, which is the Ta they experience in their subnivean hibernacula (Geiser and Broome 1993; Körtner and Geiser 1998). A change in Ta, caused by the predicted reduction of snow cover due to climate change, will impact the energetics of hibernation and therefore the overwinter survival of this species, an important factor that impacts the demographics and population of this critically endangered species (Broome 2001). Likewise, the availability of liquid drinking water in hibernacula may be important for pygmypossums to maintain hibernation until food is available in spring. Drinking to maintain water balance is one likely reason why hibernators must undergo periodic arousals from torpor during the hibernation season (Thomas and Geiser 1997). If Burramys eat snow to obtain this water, the energy required to melt and then warm the snow to normothermic Tb would reduce the hibernation season by ~30 days, compared to only ~9 days for drinking liquid water (Cooper and Withers 2014). Feathertail gliders (Acrobates pygmaeus, ~12–14 g, and A. frontalis, ~12–19 g) and the Feather-tailed Possum (Distoechurus pennatus, ~40–50 g) of the family Acrobatidae are small insectivorous/nectarivorous marsupials found in Australia and New Guinea. Feathertail gliders use torpor both in the wild and in captivity (Frey and Fleming 1984; Geiser and Ferguson 2001). In captive A. pygmaeus, torpor lasted up to 8 days; the minimum Tb was as low as 2  C, and at a Ta of 5  C, the TMR was only about 1% of the RMR of normothermic animals, and only 6% of the BMR in the TNZ (Geiser and Ferguson 2001). Although the pattern of torpor for feathertail gliders is similar to that of pygmy-possums (Burramyidae), A. pygmaeus does not fatten extensively unlike the pygmy-possums and many other hibernators, being more similar to some bats (Geiser 2021). Free-ranging feathertail gliders had a more or less constant body mass of about 13.5 g from autumn to spring and aroused daily from torpor during that time (Frey and Fleming 1984). Torpor in captive-bred feathertail gliders was less pronounced (shorter TBD, higher minimum Tb) than that expressed by wild-caught individuals, suggesting developmental phenotypic plasticity (Geiser and Ferguson 2001). Torpor expression also differed for gliders from different habitats, with animals in montane regions entering deeper torpor than those from subtropical coastal areas (Geiser and Ferguson 2001). Data on torpor in the Feather-tailed Possum from Papua New Guinea are not available, but it is likely that they are heterothermic, since they are small, feed on insects and fruit, and often nest alone in tree hollows. The Honey Possum (Tarsipes rostratus, 10 g) is the only extant species in the family Tarsipedidae and is restricted to southwestern Australia where high floral diversity ensures a year-round supply of flowering plants which provide the nectar and pollen on which this species feeds. In the wild, Honey Possums use torpor mainly during the cold season between autumn and spring, but a few individuals were observed torpid during summer (Bradshaw and Bradshaw 2012). In captivity, the species attains a torpor Tb as low as ~5  C, similar to that of hibernators on average. The minimum TMR was also similar to that of small hibernators, but they

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did not remain torpid for more than 10 h (Withers et al. 1990), indicating an unusual torpor pattern of deep, but brief (30
) often results in wider forest loss, with as many as 70% of trees that remain in the wake of selective logging succumbing within 10 years (Cameron and Vigus 1993). Most selective logging (>96%) occurs in lowland tropical rainforest in Papua New Guinea (Sekhran and Miller 1994), where the majority of marsupials occur (Menzies 2011). Arguably the best studied example of multiscale logging effects comes from work of the assemblage of arboreal marsupials in the wet-ash-type eucalypt forests of the Central Highlands of Victoria, in Southeastern Australia. These forests have long been subject to widespread clearcutting for several decades. These are intensive operations in which almost all trees are removed and several hundred tonnes of logging debris is then burnt in a high-intensity fire lit to promote the regeneration of harvested areas. Animals resident on logged sites die in situ. Key nesting and denning habitat for arboreal marsupials in large old hollow-bearing trees is severely

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Fig. 2 Location of cutblocks of clearcut ash-type eucalypt forest in the Central Highlands of Victoria. (Photo by Dave Blair and The Australian National University)

depleted in logged areas. There is therefore habitat loss for cavity-tree-dependent arboreal marsupials at the individual tree level on logged sites; large old trees are either removed or those that are retained on harvested sites collapse soon after logging as a result of exposure, accelerated decay, or both (Lindenmayer et al. 2016a). Newly regenerated trees on logged sites can take a century or more to first begin to develop cavities suitable for occupancy by arboreal marsupials (Lindenmayer et al. 2017a). Logged areas in the Central Highlands of Victoria can be up to 40 ha in size, with up to three adjacent cutblocks summing to cutover areas approaching 120 ha (Fig. 2). The amount of logging in the landscape has significant negative effects on levels of site occupancy by species such as the Critically Endangered Leadbeater’s Possum (Lindenmayer et al. 2020a). There are therefore landscape-level effects of logging-generated habitat loss on arboreal marsupials in ash-type forests. Similar findings have made for other species such as the Yellowbellied Glider (Lefoe et al. 2021). Logging operations are typically planned many years in advance in Victorian forests, including those dominated by ash-type eucalypt stands, and the areas targeted for future harvesting also tend to be of high conservation value for threatened forest-dependent species, including a range of species of arboreal marsupials and ground-dwelling taxa like the Long-footed Potoroo (Potorous longipes) (Taylor and Lindenmayer 2019). Logging has a range of other effects on habitat suitability in forest ecosystems which can contribute to habitat loss and habitat fragmentation for marsupials. For example, recurrent logging operations in Southeastern New South Wales appear to

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have altered the composition of tree species throughout large parts of the region (Au et al. 2019). These changes in tree species composition have, in turn, altered the suitability of food resources for specialist folivores such as the Koala in these forests and resulted in widespread habitat loss (Au et al. 2019). Finally, logging infrastructure such as roads is known to limit movements of marsupial species such as the Brown Antechinus (Antechinus stuartii) (Barnett et al. 1978).

Tackling Logging as a Driver of Marsupial Decline There are several ways in which the effects of logging on marsupial biodiversity can be reduced or reversed. The most straightforward way is to not log at all – and source wood products from other places such as plantations. Ceasing logging is particularly important when it occurs in forests with high conservation value – as is proposed in the coming 5 years in the Australian State of Victoria (Taylor and Lindenmayer 2019). Ceasing logging is also crucial in already heavily disturbed landscapes, where small remaining areas of intact forest can be lost or fragmented by further harvesting operations (Taylor and Lindenmayer 2020). Other ways to reduce the impacts of logging include dispensing with highly damaging intensive silvicultural systems like clearcutting and instead adopting more biodiversity-sensitive harvesting methods such as variable retention harvesting (Franklin et al. 1997). Under such systems, key elements of stand structure like large old trees which are critical habitat for marsupial biota are maintained across multiple cutting cycles (Fedrowitz et al. 2014). Variable retention harvesting was found to be better than clearcutting in promoting the persistence of marsupial species such as the Agile Antechinus (Antechinus agilis) in logged wet forests in Victoria (Lindenmayer et al. 2010a). Forest restoration also can make an important contribution to both reversing habitat loss and reducing the impacts of fragmentation. For example, strengthened protection from logging can help boost the extent of critical age classes like old growth that are hotspots of biodiversity, including for marsupials such as the Yellowbellied Glider and Southern Greater Glider in some Australian eucalypt forest types. Ongoing logging operations often depend on the construction of human infrastructure like roads which can, in turn, fragment populations in remaining unlogged patches. Careful planning of the location, width, and other attributes of roads (such as the amount of physical connectivity of overstorey vegetation) may limit their negative effects on biodiversity. In other cases, establishing structures such as rope bridges across roads may enhance connectivity in populations of species that would otherwise face limited mobility (Yokochi and Bencini 2015).

Tree Plantation Development Tree plantation establishment can result in both habitat loss and habitat fragmentation for some species of marsupials. For example, the Southern Greater Glider and the Mountain Brushtail Possum (Trichosurus caninus) died en masse when areas of native eucalypt forest were cleared and replaced by stands of exotic Radiata Pine

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(Pinus radiata) trees (How 1972; Tyndale-Biscoe and Smith 1969). Similarly, populations of the Black Spotted Cuscus (Spilocuscus rufoniger) have declined by >80% due to the establishment of oil palm plantations and logging concessions (Helgen and Jackson 2015), with plantation establishment placing at risk populations of many other arboreal marsupials in Papua New Guinea and on large islands such as Seram and Sulawesi (Menzies 2011). Patches of original forest and woodland vegetation sometimes remain within the boundaries of areas that have been subject to conversion to stands of plantation trees. In these environments, these native forest and woodland patches are surrounded by stands of plantation trees (Lindenmayer et al. 2019a). Pine stands can be unsuitable habitat for some (but not all) species of marsupials (e.g., for leaf-eating specialists like the Southern Greater Glider), and act as a complete or partial barrier to movement (including dispersal) (Banks et al. 2005; Taylor et al. 2007). In some cases, Radiata Pine and eucalypt plantations are established in areas that was former grazing land (Felton et al. 2010), and these treed environments can create habitat for some species of marsupials that might otherwise be absent. For example, there are records of the Koala colonizing hardwood plantations (Smith 2004) and this can create complications for management when it comes time to harvest them (https://www.forestrycorporation.com.au/about/releases/2019/statement-koala-tim ber-plantation). Other species of marsupials which are often found in stands of exotic plantation trees include the Common Wombat (Wombat ursinus) (Rishworth et al. 1995) and the Common Ringtail Possum (Lindenmayer et al. 1999).

Tackling Plantation Development as a Driver of Marsupial Decline Most plantation development in Australia now occurs on already cleared land, in which case there is a transformation from one already modified environment to another (Watson et al. 2014). An exception is Northern Australia where areas of native vegetation have been cleared to establish plantations and temperate native grasslands in Southern Australia on which plantations have sometimes been established. On this basis, it is important to carefully assess the environmental values of land (including their suitability as habitat for marsupials) before they are converted to tree plantations. Although the primary objective of plantation establishment is to generate large quantities of timber, there are well-recognized ways to manage them so they retain some values for biodiversity (Lindenmayer and Hobbs 2004). For example, there are often remnant patches of native forest and woodland within the boundaries of many plantations and these areas can provide habitat for a range of native animals, including marsupial species. These important natural assets should be retained during initial plantation establishment and then through successive harvesting rotations as there is evidence of long-term persistence of marsupial species like possums and gliders in such areas (Youngentob et al. 2013b). There are often edge effects at the boundary between remnant patches and adjacent stands of plantation trees (Youngentob et al. 2012) and this can make it particularly important to maintain larger patches of native forest and woodland with a low edge to interior ratio as part of plantation management. Conversely, very narrow strips of remnant vegetation

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(like those along creeks) can be difficult environments for animals to persist, in part because of high energy costs in gathering food (Recher et al. 1987).

Fire Fire is a key ecological process in the majority of Australian terrestrial ecosystems (Bradstock et al. 2012), but much less so in the perennially wet environment of Papua New Guinea and Irian Jaya. The natural fire regime varies considerably between these ecosystems – from rare, very high-severity conflagrations to frequent, low-severity fires (Bradstock 2010). Fires can have marked impacts on many elements of biodiversity, including populations of marsupials. For example, fire can lead to the direct mortality of some individuals (see Fig. 3); an estimated three billion animals including numerous individual marsupials perished in the 2019–2020 wildfires (Dickman and Lindenmayer 2022). The habitats of numerous species of marsupials were extensively altered as a result of the 2019–2020 wildfires in Eastern Australia (Ward et al. 2020). However, in some cases, individual animals may persist during and immediately after high-severity fires and can instigate marked population recovery, as occurred in populations of the Agile Antechinus following the 2009 wildfires in the forests of Victoria (Banks et al. 2017). Similar results were found for this species and other marsupials like the Yellow-footed Antechinus following wildfires in the Grampians National Park in Victoria (Hale et al. 2021).

Fig. 3 A Leadbeater’s Possum (photo by Tim Bawden), and the body of one found incinerated following the 2009 wildfires (photo by Doug Beckers)

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Fire can have marked impacts on habitat suitability for marsupials. For example, wildfires in 2009 in the wet forests of the Central Highlands of Victoria consumed or badly damaged large numbers of large old hollow-bearing trees that were critical nesting and denning sites for arboreal marsupials and other cavity-dependent species such as the Agile Antechinus (Lindenmayer et al. 2012). Indeed, the amount of area burnt in the landscape during the 2009 fires was found to be a key driver of site occupancy by species such as the Southern Greater Glider (Lindenmayer et al. 2020a). Similarly, fires have destroyed numerous paddock trees in agricultural landscapes of Southern New South Wales (Crane et al. 2016), many of which would have been valuable denning and nesting habitat for species like the Squirrel Glider (Crane et al. 2008). In some cases, altered fire regimes can lead to an absence of fire and this, in turn, can result in habitat loss for some marsupials. As an example, species such as the Northern Bettong (Bettongia tropica) are strongly associated with the open grassy understorey of wet eucalypt forests of far North Queensland (Winter 1997). In the absence of fire, wet sclerophyll forest can be invaded by tropical rainforest (Harrington and Sanderson 1994) and habitat loss occurs (possibly, in part, because of declines in suitable food resources such as ectomycorrhizal fungi [truffles]) (https:// www.awe.gov.au/environment/biodiversity/threatened/recovery-plans/recoveryplan-northern-bettong-bettongia-tropica-2000-2004). There are other important factors that can influence the impact of fire on marsupials. These include the condition of the vegetation prior to a fire and therefore potential habitat suitability after fire in the process of post-disturbance stand recovery and vegetation succession. For example, in the wet forests of Victoria, fires that burn in old growth forest subsequently produce pulses of key biological legacies such as large old dead and fire-scarred trees that are eventually suitable nesting sites for cavity-dependent marsupials (Lindenmayer et al. 2019b). Conversely, such legacies are generally not produced when fires burn young forests like those that had previously been clearcut, or which had been subject to both logging and fire (e.g., post-fire salvage logging) (Lindenmayer et al. 2019b).

Tackling Altered Fire Regimes as a Driver of Marsupial Decline Relationships between fire, habitat loss, and habitat fragmentation for marsupials are complex and highly nuanced. This is because such relationships are underpinned by the natural fire regime in a given ecosystem and how regimes have both been altered and interact with changes in landscape cover (Driscoll et al. 2021). Therefore, fire impacts extend beyond a single fire, to the sequence of many fires in a landscape over time, and whether there have been changes in the severity, frequency, seasonality, and spatial heterogeneity (patchiness) of fire with which particular marsupial species have co-evolved (Whelan 1995). In some forest types, such as Gondwanan rainforest and mangrove forests in Eastern Australia, the natural fire regime can include a complete absence of fire (Kooyman et al. 2020). In other forest ecosystems such as the tropical savannas of Northern Australia, the natural fire regime is frequent with low-severity fires that occur every few years (Russell-Smith et al. 2014). In yet others, the fire regime is rare with high-severity stand-replacing fire that

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occurs every 75–150 years (such as in the Mountain Ash and Alpine Ash forests of Southeastern Australia; Cary et al. 2021). Fire can become a threatening process for marsupials when the fire regime appropriate for a given ecosystem is altered. Countering altered fire regimes as a driver of marsupial decline requires maintaining or restoring the natural fire regime for a given ecosystem and, where possible, ensuring that the frequency, severity, extent, and heterogeneity of fires are restored in ways that are within the bounds of natural variability. Potential actions range from: (1) doing nothing (as the ecosystem already maintains full post-fire regenerative capacity and species can readily persist); (2) employing interventions prior to a conflagration like prescribed burning to limit the risks of high-severity fire; (3) excluding activities that impair post-fire recovery (e.g., post-fire logging); and (4) applying artificial seeding where natural regeneration fails to produce suitable habitat. The most ecologically effective actions will be ecosystem specific, species specific, and context specific and informed by knowledge of the ecosystem and animal species in question as well as interrelationships with attributes like vegetation condition at the time a given area is burnt (e.g., young versus old forest) (Lindenmayer et al. 2023). Efforts to restore natural fire regimes in some forest ecosystems around the world have included recommendations to implement Indigenous burning practices and these often entail frequent low-severity fire to limit the risks of subsequent highseverity wildfire (Russell-Smith et al. 2013). However, there are some considerations associated with the use of cultural burning. Cultural burning (even at low intensity and severity) was not practiced in some forest types as it could eliminate the forest altogether (e.g., where the natural fire regime is an absence of fire like the Gondwanan rainforests of Southern Australia; Kooyman et al. 2020) or where the natural fire regime is rare with very high-severity wildfire such as the tall, wet temperate eucalypt forest types (Lindenmayer 2009; McCarthy et al. 1999). A key need in managing fire regimes for marsupial conservation is to be aware of the total fire burden – cultural burns, prescribed burns, and wildfires in restored forest landscapes to ensure there is an understanding of where and how frequently all types of fires have occurred. This is critical because the total number of fires, the frequency of fire, and the time since the last fire (and the severity of previous fires) all can have major impacts on both ecosystem function and habitat suitability for particular marsupial species (Lindenmayer et al. 2016b). Mitigating the impacts of fire on marsupial biodiversity may require reducing the potential for interactions with other processes that influence habitat loss and habitat fragmentation. In an example from agricultural Australia, widespread land clearing and intensive grazing by domestic livestock have resulted in major losses of paddock trees (Fischer et al. 2009). The decline of paddock trees, coupled with a paucity of recruitment of such trees, is a profound environmental issue for biodiversity conservation in many Australian agricultural landscapes (Manning et al. 2006), including for species dependent on these trees (e.g. Crane et al. 2008). The problem of rapidly declining numbers of paddock trees is exacerbated by periods of high-severity wildfires in some farming districts. These fires totally consume many large old

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paddock trees and badly damage numerous others (Crane et al. 2016), thereby accelerating their collapse. Another example of interactions between habitat loss, habitat fragmentation, and fire is the increasing body of evidence showing that forests regenerating after logging are at increased risk of high-severity wildfire (Taylor et al. 2020), with such effects persisting for 40+ years after timber harvesting ( Taylor et al. 2014). Therefore, populations of marsupials in wood-production forests of Southeastern Australia must deal not only with the direct impacts of logging and the direct effects of wildfire, but also the interaction between these two drivers which serve to further promote both the prevalence of high-severity fire and the resulting spatial extent of young fire-prone forests. Fire and logging can interact in other ways. For instance, burnt wood production forests are often subject to post-fire (salvage) logging in which fire-damaged trees are cut in an attempt to recover some of their economic value (Lindenmayer et al. 2008). Such operations have marked effects on soil environments and understorey vegetation (Bowd et al. 2018, 2019) as well as on the prevalence of large old hollow-bearing trees (Lindenmayer and Ough 2006) – all of which can influence habitat suitability for a range of biota, including marsupials. Finally, fire can interact with other important landscape processes which influence populations of marsupials such as levels of predation by exotic carnivores. For example, feral cats (Felis catus) target burnt areas for hunting after fire (McGregor et al. 2014). Similarly, there can be increased macropod browsing of burnt areas which can reduce populations of palatable plants and affect habitat suitability for a range of animal species (Foster et al. 2015a, b).

Urbanization and Human Infrastructure Urbanization and human infrastructure can drive both habitat loss and habitat fragmentation for populations of marsupials. There is increasing pressure to accommodate expanding urban settlements in almost all parts of Australia, in many parts of Papua New Guinea, Irian Jaya, and throughout the Eastern Indonesian archipelago due to government resettlement initiatives. These pressures have both direct and indirect impacts on habitat loss and habitat fragmentation for marsupial populations. Indeed, many threatened species, including a range of at-risk marsupial species, have distributions that overlap with urban areas, including expanding human settlements where habitat loss and habitat fragmentation are likely (Ives et al. 2016). Human infrastructure also can have significant impacts on marsupial populations (Taylor and Goldingay 2009). For example, roads can lead to significant mortality through collisions with motor vehicles and thereby serve to fragment populations, as has been well documented in species such as the Lumholtz’s Tree Kangaroo (Dendrolagus lumholtzi) (Shima et al. 2018), the Koala (Gonzalez-Astudillo et al. 2017), the Eastern Quoll (Dasyurus vivverinus), and the Tasmanian Devil (Sarcophyilus harrisii) (Jones 2000). Roadkill by vehicles was a major reason for the failure of a reintroduction program for the Eastern Quoll at Booderee National Park in the Jervis Bay Territory (Robinson et al. 2019). In other cases, infrastructure

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like the establishment of ski fields can affect connectivity for biodiversity (Sato et al. 2013); one such affected species is the Mountain Pygmy Possum (Mansergh and Broome 1994). Less obvious but perhaps equally insidious is the effect of elevated human activity in otherwise intact habitat in urban and peri-urban areas. Activities such as running, bicycle riding, and dog walking can lead to disturbance and high levels of stress for many wildlife species (Fardell et al. 2020), effectively fragmenting their populations even if suitable habitat is available (Fardell et al. 2020, 2021). Chronic stress contributes to declines of Agile Antechinus populations in disturbed and fragmented habitats (Johnstone et al. 2011), and likely depletes populations of other marsupials such as the Brown Antechinus and Northern Brown Bandicoot in urban and peri-urban areas (Fardell et al. 2020, 2021).

Tackling Urbanization and Human Infrastructure as a Driver of Marsupial Decline Several strategies can be employed to tackle the problems of habitat loss and habitat fragmentation arising from urbanization and the establishment of human infrastructure. An important one is to limit the development of new urban settlements in areas that have high conservation value for marsupial biota. In other cases, where urban development does proceed, careful consideration of housing density may be required because it can have a marked effect on the kinds of marsupial taxa which can and cannot persist in a developed area (Villaseñor et al. 2017). In the case of human infrastructure such as roads, various options can be employed to limit their impacts. For example, rope bridges have been installed to assist arboreal marsupials successfully cross major roads such as in the case of the Endangered Western Ringtail Possum (Pseudocheirus occidentalis) (Yokochi and Bencini 2015). In addition, traffic calming strategies as well as clear signage can be useful to reduce collisions with motor vehicles. In a much-celebrated example of restoring connectivity disrupted by human infrastructure, rocks were added to the landscape to link the boulder fields occupied by male and female populations of the Mountain Pygmy Possum that had become separated by a ski run (Mansergh and Broome 1994).

Interactions Among Drivers The preceding sections have focused primarily on individual drivers of habitat loss and habitat fragmentation and their respective effects on populations of marsupials. However, many of these drivers do not act in isolation. Rather, they interact with other factors, sometimes producing cumulative effects (Driscoll et al. 2021). As an example, fragmentation of habitat in Papua New Guinea allows hunters easier ingress into onceremote forest areas, with the effects of hunting then magnifying the impacts of fragmentation on marsupials such as bandicoots, forest wallabies (Dorcopsis and Dorcopsulus spp.), and tree-kangaroos (Dendrolagus spp.) (Menzies 2011). As another example of interactions between drivers, there is a body of evidence that indicates that microclimate conditions are cooler and less subject to extremes in

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old growth forests relative to younger logged and regenerated stands (Frey et al. 2016; Lindenmayer et al. 2022a). This, in turn, can influence patterns of local and regional occurrence of some elements of biodiversity, which may have important effects on temperature-sensitive species such as the Southern Greater Glider (Youngentob et al. 2021). Overlaid on the challenges created by microclimatic conditions, associated with forests of different ages, has been the widespread loss of old growth forests as a result of fire and logging in states such as Victoria (where there has been a 77% decline in old growth since 1995; Lindenmayer and Taylor 2020). This is also coupled with changes in tree species composition in logged forest toward nonpalatable food sources for animals such as the Koala and the Southern Greater Glider (Au et al. 2019). In summary, this means that habitat loss and habitat fragmentation can result from an interaction between logging, fire, climate, and changes in tree species composition. As outlined above, there are numerous other examples of interactions between drivers of decline that result in habitat loss and habitat fragmentation, including land clearing, human hunting, fire, predation by exotic animals, and browsing by native herbivores following fire.

Tackling Interacting Factors as a Driver of Marsupial Decline Multiple interacting stressors can place species at elevated risk of decline and extinction. Indeed, the number of threats to which a species is exposed is a key driver of eroded resilience to decline in populations of vertebrates globally (Capdevilia et al. 2022). Therefore, a key response must be to reduce the number of stressors on a given population. This demands identifying the suite of drivers of decline for that population which can require detailed long-term work (Lindenmayer et al. 2020c), including well-designed experiments (Foster et al. 2016). From a conservation and management perspective, it can take substantial logistical effort and financial investment to effectively address all the drivers threatening a particular taxon. In some cases, the effects of particular drivers can be more readily mitigated than others – providing what are termed leverage points in management (Lindenmayer et al. 2020c). As an example, tackling climate change is a complex global issue that will take enormous societal effort and money to change. At a state and regional level, a strategy like stopping native forest logging is a far more tractable policy option (and requires not global but local and statewide action), and by halting it, interactions with other drivers like climate change can be prevented (Lindenmayer et al. 2020c).

General Discussion Australia is famous for its iconic marsupial fauna. Sadly, it is also infamous for its appalling rate of mammal extinctions, including the loss of many iconic species of marsupials (Dickman and Lindenmayer 2022; Woinarski et al. 2015). Many Australian ecosystems are now characterized by a highly depauperate marsupial fauna relative to the complement of species they supported at the time of European settlement ~230 years ago. This is particularly true in some biomes such as deserts, temperate woodlands, and temperate-native grasslands. Often the drivers of decline

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Table 1 Examples of drivers of decline of populations of Australasian marsupials. Note that only one driver has been listed for a given species, although many of the species listed in the table are susceptible to the impacts of multiple drivers Common name Squirrel Glider Southern Greater Glider Brown Antechinus Koala Mountain Pygmy Possum Leadbeater’s Possum Northern Bettong Rock Wallaby species Tasmanian Devil a

Latin name Petaurus norfolcensis Petauroides volans Antechinus stuartii Phascolarctos cinereus Burramys parvus

Example of a driver of declinea Habitat loss through clearing for grazing and cropping Habitat loss through clearing for plantation establishment Habitat fragmentation Reduced food quality

Example citation Van der Ree et al. (2004) Tyndale-Biscoe and Smith (1969) Dunstan and Fox (1996) Au et al. (2019)

Climate change

Steffen et al. (2009)

Gymnobelideus leadbeateri Bettongia tropica Petrogale spp.

Logging Altered fire regimes

Lindenmayer et al. (2020a) Winter (1997)

Feral predators

Lavery et al. (2021)

Sarcophilus harrisii

Human infrastructure (roads)

Jones (2000)

It is recognized that many species will be at risk of several key drivers of decline

are well known but they may not be the direct effects of habitat loss and habitat fragmentation, such as in the case of marsupial declines in Northern Australia which have occurred in protected areas like Kakadu National Park (Woinarski et al. 2015) (Table 1). Conversely, habitat loss and potentially also habitat fragmentation have been drivers of decline in other circumstances. For example, fire, logging, and their interaction appear to be important factors contributing to both the loss of habitat and the fragmentation of habitat for arboreal marsupials in the wet eucalypt forests of the Central Highlands of Victoria (Lindenmayer et al. 2020a; Taylor and Lindenmayer 2020). In yet other cases, the drivers of marsupial decline remain unknown, such as in populations of threatened species like the Southern Greater Glider, but also previously abundant species such as the Common Ringtail Possum in Booderee National Park in Jervis Bay Territory (see Lindenmayer et al. 2018).

The Impacts of Habitat Loss and Habitat Fragmentation Occur at Multiple Spatial Scales A major challenge in studies of, and management efforts to mitigate, the effects of habitat loss and habitat fragmentation is that their impacts can manifest at multiple spatial scales. These scales can range from effects on individual trees (van der Ree

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et al. 2004) to those across entire landscapes (Lindenmayer et al. 2020a), and even regions and biomes (Betts et al. 2019). Determining the best scales to achieve the most effective outcomes for marsupial conservation is not always straightforward. Indeed, in many cases, actions at multiple scales will be needed, especially if different stressors act at different spatial scales or over different temporal scales. As an example, efforts to conserve suitable habitat may demand providing: (1) suitable tree-level denning and/or nesting resources; (2) suitable patch-level foraging resources for individuals and pairs or colonies of animals; (3) sufficient connectivity at a landscape scale to promote dispersal between animals in different patches; and (4) appropriate bioclimatic conditions at a regional scale. These multiscaled responses further underscore why efforts to tackle the problems they create will often be species specific and landscape and ecosystem context specific.

There Are Temporal Dimensions to the Effects of Habitat Loss and Habitat Fragmentation There are important temporal dimensions to understanding the effects of habitat loss and habitat fragmentation. That is, the impacts on biodiversity of changes in landscapes may take many decades to manifest: the so-called extinction debt (Figueiredo et al. 2019). For example, populations of some species will still be declining as a result of land clearing that took places many decades earlier. This may be the case for the small and isolated lowland population of Leadbeater’s Possum at Yellingbo Nature Reserve in Victoria where the number of animals has gradually dwindled by 75% over the past 20 years to just a few dozen individuals (D. Harley, personal communication). There also can be very long-term biogeographical effects of species sensitivity to habitat fragmentation, particularly as a function of past natural disturbance history. For example, a global study by Betts et al. (2019) indicated that the prevalence of fragmentation-sensitive animal species (as reflected by avoidance of edges) was three times higher in areas with limited rates of past disturbance history (such as a result of fires, glaciation, and hurricanes) than where disturbances were common. These effects were particularly marked in tropical areas when compared to biomes in higher latitudes (Betts et al. 2019). Quantifying the risk of decline and extinction as a result of extinction debts is challenging and can require well-parameterized models such as those for population viability analysis (Sebastián-González et al. 2011). Such work has been conducted for a number of species of marsupials in Australia and, in many cases, there are major concerns about the long-term persistence of particular marsupial species in response to the effects of multiple drivers of decline, including habitat loss and habitat fragmentation (e.g., Taylor and Goldingay 2009). However, a key issue in the use of population viability analysis is the need to better document all model input parameters in published applications of the approach to ensure that work is repeatable and reproducible (see Morrison et al. 2016).

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The Use of Reintroductions and Translocations to Tackle the Problems of Habitat Loss and Habitat Fragmentation Populations of some species of marsupials have become so fragmented that the potential for natural dispersal between them is very limited. This is the case for small remaining populations of species such as the Mountain Pygmy Possum which is restricted to alpine areas like those at Mt. Buller in Victoria. Such isolation has led to losses of genetic diversity, with corresponding negative impacts on the viability of small remaining populations. Assisted movements of animals through translocations from other populations of the Mountain Pygmy Possum have helped boost genetic variability and rates of breeding success in the species (Weeks et al. 2017). There are other examples of the use of translocations and reintroductions to supplement existing populations of marsupials or reestablish populations where they previously occurred but have since suffered extinction. Organizations like the Australian Wildlife Conservancy and Bush Heritage Australia have developed significant expertise in successful marsupial translocations and reintroductions, typically in mainland “islands” where purpose-built fences preclude exotic predators and herbivores to protect reestablished populations of native mammals (Hayward 2012; Ringma et al. 2018). However, it is inappropriate to conduct such movements of animals without ensuring that the factors giving rise to the original demise of populations (e.g., predation by feral animals) have been overcome (Fischer and Lindenmayer 2000). Of course, effective translocations and reintroductions will be dependent on the recipient area supporting suitable habitat for the target species – which may be increasingly rare for some taxa because of the rapid climate change (Steffen et al. 2009).

There Is a Critical Need for Enhanced Conservation Policy and Environmental Regulation Good conservation outcomes for marsupials can occur only when management actions are supported by good legislation that underpins effective policy. Australia is deficient in all these regards, with the nation’s appalling record on mammal extinction (including recent mammal extinctions) reflecting, in part, limitations of conservation legislation (Woinarski et al. 2017). Drivers of habitat loss and habitat fragmentation for marsupials like land clearing are poorly regulated in Australia (Ashman et al. 2021; Ward et al. 2019); very few applications for land clearing are rejected under Australian Government legislation (Ward et al. 2019). For instance, land clearing and logging, which lead to habitat loss for the Southern Greater Glider, have actually increased since the species was listed under the Australian Government’s Environment Protection and Biodiversity Conservation (EPBC) Act (Ashman et al. 2021). In other cases, legislation associated with Regional Forest Agreements to support the native forest logging industry overrides the protection of key elements of forest marsupial biota, rendering the Environment Protection and

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Biodiversity Conservation ineffective for these animals (Lindenmayer and Burnett 2021). In summary, effective marsupial conservation in Australia demands legislative reform, both at Commonwealth and state levels. It is clear that the Environment Protection and Biodiversity Conservation Act is ineffective in conserving at-risk marsupial species and populations, and weak in preventing drivers of decline over which there can be direct management control such as land clearing and forest logging (see Ashman et al. 2021; Ward et al. 2019).

There Is Critical Need for Long-Term Research and Monitoring and Adequate Funding to Support It Many of the key insights into the effects of habitat loss and habitat fragmentation on marsupials are based on long-term studies including those that result in a detailed understanding of broader ecosystem dynamics (e.g., Dickman et al. 2014; Hayward 2012). Yet, there are very few long-term studies of marsupials in Australian landscapes (Youngentob et al. 2013a). This is preventing the development of the key bodies of knowledge urgently needed to promote the conservation and management of this critically important component of Australia’s mammal fauna. Such long-term work is essential, especially in Australia where hypervariable climatic conditions result in large annual fluctuations in populations sizes and, in turn, can make it difficult to untangle natural temporal changes from long-term drivers of decline. Long-term work is also essential to quantify problems that take a long time to manifest such as those associated with extinction debts in the dwindling lowland population of Leadbeater’s Possum. Australia requires proper long-term investment not only in management actions to recovery marsupial biodiversity, but also to monitor those actions (Wintle et al. 2019). Too often conservation actions are undertaken in crisis mode when populations are very small, the cost of interventions is very high, and the chances of success are low. Reintroduction and translocation programs are a good example (Fischer and Lindenmayer 2000). Preemptive and proactive conservation actions for marsupials are needed well before crises have manifested. Such an approach demands proper resourcing. However, current investments are ~10% of what they need to be to adequately conserve Australia’s biodiversity, including its marsupial biota (Wintle et al. 2019). Australia also could (and should) learn from other nations where long-term monitoring programs are strongly connected to well-developed and effective programs for conservation action. These include not only small nations such as Switzerland (Federal Office for the Environment 2017) but larger ones like the USA where conservation actions are a mandated part of responses to the Endangered Species Act (Wintle et al. 2019). Such connections between robust long-term monitoring and effective conservation actions are largely missing in Australian biodiversity conservation (e.g., see Queensland Audit Office 2018; Victoria Auditor-General’s Office 2021), and this must be rectified urgently.

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Concluding Remarks Australia supports some of the world’s best known and most iconic and charismatic marsupials. Many are threatened and there is an array of drivers of decline. Two of these are habitat loss and habitat fragmentation. Habitat loss and habitat fragmentation can occur in a range of ways including land clearing, climate change, native forest logging, plantation establishment, altered fire regimes, and urbanization. These are often widespread and pervasive human drivers of habitat loss and habitat fragmentation that lead to marsupial decline. Halting habitat loss and habitat fragmentation will be a major challenge and will demand multifaceted strategies ranging from slowing climate change, limiting land clearing, mitigating logging impacts, and better planning urban developments. Allied with slowing and mitigating these drivers of decline will be an urgent need for legislative reform (giving rise to better environmental and biodiversity protection) as well as proper funding for conservation efforts, and a commitment to robust long-term monitoring and research. Without these changes, Australia’s appalling record on conserving its unique marsupial fauna will only get worse.

Cross-References ▶ Impact of Habitat Loss and Fragmentation in Assemblages, Populations, and Individuals of American Marsupials ▶ Multiple Threats Affecting the Marsupials of Australasia: Impacts and Management ▶ Novel Conservation Strategies to Conserve Australian Marsupials

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Marsupials and the Coverage Provided by Protected Areas in Brazil

45

Rafael Loyola, Raísa R. S. Vieira, and Bruno R. Ribeiro

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Data on Marsupial Species Occurring in Brazil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Data on Location of Protected Areas in Brazil . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Marsupial Species Representation in PAs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cross-References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1446 1448 1455 1455 1458 1458

Abstract

The United Nations Convention on Biological Diversity strategic plan to halt biodiversity loss through the achievement of 20 outcome-based targets failed at large. While some targets were partially met, most were not achieved. One of these targets (Aichi Target 11) states that 17% of terrestrial ecosystems should be preserved in situ. Brazil has met such target by means of its wide network of protected areas (PAs), but does this network really protect biodiversity? Here, the effectiveness of the Brazilian current network of PAs and Indigenous Lands (ILs) in representing all known marsupial species occurring in the country was assessed. The results show that species are relatively well covered by these areas, but the authors’ estimates depended on the data type. On average, species were less represented in strict protection PAs (6.3%  4.6%), followed by R. Loyola (*) International Institute for Sustainability, Rio de Janeiro, RJ, Brazil Departamento de Ecologia, Universidade Federal de Goiás, Goiânia, Brazil e-mail: [email protected] R. R. S. Vieira Instituto Internacional para Sustentabilidade, Rio de Janeiro, Brazil B. R. Ribeiro Programa de Pós-graduação em Ecologia e Evolução, Universidade Federal de Goiás, Goiânia, Brazil © Springer Nature Switzerland AG 2023 N. C. Cáceres, C. R. Dickman (eds.), American and Australasian Marsupials, https://doi.org/10.1007/978-3-031-08419-5_28

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sustainable use PAs (13%  8.4%) and ILs (14.4%  16.2%). Evaluating the effectiveness of PAs to biodiversity protection is a fundamental step toward understanding the impact of decision-making and conservation policy. Gap analysis such as the one reported here should be carried out elsewhere to support the establishment of PAs where they are most needed to guarantee the best allocation of scarce conservation resources available. Keywords

Aichi targets · Brazilian mammals · Conservation policy · Gap analysis · Research-implementation spaces

Introduction The increasing human occupation of the Earth’s surface and its resulting impacts on natural ecosystems over the last century have accelerated human-induced species losses (IPBES 2019). Three-quarters of terrestrial environments and about 66% of the marine environment have been significantly altered by human actions (IPBES 2019), and between 1970 and 2014, there was an overall decline of 60% in population sizes of vertebrates (WWF 2018). To curb such threats, protected areas (PAs) still remain as the cornerstone strategy to protect biodiversity and guarantee the continuous provision of ecosystem services to people. The Convention on Biological Diversity (CBD) defined a protected area as “a geographically defined area which is designated or regulated and managed to achieve specific conservation objectives.” CBD signatory parties had agreed to protect 17% of land and inland water and 10% of marine areas by 2020, part of Aichi Target 11 (CBD 2010). Accumulated evidence show that PAs has been effective in reducing deforestation (Andam et al. 2008; Brum et al. 2019) and buffering fire incidence (Nelson and Chomitz 2011), for example. Although the PA coverage targets were not met uniformly around the globe, PAs now cover almost 20 million km2 of terrestrial and inland waters area (UNEPWCMC and IUCN 2020). Hence, considerable progress have been achieved over the last 10 years and new discussions are now underway on the post-2020 Global Biodiversity Framework (Visconti et al. 2019). Brazil, in particular, has one of the largest networks of PAs in the world (Vieira et al. 2019). The country holds 2446 PAs and > 2.5 million km2 under protection, which represents 18.7% of its continental area and 25.5% of its marine territory (CNUC 2020). These figures account for PAs managed by the National System of Protected Areas (SNUC – acronym in Portuguese). The SNUC was constituted in the year 2000 to unify and standardize management of PAs established with nature conservation as their main goal. In the system, there are two main categories of PAs following their management goals: those established for strict protection and those targeted for the sustainable use of natural resources. Currently, strict protection PAs represent 31.8% of reserves in SNUC, and they are

45

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equivalent to the International Union for Conservation of Nature (IUCN) categories Ia, II, and III. Sustainable use PAs represent 68.2% of the network and are equivalent to IUCN categories IV, V and VI. They are managed at the federal, state, and municipal levels. In addition to SNUC PAs, Brazil has other categories of protected areas, such as indigenous lands and a mandatory minimum percentage of natural reserves inside rural private lands (Vieira et al. 2018). Indigenous lands (ILs) are those traditionally occupied by the indigenous peoples of Brazil and are essential for preserving the natural resources needed for their well-being according to their customs and traditions (FUNAI 2020). Brazil has 628 ILs covering an area of about 1.2 million km2 (considering the different phases of the ILs demarcation procedure), which represents nearly 14% of the country’s territory (FUNAI 2020). In the past, ILs were not accounted as areas for biodiversity conservation, however, indigenous peoples are increasingly recognized for contributing to nature conservation and their lands hold a great part of the world’s biodiversity (Garnett et al. 2018; Leiper et al. 2018). Besides protecting their culture and heritage, ILs and other protected areas in the Brazilian Amazon are responsible for inhibiting fires and deforestation (Nepstad et al. 2006) and indigenous-managed lands were slightly richer in vertebrate species than other existing protected areas in Australia, Brazil, and Canada (Schuster et al. 2019), for example. The mechanism behind those results is an active enforcement of legal restrictions on natural resources exploitation, which varies according to the type of land management. Previous studies have evaluated the role of Brazilian PAs in climate change mitigation (Soares-Filho et al. 2010), in avoiding deforestation in the Amazon and the Cerrado (Nolte et al. 2013; Brum et al. 2019) and the degree of biodiversity protection and knowledge within them (Oliveira et al. 2017; Ribeiro et al. 2018a, b). They provide several benefits for species conservation and ecosystem services provision; however, their potential could be even higher (Oliveira et al. 2017; Brum et al. 2019; Resende et al. 2019; Vieira et al. 2019). In Brazil, PA cover is highly heterogeneous across biomes and the vast majority of PAs are located in the Amazon (Vieira et al. 2019). The other five Brazilian biomes have a PA coverage gap and most of their remaining natural habitats are not under legal protection. Further, PAs are not representative for half of the Brazilian ecosystems, a likely outcome due to their establishment biases toward landscapes with least suitability for extractive uses, i.e., their residual nature (Vieira et al. 2019). Nevertheless, PAs will continue to be a key strategy for nature conservation, and the current gaps highlight the need to evaluate their effectiveness for different biodiversity groups and ecosystem services to improve the PAs network. Information on species representation in different PAs categories has been done sporadically (Oliveira et al. 2017; Ribeiro et al. 2018a, b), but it has not been done yet focusing on marsupials. In Brazil, there are 15 genera and 65 species of Didelphidae marsupials, a group that occurs only in the Americas (Abreu-Jr et al. 2020b). They are distributed across all the Brazilian biomes, with the greatest diversity of species found in the dense forests of the Amazon and the Atlantic Forest, a pattern related to the adaptation of most species to arboreal habitats (Melo and Sponchiado 2012). Despite their wide

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distribution in Brazil, little is known about the details of the distribution of marsupials in non-forest biomes (Díaz-Nieto and Voss 2016). The lack of information regarding species geographic range still represents an important barrier in biogeographical studies, as well as to develop specific conservation strategies. Marsupials are among the most threatened species by habitat fragmentation, and there is not enough information about their responses and how to mitigate the impacts (Püttker et al. 2012). Other studies have also shown their vulnerability to climate change (Loyola et al. 2012), and, considering the rise of deforestation rates in Brazil, PAs become even more important for the conservation of these species. In this chapter, the effectiveness of the Brazilian network of PAs (considering sustainable use, strict protection, and ILs as protected areas) in representing the marsupial species was evaluated. Information considering different types of species distribution data to assess biodiversity gaps in Brazil was compiled, to inform future targets and policies regarding marsupial species conservation.

Data on Marsupial Species Occurring in Brazil To assess the coverage of marsupial species occurrence in the Brazilian network of PAs, both species occurrence records and species geographic distribution represented by their available range maps (see also Ribeiro et al. 2018a, b) were used. Both kinds of distribution data were used, given that they offer different, but complementary, information. Occurrence records offer more accurate information on the presence of a species at a specific point in space and time but are often biased toward localities of easy access (e.g., the vicinity of roads and biodiversity facilities; Oliveira et al. 2016). Range maps, on the other hand, provide a big picture of species distribution but are typically affected by the commission error (i.e., the inference about the presence of a species where it does not occur), which can overestimate the measure of species representativeness in PAs (Rodrigues et al. 2004). Occurrence records of marsupial species occurring in Brazil (order Didelphimorphia) from the Global Biodiversity Information Facility (GBIF; www. gbif.org) and speciesLink (www.splink.org.br) databases were downloaded. Range maps were retrieved from the International Union for Conservation of Nature (IUCN; www.iucnredlist.org). To harmonize and adjust species taxonomy, the authors searched for species synonyms in several sources (e.g., Voss and Jansa 2009; Díaz-Nieto et al. 2016; Pavan and Voss 2016; Quintela et al. 2020; Voss et al. 2020) in order to find the valid name recognized in the most up-to-date list of marsupials in Brazil (Abreu-Jr et al. 2020). For occurrence records, fossil records were removed, besides those that did not contain complete information on species taxonomy (i.e., species binomial) or geographical coordinates (i.e., latitude and longitude). Moreover, records with the same name and coordinates information, records in the ocean, assigned to country and state centroids, containing zero coordinates, with equal latitude and longitude

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information, and records in other countries were removed. The clean.coordinates function of the CoordinateCleaner R package (Zizka et al. 2019) was used to do these procedures. Overall, although 65 marsupial species occur in Brazil, only 51 of them have spatially explicit distribution data (Fig. 1). There are species range maps for 45 species, and occurrence records were also compiled for 45 species, most of them sharing the two types of data (Table 1). Most occurrence records were concentrated in the Atlantic Forest with a lower number being found in other Brazilian biomes (Fig. 1).

Fig. 1 Records of 51 species occurring in Brazil and the location of indigenous lands, strict protection, and sustainable use protected areas in the country. Gap species are those not represented in any protected area or indigenous lands. Records for all species are shown together with no discrimination

AF

AM, AF, 4101.2 2.2 CA, CE, PA AM, AF, 1358.6 2.2 CA, CE 65.5 11.3

AM, AF, 3896.2 10.3 CE 1780.4 9.6

LC

LC

LC

Didelphis imperfecta Didelphis marsupialis Glironia venusta

DD

LC

7.5

2.4

1.6

DD

52.6

CE

DD

19.2

19.3

9.1

6.1

4.7

2.0

0.1

7.4

10.0

AM, AF, 2390.7 3.9 CA, CE AF, CE 1144.1 2.2

DD

LC

21.1

7.4

24.5

25.0

77.8

0.5

2.8

0.9

11.1

0.4

11.1

14.2

10.1

Didelphis aurita

Species Caluromys lanatus Caluromys philander Caluromysiops irrupta Chironectes minimus Cryptonanus agricolai Cryptonanus chacoensis Cryptonanus guahybae Didelphis albiventris

% in indigenous lands 15.9

% in sustainable use 8.7

Species range Area % in Threat Brazilian (km2 x strict status Biomes 1000) protection LC AM, AF, 2579.8 4.0 CE LC AM, AF, 2834.2 5.2 CE CR 60.3 9.9

53.3

54.6

98.2

8.8

9.7

5.3

12.8

10

25

38.4

29.5

10.1 –

–

–

– 119

12.9

5.9

100.0

0.0

0.0

217

170

1

1

19

17.6

–

– 17

4.8

62

Occurrence records % sum in % in protected # of strict areas records protection 28.6 27 7.4

–

18.5

–

21.7

22.4

0.0

0.0

0.0

5.9

–

19.4

% in sustainable use 7.4

–

2.5

–

0.9

2.9

0.0

0.0

0.0

5.9

–

0.0

% in indigenous lands 3.7

–

31.1

–

35.5

31.2

100

0

0

29.4

–

24.2

% sum in protected areas 18.5

Table 1 Marsupial species considered in this chapter along with their threat category, geographic distribution, and percentage of representation in indigenous lands, strict protection, and sustainable use protected areas in Brazil

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Gracilinanus agilis Gracilinanus emiliae Gracilinanus microtarsus Hyladelphys kalinowskii Lutreolina crassicaudata Marmosa (Marmosa) murina Marmosa (Micoureus) constantiae Marmosa (Micoureus) demerarae Marmosa (Micoureus) paraguayana Marmosa (Stegomarmosa) lepida Marmosops (Marmosops) incanus Marmosops (Marmosops) neblina

AF, CE

LC

AM

AM, AF, 605.6 CA, CE

AM

LC

LC

LC

385.7

6.8

3.6

2026.2 11.5

3.1

AF, CE

LC

814.7

AM, AF, 6130.9 7.6 CA, CE

LC

DD

LC

AF, CE, 1049.9 2.6 PA AM, AF, 4090.5 9.7 CA, CE, PA CE 335.8 5.2

LC

3.3

0.6

1750.1 11.3

615.8

122.1

2701.6 2.7

LC

LC

AF, CA, CE, PT AM

LC

12.8

7.6

19.8

7.9

14.2

2.0

19.1

6.3

20.7

9.3

36.0

6.0

52.8

0.6

32.1

0.6

16.6

7.6

20.3

1.1

25.9

0.5

0.1

1.2

72.4

11.8

63.4

11.6

38.4

14.8

49.1

10

57.9

13.1

36.7

9.9

14

186

6

58

114

1

163

0.0

23.1

0.0

10.3

14.0

0.0

13.5

4.5

–

– 22

18.8

0.0

11.9

149

1

59

0.0

21.0

0.0

17.2

17.5

0.0

19.6

9.1

–

18.8

0.0

15.3

0.0

0.0

0.0

1.7

0.9

0.0

0.0

0.0

–

0.0

0.0

0.0

Marsupials and the Coverage Provided by Protected Areas in Brazil (continued)

0

44.1

0

29.2

32.4

0

33.1

13.6

–

37.6

0

27.2

45 1451

Species Marmosops (Marmosops) noctivagus Marmosops (Marmosops) paulensis Marmosops (Sciophanes) bishopi Marmosops (Sciophanes) parvidens Marmosops (Sciophanes) pinheiroi Metachirus myosuros Metachirus nudicaudatus Monodelphis (Microdelphys) Americana Monodelphis (Microdelphys) iheringi

AM

AM

AF, CE

AM, AF, 6351.7 7.2 CA, CE AM, AF, 1583.0 1.8 CA, CE

AF

LC

LC

NE

LC

NT

LC

CE

LC

3.6

–

–

679.1

16.5

16.6

213.0

859.0

1522.0 7.2

8.4

8.1

12.8

–

36.3

24.7

10.5

27.9

9.7

AF

VU

74.0

% in sustainable use 22.0

Species range Area % in Threat Brazilian (km2 x strict status Biomes 1000) protection LC AM, CE 1188.4 8.7

Table 1 (continued)

0.5

0.7

17.3

–

8.8

31.7

20.5

0.7

% in indigenous lands 21.3

12.5

10.6

37.3

–

61.6

73

38.2

38.3

20

85

115

29

3

12

1

11

0.0

14.1

14.8

13.8

0.0

0.0

0.0

36.4

Occurrence records % sum in % in protected # of strict areas records protection 52 13 7.7

45.0

27.1

14.8

10.3

0.0

25.0

0.0

54.5

% in sustainable use 23.1

0.0

0.0

5.2

0.0

0.0

0.0

0.0

0.0

% in indigenous lands 0.0

45

41.2

34.8

24.1

0

25

0

90.9

% sum in protected areas 30.8

1452 R. Loyola et al.

Monodelphis (Microdelphys) scalops Monodelphis (Monodelphiops) dimidiata Monodelphis (Monodelphis) arlindoi Monodelphis (Monodelphis) brevicaudata) Monodelphis (Monodelphis) domestica Monodelphis (Monodelphis) glirina Monodelphis (Monodelphis) touan Monodelphis (Mygalodelphys) kunsi Monodelphis (Pyrodelphys) emiliae Philander andersoni Philander canus

AM

AF, CA, CE, PT

AM

AM

AF, CE

AM

AM

CE, PT

LC

LC

LC

LC

LC

LC

LC

NE

1.2

14.2 –

445.6

–

1055.2 3.9

410.7

–

43.3

20.6

1.2

–

20.0

4.2

28.5

–

0.3

0.6

–

84.7

42.8

6.9

–

55.3

11.1

69.7

–

8.1

18.5

7

1

9

5

3

17

23

7

0.0

0.0

0.0

0.0

33.3

5.9

4.3

0.0

0.0

–

–

3

20.8

24

0.0

0.0

0.0

20.0

33.3

47.1

4.3

14.3

33.3

–

20.8

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

0.0

–

4.2

(continued)

0

0

0

20

66.6

53

8.6

14.3

33.3

–

45.8

Marsupials and the Coverage Provided by Protected Areas in Brazil

–

27.2

18.3

4.5

–

–

–

22.8

4.5

1324.3 12.5

3385.9 2.4

1041.2 16.9

24.3

–

–

–

AM

13.3

LC

4.6

5.7

344.6

1025.6 2.1

AF, CA

LC

LC

45 1453

CE

VU

565.5

1.5

1431.4 3.6

AM, CE

LC

5.5

7.6

0.1

7.0

– – 6.3

– – 0.4

NE NE EN

18.0

18.7

AM, AF, 3276.8 9.7 CA, CE AM – – AF – – 62.1 1.3

LC

7.1

18.2

– – 8

46.4

5

3

4 6

66

20.0

0.0

25.0 50.0 –

9.1

Occurrence records % sum in % in protected # of strict areas records protection 50.2 9 0.0

40.0

0.0

0.0 16.7 –

22.7

% in sustainable use 0.0

0.0

0.0

0.0 0.0 –

6.1

% in indigenous lands 0.0

60

0

25 66.7 –

37.9

% sum in protected areas 0

Results are shown for both geographic range and occurrence records. Threat status (ICMBio 2018): Critically endangered (CR), Endangered (EN), Vulnerable (VU), Near threatened (NT), Least concern (LC), Data deficient (DD), Not evaluated (NE). Brazilian biomes in which the species occur: Amazon (AM), Atlantic Forest (AF), Caatinga (CA), Pampa (PA), Pantanal (PT); blank spaces apply to species with no information on their biome occurrence. The following species were not analyzed because they do not have spatial data available for Brazil: Marmosa (Marmosa) macrotarsus, M. (Micoureus) limae, M. (Micoureus) phaea, M. (Micoureus) rapposa, M. (Micoureus) rutteri, Monodelphis (Mygalodelphys) handleyi, M. (Mygalodelphys) pinocchio, M. (Mygalodelphys) saci, M. (Monodelphis) vossi, M. (Monodelphiops) unistriata, Cryptonanus unduaviensis, Gracilinanus peruanus, Marmosops (Marmosops) caucae, and M. (Marmosops) ocellatus

Species Philander mcilhennyi Philander opossum Philander pebas Philander quica Thylamys (Thylamys) macrurus Thylamys (Xerodelphys) karimii Thylamys (Xerodelphys) velutinus

% in indigenous lands 33.7

% in sustainable use 13.2

Species range Area % in Threat Brazilian (km2 x strict status Biomes 1000) protection LC AM 409.5 3.3

Table 1 (continued)

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Data on Location of Protected Areas in Brazil Spatial data were gathered on federal, state, and municipal strict protection and sustainable use PAs (IUCN categories I–III and IV–VII, respectively) from the Brazilian Environmental Ministry website (mapas.mma.gov.br/i3geo/ datadownload.htm). Spatial data on ILs from the National Indigenous Foundation (www.funai.gov.br/index.php/shape) were obtained and the Brazilian ILs were included in the list of currently established PAs (see Fig. 1).

Marsupial Species Representation in PAs The representativeness of species distribution in PAs was assessed by overlapping species distribution data with the distribution of PAs using the function st_intersection of the sf package (Pebesma 2018). “Gap” was considered as those species not represented in any PA (Ribeiro et al. 2018a, b). The total number of occurrence records and the total area of range maps cropped to the limits of Brazil were also used to assess the proportion of each species distribution inside PAs. All analyses and figures were carried out in the software R (R Core Team 2020). The number of species occurring inside PAs varied according to the type of data used in the analysis. When considering range maps, all species have at least part of their distribution in PAs (strict protection, sustainable use, and ILs – Fig. 2). On the other hand, when occurrence records were considered, the number of species drops to 27 in strict protection PAs, 30 in sustainable use PAs, and 10 in ILs (Fig. 3). No gap species were found when looking at species range, but there were 13 species with no record in any PA, most of them in the Amazon biome (Table 1, Fig. 1). The percentage of occurrence records per species varied across the country (Fig. 2). Only 6 species had more than 50% of their records inside these areas, whereas 31 had more than 10% of their records in PAs. The percentage of records varied among species with some having no record at all and others, such as Cryptonanus guahybae, having all their records registered inside PAs (in this case, it is only one record; see Fig. 2, Table 1). The case of C. guahybae is interesting because although being found only in PAs, only ca. 5% of its range is covered by these areas, as shown below (Fig. 3). This situation highlights the importance of considering different types of data in analyses like the one used in this chapter. There were eight species with only one record within strict protection PAs, seven within sustainable use PAs, and six species with only one record within ILs. In addition, there were only 9 species with 10 or more occurrence records within strict protection PAs, 12 within sustainable use Pas, and no species with more than 10 records within ILs. Using species geographic range maps, it was found that, on average, species were less represented in strict protection PAs (6.3%  4.6%), followed by sustainable use PAs (13%  8.4%) and ILs (14.4%  16.2%). Percentage of coverage also varied considerably. For example, while Didelphis imperfecta had nearly all of its distribution represented in PAs, the species C. guahybae had only ca. 5% covered by these

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Fig. 2 Percentage of occurrence records for marsupial species occurring in indigenous lands, strict protection, and sustainable use protected areas in Brazil. The following species were not analyzed because they do not have spatial data available for Brazil: Marmosa (Marmosa) macrotarsus, M. (Micoureus) limae, M. (Micoureus) phaea, M. (Micoureus) rapposa, M. (Micoureus) rutteri, Monodelphis (Mygalodelphys) handleyi, M. (Mygalodelphys) pinocchio, M. (Mygalodelphys) saci, M. (Monodelphis) vossi, M. (Monodelphiops) unistriata, Cryptonanus unduaviensis, Gracilinanus peruanus, Marmosops (Marmosops) caucae, and M. (Marmosops) ocellatus

areas. Thirteen species had more than 50% of their distribution covered by PAs; most of them occurring in the Brazilian Amazon. For more details, see Fig. 3 and Table 1. Evaluating the effectiveness of PAs to biodiversity protection is a fundamental step toward understanding the positive impact of environmental decision-making and conservation policy (Ferraro and Pressey 2015). In Brazil (Vieira et al. 2019) and in other parts of the world (Ferraro and Pressey 2015), PAs tend to be residual; that is, they have been consistently established on marginal lands that minimize costs and conflicts with extractive uses instead of focusing on places important to biodiversity. It has been shown that Brazilian PAs do not do a good job in protecting plant species, given that 33% of all threated species still lie completely outside those areas (Ribeiro et al. 2018a, b), although they have been proven to be effective in refraining deforestation, at least in the Amazon (Nolte et al. 2013) and the Cerrado (Brum et al. 2019). As for whole ecosystems, nearly half of them are currently underrepresented in PAs (Vieira et al. 2019).

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Fig. 3 Percentage of marsupial species geographic range overlapping with indigenous lands, strict protection, and sustainable use protected areas (PAs) in Brazil. Species with no bar had no records registered inside PAs. The following species were not analyzed because they do not have spatial data available for Brazil: Marmosa (Marmosa) macrotarsus, M. (Micoureus) limae, M. (Micoureus) phaea, M. (Micoureus) rapposa, M. (Micoureus) rutteri, Monodelphis (Mygalodelphys) handleyi, M. (Mygalodelphys) pinocchio, M. (Mygalodelphys) saci, M. (Monodelphis) vossi, M. (Monodelphiops) unistriata, Cryptonanus unduaviensis, Gracilinanus peruanus, Marmosops (Marmosops) caucae, M. and (Marmosops) ocellatus

Being the first investigation to analyze the formal protection of marsupial species, the current results suggest that PAs in Brazil do cover the distribution of marsupials reasonably well as the authors found few or none gap species (depending on the type of data being considered), although average coverage of species geographic range is still poor in strict protection PAs. However, the present analyses do not cover severe threats that menace marsupial species in Brazil, in particular climate change and deforestation. The authors have previously alerted that marsupials in Brazil might lose considerable portions of their geographic range owing to climate change (Loyola et al. 2012). The case is particularly true for the Brazilian Atlantic forest (Vale et al. 2020), a biome that is already severely threatened by changes in its climatic regime and that might suffer more pressure with the climate crisis (Scarano 2019). The biome is also home for most marsupial species in Brazil, where patches of native vegetation can protect them and support their populations (Bovendorp et al. 2019). In this case, the

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role of native vegetation cover (Rezende et al. 2018), restoration (Strassburg et al. 2019), and areas formally protected are incommensurable, although studies suggest that PAs might not be able to counterbalance the effects of climate change for other vertebrates (Lemes et al. 2013) or even invertebrates (Ferro et al. 2014). In the Cerrado, conversion of native vegetation to agriculture is the biggest threat (Strassburg et al. 2017; Borges et al. 2019), and it applies to marsupial species (Loyola et al. 2012). In the Amazon, deforestation and climate change imperil marsupials as well as other mammals (Ribeiro et al. 2018a, b; Sales et al. 2019). Hence, climate change and deforestation, both inside and outside Pas, should be considered as a silent threat to marsupial species survival and might reduce the optimism found in the current results. Brazil is home for 65 marsupial species (Abreu-Jr et al. 2020) ranging from small (ca. 10 g) to large species (ca. 3 kg) distributed mostly in forest areas such as the Amazon and the Atlantic Forest (Cáceres and Monteiro-Filho 2006). However, the scientific community still faces knowledge gaps about this group, which reinforces the importance of evaluating their taxonomy, distribution, threat status, and representation inside PAs, ILs, and also other formally protected areas in Brazil, such as the native vegetation protected within private lands (see Brancalion et al. 2016 and Vieira et al. 2018 for a discussion about these areas). To take the next step in decision-making for biodiversity conservation, it is fundamental to know how current actions and strategies are performing. Additional measures, such as habitat restoration, can complement PAs and achieve more impactful outcomes in marsupial conservation. Simultaneously, investments in the PA network and in biodiversity inventories in poorly sampled PAs and biomes need to be expanded. Gap analysis such as the one it is reported here should be carried out elsewhere to support the establishment of PAs where they are most needed the guarantee the best allocation of scarce conservation resources available.

Cross-References ▶ Conservation Biogeography of Living American Marsupials: Didelphimorphia, Microbiotheria, and Paucituberculata ▶ Impact of Habitat Loss and Fragmentation in Assemblages, Populations, and Individuals of American Marsupials ▶ Multiple Threats Affecting the Marsupials of Australasia: Impacts and Management

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Human-Wildlife Interactions in Urban Areas: Case of Didelphis aurita

46

Stephanie Santos Simioni, Fernando Silve´rio Ribeiro, Renata Pardini, and Thomas Pu¨ttker

Contents Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Study Area . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Quantifying Human-D. aurita Interactions and Their Spatial Drivers . . . . . . . . . . . . . . . . . . . . Data Analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Cross-References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

1464 1466 1466 1467 1468 1470 1470 1478 1479

Abstract

Research has shown that human-wildlife conflicts represent critical conservation challenges in rural settings. Despite intense urbanization, and the disconnection from nature that comes with it, those conflicts are yet to be studied in urban settings. To start closing that gap, this chapter focuses on the black-eared opossum (Didelphis aurita) – a common, synanthropic marsupial endemic to the Atlantic Forest – as a model to explore the drivers of human-wildlife interactions in one of the largest cities worldwide, the metropolis of São Paulo in Brazil. Using data from São Paulo Wildlife Rehabilitation Center, the

S. S. Simioni · R. Pardini Departamento de Zoologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil F. S. Ribeiro Departamento de Ecologia, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil T. Püttker (*) Departamento de Ciências Ambientais, Universidade Federal de São Paulo, Diadema, SP, Brazil e-mail: [email protected] © Springer Nature Switzerland AG 2023 N. C. Cáceres, C. R. Dickman (eds.), American and Australasian Marsupials, https://doi.org/10.1007/978-3-031-08419-5_29

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relative importance of vegetation cover, density of roadside trees, and human population density were tested on the frequency of both direct (encounters with humans) and indirect (injuries caused by infrastructure or domestic animals) human-D. aurita interactions. The frequency of interactions was overall high and explained by the synergistic effect of vegetation cover and human density. The positive effect of vegetation cover on the frequency of interactions was only observed in densely populated areas of the city. The current results corroborate the importance of marsupials to human-wildlife interactions in Neotropical cities and highlight the relevance of prioritizing preventive measures to minimize impacts of negative human-wildlife interactions in vegetated, densely populated urban areas. Keywords

Urban ecology · Human-wildlife conflict · Didelphids · Urban parks · Urban trees · Domestic dogs

Introduction Human-wildlife interactions are either positive or negative impacts that humans and wildlife may cause on each other (Frank 2016). The result of these interactions depends on different factors. Prior experiences, beliefs, and attitudes, all of which shape people’s behavior, can lead either to the perception of a conflict that may result in persecution (negative direct interaction) or to tolerance and coexistence (Frank 2016). Besides these direct human-wildlife interactions, indirect interactions resulting from human infrastructure and/or activities such as collisions with buildings (Loss et al. 2015), roadkills (Monge-Najera 2018), injuries from the power grid (Bernardino et al. 2018), and predation by dogs (Ribeiro et al. 2019) are common and have potentially severe negative consequences to wildlife. Human-wildlife interactions have been the focus of numerous studies (Torres et al. 2018), many of which have been carried out in rural areas, where wildlife is more diverse and abundant. In these rural settings, wildlife attacks on crops and livestock frequently lead to economic losses that negatively impact human livelihoods, and to human persecution that has threatened many species (Ripple et al. 2014). However, two aspects indicate the relevance of studying human-wildlife interactions in urban settings. On the one hand, ongoing urbanization is increasing the size of cities as well as the population density within cities on a global scale (Seto et al. 2012), leading to an increase in the number of people interacting with urban wildlife. On the other hand, this urbanization process is known to trigger a disconnection of people from nature (Shanahan et al. 2010), leading to negative changes in attitude toward nature, wildlife, and conservation (Whitburn et al. 2019). Indeed, human-wildlife interactions within urban areas have increased in the last decades (Soulsbury and White 2015). Further, although most studies on human-wildlife

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interactions in urban context focus on negative interactions (Soulsbury and White 2015), there is increasing recognition of the possible benefits of wildlife in urban areas (e.g., Markandya et al. 2008). The city of São Paulo in Brazil is one of the largest metropolitan areas globally and represents an extreme example of the complexity and heterogeneity of urban environments. São Paulo is the financial-, commercial-, and business center of Brazil and South America, and the most populous city in the Southern Hemisphere. At the same time, 22% of Sao Paulo’s municipal area is covered by forest remnants, including one of the largest urban forests in the world – the Cantareira State Park (SMA 2012), and the city is surrounded by large tracks of forest. These characteristics make the city a good model for investigating the factors driving the frequency of human-wildlife interactions in urban areas. Large opossums (genus Didelphis) are medium-sized generalist marsupials that are commonly encountered in urban areas across the Americas (Cáceres 2000; Souza et al. 2012; Wright et al. 2012; Abreu 2013; Gentile et al. 2018). Didelphis spp. are synanthropic omnivores able to benefit from anthropogenic resources within cities, as evidenced by their ability to maintain a larger body mass and smaller home ranges in cities compared to rural environments (Wright et al. 2012). Encounters between humans and Didelphis spp. are common, and citizens’ perception of these mammals seems to be mostly negative (Abreu 2013). In the city of São Paulo, the most abundant large New World opossum is D. aurita, which is endemic to the Atlantic Forest but widely distributed within its boundaries, occurring from the Northeast of Brazil to Northern Argentina (Wilson and Reeder 2005). Didelphis aurita is a generalist, onivorous species (Cáceres and Monteiro-Filho 2001; Cáceres 2004), with low vulnerability to forest fragmentation (Püttker et al. 2012), and frequently encountered in periurban and urban environments throughout its distributional range (e.g., Stabenow et al. 2012). Encounters between citizens and D. aurita are the most common human-mammal interaction in São Paulo city (S. S. Simioni, unpublished data). Based on these characteristics, D. aurita represents a promising model species for investigating human-wildlife interactions in São Paulo. Successful implementation of measures to mitigate negative human-wildlife interactions in cities depends on understanding the spatial drivers of these interactions across the heterogeneous and complex mosaics of urban areas. It is reasonable to expect that the frequency of human-wildlife interactions will vary according to the size of both wildlife and human populations. If this is the case, relevant spatial drivers of the distribution of such interactions should be those quantifying vegetation or tree cover (which represent the source of wildlife populations) and human population density. Using a large database provided by the Wildlife Rehabilitation Center of São Paulo, the relative importance of vegetation cover (quantified considering different types of vegetation), number of roadside trees, and human population density were investigated on the frequency of direct and indirect interactions between citizens and D. aurita.

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Methods Study Area São Paulo is the capital of the state of São Paulo, which is located in the Southeast region of Brazil (Fig. 1) and is the country’s most populous state, concentrating the majority of its industrial production and gross domestic product. The municipality of São Paulo harbors more than 12 million people and is the center of the metropolitan region of São Paulo, which includes 39 municipalities and harbors 21.5 million people (IGBE 2017). Although the Human Development Index of the municipality is high (0.805), there is large social inequality across its 96 districts (Rede Nossa São Paulo 2016). Of the 1509 km2 of the municipality, 30.4% (459 km2) is covered by native vegetation, including dense ombrophilous forest, heterogeneous forest (representing a mix of native and exotic species), flooded forest, montane grasslands, and floodplains with aquatic vegetation (SVMA 2016). Green areas (areas with native or exotic arboreal, shrub or grass cover with ecological, scenic or recreational function) such as urban squares and parks and protected areas (areas legally destined to conservation) within the city cover 160 km2 (SVMA 2014). However, the amount

Fig. 1 (a) Brazil with the location of São Paulo state; (b) São Paulo state with the location of São Paulo municipality; (c) distribution of native forest, heterogeneous forest, and all other non-arboreal native vegetation and green areas in São Paulo municipality together with the locations of direct and indirect human-Didelphis aurita interactions; (d) human population density together with direct and indirect human-D. aurita interactions; (e) detail of (c) showing the distribution of roadside trees across one sampling unit (red square in c); squares within the limits of the municipality in (c) and (d) represent sampling units. All white areas in (c) and (e) represent urban land use

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of public green spaces per inhabitant is extremely variable across the city (Rede Nossa São Paulo 2016). The wildlife rehabilitation center in São Paulo municipality is the Technical Division for Veterinary Medicine and Wildlife Management (Divisão Técnica de Medicina Veterinária e Manejo da Fauna Silvestre; DEPAVE-3), founded in 1993 as a department of the Municipal Secretary for Green Areas and the Environment (Secretaria Municipal do Verde e do Meio Ambiente, SVMA). DEPAVE-3 is responsible for surveying and monitoring wildlife in the municipality, as well as receiving, treating, rehabilitating, and reallocating wildlife. It is also responsible for developing and enforcing policies and procedures aiming at wildlife conservation. According to DEPAVE-3 surveys, 105 mammal species occur in São Paulo municipality, with many large, rare, and endangered species restricted to the extreme South of the city, where native forest fragments are connected to one of the largest remaining tracks of Atlantic Forest, the Serra do Mar (SVMA 2017).

Quantifying Human-D. aurita Interactions and Their Spatial Drivers The dataset used in this chapter comprises D. aurita records by DEPAVE-3 from January to December 2017 (the only year for which data has been fully organized and checked). Records comprise information on animals that were either taken into custody following a request by citizens or brought to the center by citizens. Besides information on clinical diagnoses, treatment, and destination after treatment (not used in this study), each record includes the geographic coordinates where the animal was found, and the reason for DEPAVE-3 taking action. That was classified into two broad categories: “conflict” and “trauma.” Records classified as “conflict” are the result of direct human-wildlife interactions, including all healthy animals that caused discomfort, distress, or fear in people, including opossums falsely considered sick or injured, as well as those considered dangerous or unwelcome. On the other hand, records classified as “trauma” are the result of indirect human-wildlife interactions, including animals injured in accidents involving the power grid, roadkills, or preyed on by dogs. Three response variables were considered, representing three different counts (frequencies) of human-D. aurita interactions: (1) the number of all interactions (including both direct and indirect interactions), (2) the number of direct interactions, and (3) the number of indirect interactions. The explanatory variables comprise four different measures of vegetation cover as well as human population density. Human population density was extracted from a database provided by the Instituto Brasileiro de Geografia e Estatistica (IGBE 2017). This database comprises a layer with the estimated number of inhabitants in 200
200 m cells, which was first rasterized (50
50 m pixels) and then divided the value attributed to each pixel by the number of pixels per cell. To investigate the importance of different types of urban vegetation as a source for D. aurita populations, vegetation cover was measured using four different (but related) variables, quantified according to public information provided by the São Paulo City government:

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(a) Native forest: cover of native forests including dense ombrophilous forest and flooded forest (SVMA 2016). (b) Any forest: cover of forests including both native forest (as in “a”) plus heterogeneous forest (mixing both native and exotic trees) (SVMA 2016). (c) Any vegetation: cover of all types of vegetated areas including native forest and heterogeneous forest (as in “b”) plus all non-arboreal native vegetation (montane grasslands and floodplains with aquatic vegetation) and all green areas (areas with native or exotic arboreal, shrub, or grass cover) such as public squares and parks, private green areas, and cemeteries (Centro de Estudos da Metrópole 2018; SVMA 2016). (d) Roadside trees: number of trees along streets (Prefeitura de São Paulo 2016). To quantify both the frequency of human-D. aurita interaction and its spatial drivers (as described above), the city was defined into contiguous 4
4 km squares. The size of these sampling units represents a trade-off between avoiding too many sampling units with no interactions (when using smaller sampling units) and capturing variation in the number of interactions across sampling units (which decreases with increasing size of sampling units). Only sampling units with 50% of the area within the municipality were considered (Fig. 1), resulting in 98 sampling units, 73.7% of which had at least one human-D. aurita interaction. Response as well as explanatory variables varied considerably among sampling units (Table 1). All variables were calculated in R (R Core Team 2016).

Data Analysis For each of the three response variables, a set of 14 generalized linear models was compared, comprising: a reference model (including only the intercept), five simple models including each of the five explanatory variables alone (four vegetation cover variables – native forest, any forest, any vegetation, number of roadside trees – and population density), four multiple models including each of the four vegetation cover variables plus population density, and four interaction models that consider the interaction between each of the four vegetation cover variable and population density. No severe multicollinearity was detected among explanatory variables included in the same model (variance inflation factors