Status of Conservation and Decline of Amphibians: Australia, New Zealand, and Pacific Islands

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STATUS OF CONSERVATION AND DECLINE OF AMPHIBIANS

© CSIRO 2018 All rights reserved. Except under the conditions described in the Australian Copyright Act 1968 and subsequent amendments, no part of this publication may be reproduced, stored in a retrieval system or transmitted in any form or by any means, electronic, mechanical, photocopying, recording, duplicating or otherwise, without the prior permission of the copyright owner. Contact CSIRO Publishing for all permission requests. A catalogue record for this book is available from the National Library of Australia. Published by CSIRO Publishing Locked Bag 10 Clayton South VIC 3169 Australia Telephone: +61 3 9545 8400 Email: [email protected] Website: www.publish.csiro.au Front cover: (top) Neobatrachus sutor, Stephen Mahony; (bottom) mountain ash forest, David Blair; (thumbnails, left to right) Cornufer vogti, Robert Fisher, U.S. Geological Survey; Notaden nicholsii, Stephen Mahony; Leiopelma archeyi, Phil Bishop Back cover: (left to right) Cyclorana platycephela, Stephen Mahony; Litoria cyclorhyncha, JD Roberts; Myobatrachus gouldii, Stephen Mahony Set in 10/13 Adobe Minion Pro and ITC Stone Sans Edited by Peter Storer Cover design by James Kelly Typeset by Desktop Concepts Pty Ltd, Melbourne Index by Max McMaster Printed in China by 1010 Printing International Ltd CSIRO Publishing publishes and distributes scientific, technical and health science books, magazines and journals from Australia to a worldwide audience and conducts these activities autonomously from the research activities of the Commonwealth Scientific and Industrial Research Organisation (CSIRO). The views expressed in this publication are those of the author(s) and do not necessarily represent those of, and should not be attributed to, the publisher or CSIRO. The copyright owner shall not be liable for technical or other errors or omissions contained herein. The reader/user accepts all risks and responsibility for losses, damages, costs and other consequences resulting directly or indirectly from using this information. Original print edition: The paper this book is printed on is in accordance with the rules of the Forest Stewardship Council ®. The FSC® promotes environmentally responsible, socially beneficial and economically viable management of the world’s forests.

AMPHIBIANS STATUS OF CONSERVATION AND DECLINE OF

AU S T R A L I A , N E W Z E A L A N D, A N D PAC I F I C I S L A N D S

Editors: Harold Heatwole and Jodi J. L. Rowley

Dedication

The name of Dr Harold (Hal) Cogger has been synonymous with Australian herpetology for several generations. His monumental treatise Reptiles & Amphibians of Australia won the coveted Whitley Award and has been the mainstay of professionals, and an inspiration for amateur herpetologists and naturalists. Not only is it a classic work – seldom, if ever, equalled for any other geographic region – but he has revised it frequently so that it has served as a continuous, authoritative, publicly available source of the latest information on the frogs, lizards, snakes, turtles, and crocodiles of Australia. The first edition in 1975 listed the 664 species then known for the country. The discovery of new species, at least five described by Dr Cogger himself, has burgeoned over the decades since then, with seven successive editions sequentially yielding additional species, until the latest one in 2014 was double in size and peaked at 1218 species! Without this manual, it would have been nearly impossible for even the professional herpetologist to keep abreast of so many advances in knowledge, or to be able to readily identify species encountered in the field. Dr Cogger is an excellent photographer and he took all but a few of the more than 840 coloured pictures gracing his guide. This book alone constitutes a lasting legacy of enormous proportions, but it is merely one of his many achievements. In collaboration with his assistant, Elizabeth Cameron, and his wife Heather Cogger, he (1983) produced a catalogue Amphibia and Reptilia as the first volume of the Zoological Catalogue of Australia. In addition to these books, he has published about 160 professional scientific articles. His thorough knowledge of the Australian herpetofauna is evident in his treatment of amphibians in Chapter 2 of the present volume. He has had one genus (Coggeria), seven species (Coggeria naufragus, Ctenotus coggeri, Lampropholis coggeri, Oedura coggeri, Aprasia haroldi, Delma haroldi, Lerista haroldi, and one subspecies, Amphibolurus nobbi coggeri of lizard, as well as one species of sea snake, Hydophis coggeri, named in his honour. Harold Cogger is a consummate field biologist with wide experience in New Guinea and Australia and its islands (Cape York, Swain Reefs, Central Australia, Arnhem Land, Cocos-Keeling, Torres Straits, Ashmore Reef). He has participated in various international field expeditions: for example, to Australasia to study sea snakes aboard the Alpha Helix, a vessel of Scripps

Institution of Oceanography, on two expeditions, as well as several expeditions sponsored by the Japanese Ministry of Science, Education, and Culture to study sea snakes in the western and south-western Pacific. These expeditions were memorable for the comradery among the participants from Japan, France, Australia, and the United States. Hal Cogger started out as a cadet preparator at the Australian Museum in 1952 and rose through the ranks of that institution progressively as Assistant Curator (birds, reptiles, and amphibians), Curator (reptiles and amphibians), Senior Research Scientist, and Deputy Director. He retired in 1995 but has remained active in research as a John Evans Memorial Fellow of the Australian Museum up to the present and was Conjoint Professor in Sustainable Resource Management at the University of Newcastle from 1997 until 2002. Many of his later contributions have been in the field of conservation as: Chairman of the Australasian Reptile and Amphibians Specialist Group, Survival Commission, International Union of the Conservation of Nature (1991–2000); Chairman of the Australian Biological Resources Study Advisory Committee (1992–1997); member of the Endangered Fauna (Interim Protection) Act 1991 Scientific Committee (1992–1995); and the Australian Biological Diversity Advisory Committee (1991–1993). He was the lead researcher and the author of the Action Plan for Australian Reptiles in 1993. In modern times, scientists often are competitive, but Harold Cogger treats science as a cooperative venture and generously and freely shares his knowledge, expertise, and enthusiasm about reptiles and amphibians. His immersion in his chosen field is perhaps best measured by his expression on one occasion that ‘You haven’t really lived until you’ve heard a full-throated chorus of frogs’. A glimpse of what stimulated Hal Cogger to embark on such a successful career and develop exuberance for the hobby he turned into a profession is captured by a published interview with him by Neville Burns in 2014. I have kept secret the fact that I planned to honour Hal by dedicating this book to him. The first he will be aware of it is when he opens his personal copy and stares at his own face peering from the page! Harold Heatwole 1 August 2017

Contents This book is part of the Amphibian Biology series, Volume 11, Status of Conservation and Decline of Amphibians: Eastern Hemisphere. The chapters in this book (Chapters 1–14) are consecutive chapters in Part 6 (Australia, New Zealand, and Pacific Islands); numbers of chapters in parentheses (68–81) are the same chapters numbered consecutively across all parts of Volume 11. Dedication iv Contents of Previous Parts of Volume 11

viii

Contributors to Part 6

xiii

Preface xv

Chapter 1 (68).

Introduction

1

Harold Heatwole and Jodi J. L. Rowley

Chapter 2 (69).

A Brief Demographic Overview of Australia’s Native Amphibians

5

Harold G. Cogger

Chapter 3 (70).

Status of Decline and Conservation of Frogs in the Wet Tropics of Australia

15

Ross A. Alford and Jodi J. L. Rowley

Chapter 4 (71).

Frogs of the Monsoon Tropical Savannah Regions of Northern Australia

23

Graeme R. Gillespie and J. Dale Roberts

Chapter 5 (72).

An Update on Frog Declines from the Forests of Subtropical Eastern Australia

29

David Newell

Chapter 6 (73).

Frog Declines and Associated Management Response in South-eastern Mainland Australia and Tasmania

39

David Hunter, Nick Clemann, David Coote, Graeme R. Gillespie, Greg Hollis, Ben Scheele, Annie Philips, and Matt West

Chapter 7 (74).

The Status of Decline and Conservation of Frogs in Temperate Coastal South-eastern Australia

59

Frank Lemckert and Michael Mahony

Chapter 8 (75).

Conservation of Frogs in South-western Australia J. Dale Roberts

73

Contents

Chapter 9 (76).

The Status of Decline and Conservation of Frogs in the Arid and Semi-arid Zones of Australia

91

Joanne Ocock and Skye Wassens

Chapter 10 (77). The Impact of an Invasive Amphibian: The Cane Toad Rhinella marina 107 Richard Shine

Chapter 11 (78).

The Role of Ex-Situ Amphibian Conservation in Australia

125

Michael S. McFadden, Deon Gilbert, Kay Bradfield, Murray Evans, Gerry Marantelli, and Philip Byrne

Chapter 12 (79).

Conservation of Frogs in Australia: State and Federal Laws

141

J. Dale Roberts

Plates

153

Chapter 13 (80).

185

Status of Decline and Conservation of Frogs in New Zealand Ben D. Bell and Phillip J. Bishop

Chapter 14 (81).

Amphibians of the Pacific: Natural History and Conservation

201

George R. Zug and Robert N. Fisher Index 213

vii

Contents of previous parts of Volume 11, Amphibian Biology: Eastern Hemisphere PART 1.

CONSERVATION BIOLOGY OF AMPHIBIANS OF ASIA (EDITED BY HAROLD HEATWOLE AND INDRANEIL DAS), 2014. NATURAL HISTORY PUBLICATIONS (BORNEO), KOTA KINABALU. HARDBACK.

Chapter 1.

Changes in Amphibian Populations in the Commonwealth of Independent States (Former Soviet Union) Sergius L. Kuzmin and C. Kenneth Dodd Jr.

Chapter 2.

Status of Conservation and Decline of Amphibians of Mongolia Sergius L. Kuzmin

Chapter 3.

Diversity and Conservation Status of Chinese Amphibians Jianping Jiang, Feng Xie, and Cheng Li

Chapter 4.

The Conservation of Amphibians in Korea Daesik Park, Mi-Sook Min, Kelly C. Lasater, Jae-Young Song, Jae-Hwa Suh, Sang-Ho Son, and Robert H. Kaplan

Chapter 5.

Conservation Status of Japanese Amphibians Masafumi Matsui

Chapter 6.

Status and Decline of Amphibians of Afghanistan Indraneil Das

Chapter 7.

Amphibians of Pakistan and their Conservation Status Muhammad Sharif Khan

Chapter 8.

Status and Decline of Amphibians of India Indraneil Das and Sushil K. Dutta

Chapter 9.

Sri Lankan Amphibians: Extinctions and Endangerment Rohan Pethiyagoda, Kelum Manamendra-Arachchi, and Madhava Meergaskumbura

Chapter 10.

Amphibians of the Maldives Archipelago Indraneil Das

Chapter 11.

Status, Distribution, and Conservation Issues of the Amphibians of Nepal Karan B. Shah

Chapter 12.

Status of Amphibian Studies and Conservation in Bhutan Indraneil Das

Contents of previous parts of volume 11

Chapter 13.

Status, Distribution and Conservation of the Amphibians of Bangladesh A. H. M. Ali Reza

Chapter 14.

Amphibian Conservation: Myanmar Guinevere O. U. Wogan

Chapter 15.

Decline of Amphibians in Thailand Yodchaiy Chuaynkern and Prateep Duengkae

Chapter 16.

Amphibian Conservation in Vietnam, Laos, and Cambodia Jodi J. L. Rowley and Bryan L. Stuart

Chapter 17.

Conservation Status of the Amphibians of Malaysia and Singapore Indraneil Das, Norsham Yaakob, Jeet Sukumaran, and Tzi Ming Leong

Chapter 18.

Conservation Status of the Amphibians of Brunei Darussalam T. Ulmar Grafe and Indraneil Das

Chapter 19.

Status and Conservation of Philippine Amphibians Arvin C. Diesmos, Angel C. Alcala, Cameron D. Siler, and Rafe Brown

Chapter 20.

Human Impact on Amphibian Decline in Indonesia Djoko T. Iskandar

Chapter 21.

Amphibians of Timor-Leste: a Small Fauna under Pressure. Hinrich Kaiser, Mark O’Shea, and Christine M. Kaiser

Chapter 22.

Status and Diversity of the Frogs of New Guinea Allen Allison

PART 2.

STATUS OF CONSERVATION AND DECLINE OF AMPHIBIANS: NORTHERN AFRICA (EDITED BY STEPHEN D. BUSACK AND HAROLD HEATWOLE), 2013. BASIC AND APPLIED HERPETOLOGY, ASOCIACIÓN HERPETOLÓGICA ESPAÑOLA, MADRID. PAPERBACK.

Chapter 23.

Introduction. Harold Heatwole and Stephen D. Busack

Chapter 24.

Amphibian Conservation in Mauritania José Manuel Padial, Pierre-André Crochet, Philippe Geniez, and José Carolos Brito

Chapter 25.

Amphibians of Morocco, including Western Sahara: A Status Report Ricardo Reques, Juan M. Pleguezuelos, and Stephen D. Busack

Chapter 26

Diversity and Conservation of Algerian Amphibian Assemblages José A. Mateo, Philippe Geniez, and Jim Pether

Chapter 27.

Conservation Status of Amphibians in Tunisia Nabil Amor, Mohsen Kalboussi, and Khaled Said

ix

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Status of Conservation and Decline of Amphibians

Chapter 28.

Amphibians in Libya: A Status Report Adel A. Ibrahim

Chapter 29.

Amphibians of Egypt: A Troubled Resource Adel A. Ibrahim

Chapter 30.

Withdrawn

PART 3.

STATUS OF CONSERVATION AND DECLINE OF AMPHIBIANS: WESTERN EUROPE (EDITED BY HAROLD HEATWOLE AND JOHN W. WILKINSON), 2013. PELAGIC PUBLISHING, EXETER, UK. PAPERBACK.

Chapter 31.

Infectious Diseases that May Threaten Europe’s Amphibians Trent W. J. Garner, An Martel, Jon Bielby, Jaime Bosch, Lucy G. Anderson, Anna Meredith, Andrew A. Cunningham, Matthew C. Fisher, Daniel A. Henk, and Frank Pasmans

Chapter 32.

Conservation and Declines of Amphibians in Ireland Ferdia Marnell

Chapter 33.

Amphibian Declines and Conservation in Britain John W. Wilkinson and Richard A. Griffiths

Chapter 34.

Conservation and Declines of Amphibians in The Netherlands Anton Stumpel

Chapter 35.

Amphibian Declines and Conservation in Belgium. Dirk Bauwens and Gerald Louette

Chapter 36.

Amphibian Declines and Conservation in France Jean-Pierre Vacher and Claude Miaud

Chapter 37.

Conservation and Declines of Amphibians in Spain Cesar Ayres

Chapter 38.

Conservation and Declines of Amphibians in Portugal Rui Rebelo, Maria José Domingues Castro, Maria João Cruz, José Oliveira, José Teixeira, and Eduardo Crespo

PART 4.

STATUS OF CONSERVATION AND DECLINE OF AMPHIBIANS: SOUTHEASTERN EUROPE AND TURKEY (EDITED BY HAROLD HEATWOLE AND JOHN W. WILKINSON), 2015. PELAGIC PUBLISHING, EXETER, UK. PAPERBACK.

Chapter 39.

The Amphibians of the Italian Region: a Review of Conservation Status Franco Andreone

Chapter 40.

Amphibian Conservation and Declines in Malta Patrick J. Schembri

Chapter 41.

Conservation and Declines of Amphibians in Croatia Olga Jovanovic and Dušan Jelić

Contents of previous parts of volume 11

Chapter 42.

Conservation and Declines of Amphibians in Slovenia David Stanković, Martina Lužnik, and Katja Poboljšaj

Chapter 43.

Conservation and Decline of European Amphibians: The Republic of Serbia Jelka Crnobrnja-Isailović and Momir Paunović

Chapter 44.

Amphibian Declines and Conservation in Montenegro Ruža Ćirović

Chapter 45.

Amphibian Declines and Conservation in Bosnia-Herzegovina Avdullahu Adrović

Chapter 46.

Conservation and Protection Status of Amphibians in Macedonia Bogoljub Sterijovski

Chapter 47.

Amphibians of Albania Idriz Haxhiu

Chapter 48.

Declines and Conservation of Amphibians in Greece Konstantinos Sotiropoulos and Petros Lymberakis

Chapter 49.

Amphibian Conservation and Decline in Romania Dan Cogălniceanu and Laurenţiu Rozylowicz

Chapter 50.

Conservation and Decline of Amphibians in Hungary Judit Vörös, István Kiss, and Miklós Puky

Chapter 51.

Conservation and Declines of Amphibians in Bulgaria Nikolay Dimitrov Tzankov and Georgi Sashev Popgeorgiev

Chapter 52.

Amphibian Conservation and Decline in Turkey Kurtuluş Olgun and Nazan Taşkın Üzüm

Chapter 53.

Conservation of Amphibians in Cyprus Petros Lymberakis, Haris Nicolaou, and Konstantinos Sotiropoulos

PART 5.

STATUS OF CONSERVATION AND DECLINE OF AMPHIBIANS: NORTHERN EUROPE (EDITED BY HAROLD HEATWOLE AND JOHN W. WILKINSON. PELAGIC PUBLISHING, EXETER, UK, IN PROGRESS.

Chapter 54.

Status and Conservation of Amphibians in Luxembourg Laura Wood, Edmee Engel, Richard A. Griffiths, Roland Proess, and Laurent Schley

Chapter 55.

Germany (in progress) Richard Podloucky and Andreas Nöllert

Chapter 56.

Conservation and Declines of Amphibians in Poland Maciej Pabijan and Maria Ogielska

xi

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Status of Conservation and Decline of Amphibians

Chapter 57.

Amphibian Conservation in Switzerland Benedikt R. Schmidt and Silvia Zumbach

Chapter 58.

Amphibian Declines and Conservation in Austria Marc Sztatecsny

Chapter 59.

Conservation and Decline of European Amphibians: The Czech Republic Lenka Jeřábková, Martin Šandera, and Vojtech Baláž

Chapter 60.

Amphibian Declines and Conservation in Slovakia Ján Kautman and Peter Mikuliček

Chapter 61.

Conservation Status of Amphibians in Norway Leif Yngve Gjerde

Chapter 62.

Conservation Measures and Status of Amphibians in Sweden Claes Andrén

Chapter 63.

Decline and Conservation of Amphibians in Finland Ville Vuorio and Jarmo Saarikivi

Chapter 64.

Decline and Conservation of Amphibians in Estonia Riinu Rannap

Chapter 65.

Decline and Conservation of Amphibians in Latvia Aija Pupina, Mihails Pupins, Andris Ceirans, and Agnese Pupina

Chapter 66.

Lithuania (in progress) Giedrius Trakimas

Chapter 67.

Denmark Kåre Fog, Lars Christian Adrados, Andreas Andersen, Lars Briggs, Per Klit Christensen, Niels Damm, Finn Hansen, Martin Hesselsøe, and Uffe Mikkelsen

Contributors to Part 6 (Australia, New Zealand, and Pacific Islands) CO-EDITORS (ALSO AUTHORS) HEATWOLE, Harold, Department of Zoology, The University of New England, Armidale, New South Wales 2351, Australia, and Department of Biology, North Carolina State University, Raleigh, NC 27695-7617, USA. [email protected] ROWLEY, Jodi J. L., Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, New South Wales 2010, Australia, and Centre for Ecosystem Science, Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, Australia. Jodi. [email protected]

AUTHORS ALFORD, Ross A., College of Marine and Environmental Science, Centre for Tropical Biodiversity and Climate Change, James Cook University, Townsville, Queensland 4811, Australia. [email protected] BELL, Ben D., Centre for Biodiversity & Restoration Ecology, School of Biological Sciences, Victoria University of Wellington, PO Box 600, Wellington 6140, New Zealand. [email protected] BISHOP Phillip J., Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand. phil. [email protected] BRADFIELD, Kay, Perth Zoo, PO Box 489, South Perth, Western Australia 6951, Australia. kay.bradfield@ perthzoo.wa.gov.au BYRNE, Philip, Biological Sciences, University of Wollongong, Northfields Avenue, Wollongong, New South Wales 2522, Australia. [email protected] CLEMANN, Nick, Arthur Rylah Institute for Environmental Research, Victorian Department of Environment,

Land, Water and Planning, Heidelberg, Victoria 3084, Australia. [email protected] COGGER, Harold G., Australian Museum Research Institute, Australian Museum, 1 William Street, Sydney, New South Wales 2010, Australia. h.cogger@ bigpond.com COOTE, David, New South Wales Office of Environment and Heritage, PO Box 2111, Dubbo, New South Wales 2830, Australia. [email protected] EVANS, Murray, ACT Government, Level 1 Building 3, 9 Sandford St, Mitchell, Australian Capital Territory 2911, Australia. [email protected] FISHER, Robert N., U.S. Geological Survey, Western Ecological Research Center, San Diego Field Station, 416 Spruance Road Suite 200, San Diego, CA 92101-0812, USA. [email protected] GILBERT, Deon, Melbourne Zoo, Elliott Avenue, Parkville, Victoria 3052, Australia. [email protected] GILLESPIE, Graeme R., Flora and Fauna Division, Department of Environment and Natural Resources, PO Box 496, Palmerston, Northern Territory 0831, Australia, and School of Biosciences, University of Melbourne, Parkville, Victoria 3010, Australia. [email protected] HOLLIS, Greg, Baw Baw Shire Council, 90 Smith St, Warragul, Victoria 3820, Australia. Greg.Hollis@ bawbawshire.vic.gov.au HUNTER, David, New South Wales Office of Environment and Heritage, PO Box 1040, Albury, New South Wales 2640, Australia. [email protected]. gov.au LEMCKERT, Frank, SMEC (Member of the Surbana Jurong Group), Level 5, 20 Berry Street, North Sydney, New South Wales 2060, Australia, and Australian

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Museum Research Institute, Australian Museum, 1 William Street, Sydney, New South Wales 2010, Australia. [email protected] MAHONY, Michael, School of Environmental and Life Sciences, The University of Newcastle, University Drive, Callaghan, New South Wales 2308, Australia. michael. [email protected] MARANTELLI, Gerry, Amphibian Research Centre, PO Box 1365, Pearcedale, Victoria 3912, Australia. gerry@ frogs.org.au McFADDEN, Michael, Herpetofauna Department, Taronga Conservation Society Australia, Bradleys Head Road, Mosman, New South Wales 2088, Australia, and School of Biological Sciences, University of Wollongong, New South Wales 2522, Australia. MMcFadden@zoo. nsw.gov.au. NEWELL, David, School of Environment, Science, and Engineering, Southern Cross University, PO Box 157, Lismore, New South Wales 2480, Australia. David. [email protected] OCOCK, Joanne, Water, Wetlands and Coastal Science, New South Wales Office of Environment and Heritage, Sydney, New South Wales, Australia. joanne.ocock@ environment.nsw.gov.au PHILIPS, Annie, Natural and Cultural Heritage Division, Department of Primary Industries, Parks, Water and

Environment, 134 Macquarie Street, Hobart, Tasmania 7000, Australia. [email protected] ROBERTS, J. Dale, Centre of Excellence in Natural Resource Management, University of Western Australia, PO Box 5771, Albany, Western Australia 6332, Australia. [email protected] SCHEELE, Ben, Fenner School of Environment and Society, Australian National University, Canberra, Australian Capital Territory 2601, Australia. [email protected]. au SHINE Richard, Heydon-Laurence Building A08, School of Life and Environmental Sciences, University of Sydney, New South Wales 2006, Australia. rick.shine@sydney. edu.au WASSENS, Skye, Institute of Land Water and Society, School of Environmental Sciences, Charles Sturt University, Albury, New South Wales 2640, Australia. [email protected] WEST, Matt, School of Ecosystem and Forest Science, University of Melbourne, Parkville, Victoria 3052, ­Australia. [email protected] ZUG, George, Department of Vertebrate Zoology, National Museum of Natural History, Smithsonian Institution, Washington, DC 20013-7012, USA. [email protected]

Preface The late 20th century and the early 21st century has been characterised by an unprecedented deterioration of the environment of the Earth and the throes of one of the major extinction events of all time. Unmitigated deforestation, desertification, erosion and salinisation of soil, pollution of water and air, and thinning of the UV-protective ozone layer constitute dire ecological threats for life on the planet. Fossil carbon is being returned to the atmosphere at an accelerated rate with a concomitant change in the Earth’s climate that is making serious inroads into ecological stability. The human population now exceeds the long-term carrying capacity of the Earth and subsists at its present level only because it is sustained by fossil resources of energy, soil, fresh water (laid down in aquifers in the Pleistocene) and even oxygen (produced by photosynthetic organisms over a few billion years). With continuing decrease in biodiversity, progressive destruction of essential habitats, degradation of major ecosystems, and contamination of life-support systems, it is likely that the carrying capacity of the Earth will decline below present levels – while at the same time the human population continues to rise exponentially. The outstripping of even the fossil resources, predicted to occur within the present century, presents a bleak outlook for our own species. We may well become victims ourselves of this most recent mass extinction. While it is undisputable that many aspects of environmental degradation and loss of biodiversity is directly attributable to unwise human activities, other aspects are deemed to result from natural forces beyond the control of mankind. It is important to be able to distinguish between the two, so that attention can be focused on mitigating those effects over which we do have control. It is important to ascertain the causes of particular declines and extinctions as soon as possible, so that steps can be taken to preserve what diversity we can. Amphibians, by virtue of their thin, moist, permeable skins, are poorly protected from harsh environments and are especially susceptible to chemical changes, desiccation, disease, and to alteration of their habitat. The biphasic lifestyle of most amphibians also exposes them to threats both on land and in water. Accordingly, it is not surprising that they manifest proportionately high

extinction rates and more severe declines than do most other organisms. They are especially important to study because they serve as an early warning system portending changes that may soon impinge upon more resistant species, including ourselves, and because they are an important part of many ecosystems: driving flows of nutrients and the transfer of energy. The series Amphibian Biology, as its name implies, treats the entire biology of amphibians, but because of the extreme importance of the decline and conservation of this taxon, four volumes are devoted to these topics. Volumes 8 and 10 contain a topical elucidation of the myriad factors responsible for amphibians’ demise and an assessment of measures that can be taken to conserve them. Volume 9 (Western Hemisphere) and 11 (Eastern Hemisphere) assess the worldwide status of the decline, extinction, and conservation of amphibians in several Parts (see Table of Contents) organised on a country-by-country basis; the present one (Volume 11, Part 6) deals with Australia, New Zealand, and the Pacific Islands. Although the various Parts of Volume 11 have been produced by different publishers, the chapters are numbered consecutively across the entire volume. CSIRO Publishing, however, required that the present Part be numbered separately as Chapters 1–14. Consequently, in the Table of Contents that sequence is followed (in parentheses) by the corresponding designation for Part 6 (Chapters 68–81) relating to consecutive numbering across the entire volume. The taxonomic nomenclature of amphibians is in a state of flux and is controversial. In this book, we retain use of the generic names Litoria and Cyclorana (following the taxonomy of AmphibiaWeb, http://amphibiaweb.org) pending a comprehensive resolution of phylogenetic relationships. There are various websites that estimate the current vulnerability of amphibian species to extinction and the present status of their decline. These websites change as status changes. Amphibian Biology does not compete with those, but rather is a ‘time capsule’ providing a perspective by present-day experts on the conservation of amphibians and the challenges faced by this taxon in each Australo-Pacific region. Because species are declining or going extinct while chapters are being written and put to

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Status of Conservation and Decline of Amphibians

press, in one sense the present treatise already will be out of date by the time it is published. In another sense, however, it is timeless because one can return to it for information on status at a specific time as a means of assessing subsequent extents and rates of change. Harold Heatwole  Raleigh, North Carolina 1 August 2017

Jodi J. L. Rowley Sydney, New South Wales 1 August 2017

1 Introduction Harold Heatwole and Jodi J. L. Rowley

HISTORY OF THE ENVIRONMENTS AND BIOTA Australia Australia’s tectonic plate separated from the Antarctic remnant of Gondwanaland sometime before 55 million years ago and drifted northwards to abut on the Asian plate toward the end of the Oligocene about 25 million years ago (Hall 2002, 2009). During the more than 30 million years for that traverse to occur, the continent was increasingly isolated from floral and faunal exchange with other continents, except possibility for exceedingly rare overwater dispersal of waifs. Amphibians, being highly sensitive to salt water, are poor subjects for such long-distance, overwater dispersal and consequently the present batrachofauna of Australia either originated in Gondwanaland in ancient times and adaptively radiated during the long voyage northward, or arrived much more recently after the Australian and Asian plates collided (Tyler and Lee 2006). Ranidae clearly belongs to the latter category because Papurana damaeli, the sole representative in Australia of this otherwise widespread family, only occurs on Cape York Peninsula and in eastern Arnhem Land. The Australian microhylids also may have originated from an Asian source (see Chapter 2), but the remaining taxa of Australian frogs probably descended from ‘hitchhikers’ aboard ‘Ark Australia’ during its northward journey from Gondwanaland. During this long passage, the Australian climate and vegetation varied dramatically, with an overall trend

toward increasing aridity and an adaptation of some frogs to dry conditions (see Chapter 2). This trend was not a straight-line progression, however, because there were reversals superimposed on overall drying (Fujioka and Chappell 2010). It is likely that there was a pulsation of expanding aridity outward from the centre, leaving coastal pockets of moist habitat and divergence of the isolated populations contained in them, followed by a retreat of aridity, with humid regions reconnecting and the ranges of the newly formed species expanding geographically (Chapter 1 in Heatwole and Taylor 1987). The repeated cycles of speciation of isolated populations followed by expansions of range, led to radiation into a wide variety of habitats and to a few species with unusual adaptations to aridity (see Chapter 2). The topography of Australia is one of generally low relief, with the Great Dividing Range skewed toward the eastern coast; the climatic pattern is of a monsoonal tropical north, a moist eastern and south-western temperate periphery, and an arid (desertified) core. These topographic and climatic features are reflected in the zonation of vegetation underlying the topical organisation of chapters in this book. New Zealand About 83 million years ago, a fragment of continental crust about the size of modern India rotated away from the Australian section of Gondwanaland to form a land mass known as Zealandia (Goldberg et al. 2008). Subsequently,

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Status of Conservation and Decline of Amphibians

the rift separating Zealandia from Australia widened to form the Tasman Sea and, over about 60 million years, Zealandia thinned and sank until only a much smaller remnant, the present New Zealand, remained above water. A boundary collision of the plate in the late Oligocene gave rise to topographic upheaval to form the Southern Alps. New Zealand’s biota consists of a mixture of ancient Gondwanan elements and more recent arrivals (Goldberg et al. 2008). In line with their physiological characteristics, frogs do not disperse over salt water easily and, not surprisingly, New Zealand’s frogs are of Gondwanan origin. In fact, they are among the most primitive of frogs, having diverged from more modern taxa in about the mid-Triassic (see Chapter 13). All are endemic to New Zealand and, in keeping with the mesic climate there, are denizens of forests. The oceanic islands of the Pacific Oceanic islands are those that arise de novo from the sea without any present or previous direct connection to a continent or isolated continental fragment (such as New Zealand). Chapter 14 and Neall and Trewick (2008) summarise the tectonic history of the Pacific Basin and the islands lying within it, and that will not be detailed here. The salient point is that most oceanic islands of the Pacific are devoid of amphibians, probably because of their great distances from a continental source of terrestrial fauna and the difficulty with which amphibians disperse across salty water. Only three island-groups near the periphery of the Pacific, and hence nearer sources of continental faunas, have native frogs – the Solomon Islands, Palau, and Fiji – although some others have species introduced by humans (see Chapter 14).

THE GLOBAL CONTEXT OF THE DEMISE OF AMPHIBIANS Throughout geologic history there have been periodic mass extinctions in which the biota of the Earth was reduced cataclysmically (McElwain and Punyasena 2007). The causes of these events have been varied: one perhaps being due to changing patterns of oceanic currents and climatic disruptions resulting from the separation of the supercontinent Pangaea into two, and eventually all seven, of the present continents. The most famous mass extinction, however, was the one marking the transition from the Mesozoic Era to the Cenozoic about 66 million years ago, attributed to the collision of a comet with the Earth, and highlighted by the precipitous disappearance of

dinosaurs as well as many other taxa (Alvarez et al. 1980). The eventual fate of all species, of course, is to disappear, either through dying out completely (extinction), or by loss of the ancestral form via its transition into new, and different, taxa (evolution, speciation). Previous mass extinctions were followed by a regenerative cycle as the surviving taxa adaptively radiated into ecological niches left vacant by the demise of victims of the extinction event. Recovery requires millions of years (McElwain and Punyasena 2007). Currently, almost one-third of all amphibian species are threatened with extinction, making them the most threatened group of terrestrial vertebrates (IUCN 2017). Thirty-three amphibian species are officially listed as recently extinct, but this likely is a severe underestimate. The causes of amphibian declines and extinctions are multiple (Heatwole 2013) and form a complex network that is nearly intractable to solution by virtue of the labyrinth of a large number of interactive links (Plate 1.1). Amphibian decline is global, but is generated by different combinations of factors in different regions, although some causes are common and widespread geographically. One of the biggest obstacles to halting the decline of amphibian species is a lack of knowledge. At the most basic level, we still do not know how many species of amphibians there are; in the past decade, an average of 157 new species of amphibians have been described annually (AmphibiaWeb 2017). This trend shows no sign of slowing. For the species of which we are aware, we often lack information necessary to carry out informed conservation. Indeed, 24% of all currently assessed amphibian species (84% total known amphibian species to date; AmphibiaWeb 2017) are so poorly understood that their conservation status cannot be determined (IUCN 2017). The mass extinction now in progress differs from previous ones by virtue of its largely anthropogenic origins – we are the root of most of the causes. This aspect, however, does have a positive side: there is an intelligent, sentient species involved in the event. If we can cause declines that lead to extinction, perhaps we also can devise ways to prevent, or at least ameliorate, them. Consequently, this book has two goals: (1) to contribute to an understanding of this complex phenomenon; and (2) to stimulate research into finding solutions to prevent the occurrence of the worst-case scenario. A lot of research toward these ends already has taken place and has been reviewed (see Preface); the material presented here is by way of application specifically to Australia, New Zealand, and the Pacific Islands.

1 – Introduction

With such a complex set of causes as illustrated in Plate 1.1, the tracing and quantifying of the links in the network of interactions is a formidable task. We must be vigilant to avoid facile oversimplifications. Too often, once a single correlation has been established, it is accepted as denoting a cause and effect relationship, with that conclusion becoming widely accepted and without delving into the possible intervention of other factors. The oversimplified version may then be enshrined as truth for all occasions in the lexicon of scientific mythology, and the complete suite of reasons bypassed by future investigators. Enigmas are important because they help identify such situations and allow greater focus on reconciling apparent contradictions. For example, Lane and Burgin (2008) reported that at lower elevations in the Greater Sydney region the diversity of amphibians was lower in more urbanised and polluted sites than in natural, less polluted ones, as one would expect, but that at higher elevations, the reverse occurred. In view of the complexity of possible interactions illustrated in Plate 1.1, paradoxes like this are important and should be followed up for verification and further scrutiny, rather than merely dismissed as aberrant. Resolution of such mysteries may lead to a far better understanding than could be achieved merely by unduly emphasising the more predicable outcome. A common misconception that also tends to disguise the dynamics of natural systems is an optimistic view of their regenerative capacity. It is true that biological systems often exhibit fluctuations around some mean level, and that departures from that level bring into play forces tending to return the system toward the mean, whether the departure is above the mean or below it. The mechanisms directing such returns toward a stable equilibrium collectively are known as negative feedback, and the entire process of oscillation around a set value is called homeostasis. Regulation of body temperature in mammals is an example of such a system. When the body begins to get too hot, certain automatic responses, such as panting, sweating, or seeking shade, occur that tend to cool the body. When the body begins to cool below the equilibrium level, other responses, such as shivering, come into play and raise the body back toward the ‘normal’ level. Such mechanisms are frequent in biological systems and operate at various levels, ranging from the physiology of an individual (as in the above example) to the dynamics of biotic communities and ecosystems. This generality has inspired unwarranted optimism that homeostasis will operate consistently and that, when disturbed, ‘nature’ will automatically restore

itself to its original condition, merely if left alone. That is not always the case and the more severe the disturbance, the more likely it is that some non-equilibrium state will prevail or that a new, less desirable, equilibrium will be reached (Rohde et al. 2013). In the worst-case scenario, an irretrievable situation, such as extinction, may alter the equilibrium. For example, amphibian population declines in Central America in the 1990s has resulted in large-scale ecosystem-level effects in stream habitats that persist today (Whiles et al. 2006, 2013). There are limits to homeostasis.

AMPHIBIANS IN AUSTRALIA, NEW ZEALAND, AND THE PACIFIC ISLANDS Australia has a relatively well-known frog fauna but much remains unknown, even with respect to the true number of species. There are currently 240 native species of frogs known from Australia (see Chapter 2 for a summary of the diversity, distributions, and conservation status), but in the past decade alone, 21 new species, representing 9% of Australia’s known frog fauna, have been discovered. Most of these species were hidden within known ‘species’ that were found to be complexes of multiple, morphologically similar species (e.g. Mahony et al. 2006; Anstis et al. 2016; McDonald et al. 2016), but others have been discovered as the result of surveys in remote or previously unsurveyed areas (e.g. Hoskin and Aland 2011). The discovery of previously undescribed species of frogs in Australia is ongoing, particularly in tropical northern regions. The frog fauna of the Pacific Islands is considerably less well known (see Chapter 14), with just over 30 known species and new species found on almost every expedition (e.g. the Solomons). New Zealand’s native frog fauna currently consists of four species belonging to a single relatively ancient lineage (see Chapter 13). Although geographically proximate, each region presents unique challenges and opportunities in amphibian research and conservation. Whereas population declines of frogs are well documented, and research and conservation have a long history in Australia and New Zealand (see Chapters 3–9, 11), present knowledge is insufficient even to determine to what extent population declines have occurred in most species (see Chapter 14). It is hoped that this book, by presenting and critically interpreting the body of available information on the current status of amphibians in Australia, New Zealand, and the Pacific, will form the basis for future research into an urgent ecological problem. Equally important, or perhaps more so, it also is hoped that persons involved in

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formulating policy or executing conservation actions will be able to do so with greater understanding and success as a result of access to the accumulated knowledge and understanding summarised in this modest volume.

REFERENCES

Alvarez LW, Alvarez W, Asaro F, Michel HV (1980) Extraterrestrial cause for the Cretaceous-Tertiary Extinction. Science 208, 1095–1108. doi:10.1126/science.208.4448.1095 AmphibiaWeb (2017) University of California, Berkeley, CA, USA, Anstis M, Price LC, Roberts JD, Catalano SR, Hines HB, Doughty P, et al. (2016) Revision of the water-holding frogs, Cyclorana platycephala (Anura: Hylidae), from arid Australia, including a description of a new species. Zootaxa 4126, 451–479. doi:10.11646/zootaxa.4126.4.1 Boone MD, Davidson C, Bridges-Britton C (2009) Evaluating the impact of pesticides in amphibian declines. In Amphibian Decline: Diseases, Parasites, Maladies and Pollution. (Eds H Heatwole and JW Wilkinson) pp. 3186–3207. Amphibian Biology Series Volume 8. Surrey Beatty & Sons, Sydney. Bridges CM, Semlitsch RD (2005) Xenobiotics. In Amphibian Declines, the Conservation Status of United States Species. (Ed. M Lannoo) pp. 89–92. University of California Press, Berkeley, CA, USA. Burrowes PA (2009) Climatic change and amphibian declines. In Amphibian Decline: Diseases, Parasites, Maladies and Pollution. (Eds H Heatwole and JW Wilkinson) pp. 3268– 3279. Amphibian Biology Series Volume 8. Surrey Beatty & Sons, Sydney. Fujioka T, Chappell J (2010) History of Australian Aridity: chronology in the evolution of arid landscapes. Geological Society, London, Special Publications 346, 121–139, https:// doi.org/10.1144/SP346.8 Goldberg J, Trewick SA, Paterson AM (2008) Evolution of New Zealand’s terrestrial fauna: a review of molecular evidence. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 3319–3334. doi:10.1098/ rstb.2008.0114 Hall R (2002) Cenozoic geological and plate tectonic evolution of SE Asia and the SW Pacific: computer-based reconstructions, model and animations. Journal of Asian Earth Sciences 20, 353–431. doi:10.1016/S1367-9120(01)00069-4 Hall R (2009) Southeast Asia’s changing palaeogeography. Blumea 54, 148–161. doi:10.3767/000651909X475941 Hayes TB (2005) Welcome to the revolution: integrative biology and assessing the impact of endocrine disruptors on environmental and public health. Integrative and Comparative Biology 45, 321–329. doi:10.1093/icb/45.2.321 Heatwole H (2013) Worldwide decline and extinction of amphibians. In The Balance of Nature and Human Impact. (Ed. K Rohde) pp. 259–278. Cambridge University Press, Cambridge, UK.

Heatwole H, Taylor J (1987) Ecology of Reptiles. Surrey Beatty & Sons, Sydney. Hoskin CJ, Aland K (2011) Two new frog species (Microhylidae: Cophixalus) from boulder habitats on Cape York Peninsula, north-east Australia. Zootaxa 3027, 39–51. IUCN (2017) The IUCN Red List of Threatened Species. Version 2017-1, . Lane A, Burgin S (2008) Comparison of frog assemblage structure between urban and non-urban habitats in the upper Blue Mountains (Australia). Freshwater Biology 53, 2484– 2493. doi:10.1111/j.1365-2427.2008.02068.x Mahony MJ, Donnellan SC, Richards SJ, McDonald KR (2006) Species boundaries among barred river frogs, Mixophyes (Anura: Myobatrachidae) in north-eastern Australia, with descriptions of two new species. Zootaxa 1228, 35–60. McCoy KA, Guillette LJ, Jr (2009) Endocrine disrupting chemicals. In Amphibian Decline: Diseases, Parasites, Maladies and Pollution. (Eds H Heatwole and JW Wilkinson) pp. 3208–3238. Amphibian Biology Series Volume 8. Surrey Beatty & Sons, Sydney. McDonald KR, Rowley JJL, Richards SJ, Frankham GJ (2016) A new species of treefrog (Litoria) from Cape York Peninsula, Australia. Zootaxa 4171, 153–169. doi:10.11646/zootaxa. 4171.1.6 McElwain JC, Punyasena SW (2007) Mass extinction events and the plant fossil record. Trends in Ecology & Evolution 22, 548–557. Neall VE, Trewick SA (2008) The age and origin of the Pacific Islands: a geological review. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 3293–3308. doi:10.1098/rstb.2008.0119 Rohde K, Ford H, Andrews NR, Heatwole H (2013) How to conserve biodiversity in a nonequilibrium world. In The Balance of Nature and Human Impact. (Ed. K Rohde) pp. 393–406. Cambridge University Press, Cambridge, UK. Rohr J, Raffel T, Sessions SK (2009) Digenetic trematodes and their relationship to amphibian declines and deformities. In Amphibian Decline: Diseases, Parasites, Maladies and Pollution. (Eds H Heatwole and JW Wilkinson) pp. 3067–3088. Amphibian Biology Series Volume 8. Surrey Beatty & Sons, Sydney. Tyler MJ, Lee MSY (2006) The origins of Australian frogs. In Evolution and Zoogeography of Australian Vertebrates. (Eds JR Merrick, M Archer, G Hickey, and M Lee) pp. 237–240. Australian Scientific Publishing, Sydney. Whiles MR, Lips KR, Pringle CM, Kilham SS, Bixby RJ, Brenes R, et al. (2006) The effects of amphibian population declines on the structure and function of Neotropical stream ecosystems. Frontiers in Ecology and the Environment 4, 27–34. doi:10.1890/1540-9295(2006)004[0027:TEO APD]2.0.CO;2 Whiles MR, Hall RO, Dodds WK, Verburg P, Huryn AD, Pringle CM, et al. (2013) Disease-driven amphibian declines alter ecosystem processes in a tropical stream. Ecosystems 16, 146–157. doi:10.1007/s10021-012-9602-7

2

A brief demographic overview of Australia’s native amphibians Harold G. Cogger

INTRODUCTION Native amphibians in Australia consist solely of members of the order Anura (frogs and toads). At the time of writing, some 241 species of frogs are recognised as occurring in the wild in Australia, all but one of which, the invasive cane toad Rhinella marina, are native to Australia. Of the 240 native species, 225 (93.5%) are Australian endemics, with only 16 species (6.5%) shared with New Guinea to the immediate north. However, new species continue to be described at a modest rate as a result of more intensive surveys of remote regions and of the increasing application of molecular genetic methods to the systematics of Australian frogs. Four Australian hylid frogs – the green and golden bell frog Litoria aurea, southern bell frog Litoria raniformis, brown tree frog Litoria ewingii, and green tree frog Litoria caerulea – became established in New Zealand long ago, although the current status of the lastcited species is uncertain. Litoria aurea, however, is also firmly established on several western Pacific Islands, including New Caledonia, the island of Efate (and probably others) in Vanuatu, and Wallis Island. Australia’s 240 native species of frogs represent only 3.58% of the world’s frog fauna of 6726 species (Frost 2017), and include representatives of five families: Limnodynastidae (40/43 species), Myobatrachidae (89/89 species), Hylidae (or Pelodryadidae) (87/210 species), Microhylidae (24/606 species), and Ranidae (1/380 species) (family totals from Frost 2017). Given Australia’s

total land area of 7.7 million km2 (5.7% of the global land area, excluding Antarctica, of ~135 million km2), and with about half of the continent and Tasmania located in temperate regions, and about two-thirds dry to arid, this relatively low proportion of the world’s frog diversity is not entirely unexpected. Indeed, these continental climatic features are clearly reflected in the relative richness and distribution of frogs within Australia, as the following sections demonstrate. Given that Australia has experienced numerous periods of greater continental precipitation during the Pleistocene and Holocene with associated expansion of mesic vegetation, one might expect that the numbers and diversity of frogs may have been much greater at that time, yet there is little fossil evidence or current species-level discontinuities of range to support such an assumption. Nevertheless, the supraspecific taxonomic diversity in the present frog fauna (25 genera compared with 21 genera in North America and 106 genera in Brazil) may well represent a reduction in diversity following the desertification of nearly two-thirds of the Australian continent in the past 200 000 years. All Australian treefrogs were, until recently, considered members of the family Hylidae. However, in a recent phylogenetic analysis of the hylid frogs by Duellman et al. (2016), Australian treefrogs were assigned to the resurrected family Pelodryadidae within an unranked suprafamilial taxon (Arboranae). These authors also

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resurrected the genus Ranoidea, into which they absorbed species previously assigned to the genus Cyclorana and a number of species previously in the genus Litoria. Although this has resulted in many changed combinations, it has not impacted on the status of individual species, on which the following analyses are based. Consequently, adoption of the Duellman et al. (2016) phylogeny would have little or no impact on this present overview, based as it is on species-level distributions. The Duellman et al. (2016) phylogeny has been adopted by Frost (2017), and is currently being roadtested by Australian phylogeneticists. However, until it has been more widely adopted I have retained here the conventional classification of Australian hylid frogs represented by such recent works as Tyler and Doughty (2009), Tyler and Knight (2011), Vanderduys (2012), Anstis (2013), and Cogger (2014).

DATA AND METHODOLOGY This chapter deals with much of the ground previously covered by Slatyer et al. (2007), including analyses of species richness and endemicity. That work used some 97 338 post-1950 observational and voucher records extracted from the aggregated frog databases at Australian museums and diverse wildlife agencies, assigning each record to a 10 km × 10 km grid of Australia and Tasmania. Subsequent analyses were based on a 30’ grid. Where our analyses overlap, there is strong congruence in our results, despite our different methodologies. However, our analyses differ in two major respects: the use of entirely different datasets (see below) and recognition of the separate family Limnodynastidae (members of the latter were included in the family Myobatrachidae by Slatyer et al. 2007). The distribution of the frogs of Australia and its adjacent regions has also been reviewed by Tyler (1999). The following overview has been facilitated by the preparation of distribution maps of Australian frogs for a revised (7th) edition of Reptiles and Amphibians of Australia (Cogger 2014). The maps in that work drew on a variety of published sources (listed in that book’s Selected References), as well as on available databases (e.g. the Atlas of Living Australia (http://www.ala.org.au/) and unpublished records from colleagues, to produce smoothed minimum convex polygons showing the outer geographic limits of the area within which each species has been recorded. The initial maps were constructed on a 30’ × 30’ grid of Australia prepared for the author by Dr

Paul Williams to accompany access to his biogeographic analytical software Worldmap, version 4.20.24 (Williams 2000). For species shared by Australia and New Guinea, their New Guinean distributions were sourced from Menzies (2006). The reliability (i.e. accuracy) of analyses based on such polygon-based maps (of the kind that accompany most regional guides/handbooks used for faunal identification), compared with those maps based solely on spot observation-based or voucher-based records using aggregated specimens or observation records in museum collections or other conservation databases, has been challenged (e.g. Doughty 2016). However, both approaches have inherent sources of error. In the case of spot or point record maps, they can suffer four major disadvantages over maps based on current polygons: (1) the accuracy of the taxonomic identity of individual records varies greatly between and within institutional databases, depending upon the identifier; (2) there is often a significant (in some cases many years) lag-time in bringing institutional identifications up to date with subsequent taxonomic revisions, especially in groups subject to substantial and/ or ongoing systematic research; (3) geographic areas that have been poorly or not surveyed, or for which few or no records exist, will contribute little to biogeographic analysis, or may seriously bias the conclusions; and (4) although an estimate may be given of the reliability of recorded location or geographic coordinates in some institutional databases, in others it is not. Consequently, often it is difficult to know whether outlying geographic records (in extreme cases, mid-ocean records of a terrestrial species) are true or simply miscalculations. The geographic range of a species is usually defined as the geographical limits of its distribution (Lincoln et al. 1986). This coincides with the IUCN concept of ‘extent of occurrence’. Both concepts accept that a species may only occupy a small proportion (area of occupancy) of its extent of occurrence. With modest survey effort, and the increasing access to large databases from museums and other sources, the geographic range of a species can be drawn with some reliability. Conversely, the area of occupancy of most species (except for those that are highly localised and/or intensely studied) is rarely known, especially at a large continental scale such as that of Australia. For most of the 240 Australian species of frogs, the critical conservation management parameter (area of occupancy) is unknown or, at best, poorly known. Whichever the source of data, the accuracy of distributions will be affected by the minimum cell size used in

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the analyses. In this review, the smallest size of range (extent of occurrence) attributable to any species is one cell measuring 30 minutes of latitude × 30 minutes of longitude, assigned an average area of ~2500 km 2 (see p. 10). This (the extent of occurrence) may often be many times greater than the area actually occupied (area of occupancy) by the target species. Further, polygon boundaries in field guides are invariably estimates based not only on observation/voucher records, but also on anecdotal and subjective assessments predicated on known distributions of suitable habitat for any particular species, and on unpublished records. Consequently, this approach introduces its own errors – errors that are hard to quantify. However, in choosing to use polygons rather than point records for its own analyses of species’ spatial data, the International Union for the Conservation of Nature (IUCN) points out that such polygons are ‘...essentially meant to communicate that the species probably occurs within this polygon, but it does not mean that it is distributed equally within that polygon or occurs everywhere within that polygon.’ (http://www.iucnredlist.org/technical-documents/red-list-training/iucnspatialresources). Caley and Schluter (1997) also selected field-guide polygons rather than dot-maps for their analyses of the relationship between local and regional diversity, on the grounds that although ‘... dot maps may convey accurate information regarding where a species has been either collected or observed, we felt unjustified in assuming the extent of the distribution of species from such maps without having any first-hand experience of these species.’ Consequently, the following analyses indicate only broad-scale trends and patterns at family-group or higher taxonomic level. Only if many polygons are significantly inaccurate will these broad patterns, at continental scale, be seriously distorted. Two introductory maps to assist the reader in interpreting the remaining maps show some key geographic locations on the grid (Plate 2.1) and the distribution of the 89 IBRA (Interim Biogeographic Regionalisation for Australia, Version 7) bioregions adopted by the Australian Government (Plate 2.2).

SPECIES RICHNESS AND RANGE CENTRES Overall species richness Overall species richness is simply a measure of the number of species found in any given 30’ × 30’ cell, and so reflects the relative abundance of species of frogs across

the Australian landscape. It contains no information about the relative abundance of frogs in any given cell. The maximum species richness of native frogs (49 species) occurs in the cell containing the Daintree River, Queensland, with high richness levels in the adjacent cells (33–41 species). The next region of high species richness is in south-eastern Queensland, where clusters of adjacent cells have values of 41–44 species. Clearly, the presence of a large number of species occurring in a particular cell – a widely used measure of a biodiversity ‘hotspot’ – may be of great significance to conservation planners and managers, and to scientists studying biodiversity, but species richness fails to assign differential significance to rare species, to local or regional endemics, to species with highly restricted ranges, to those that are narrow ecological specialists, or to phylogenetic relicts. Nor does it necessarily reflect susceptibility to a range of threatening processes. As will be indicated in the following discussion, maps of species richness alone, without respect to the character of a species (taxonomic, phylogenetic, and/or rarity) will not provide the basis for conservation decisions other than ones based solely on the number of species present. Note that an area roughly coinciding with the extent of the Nullarbor Plain adjoining the Great Australian Bight appears to be frog free. Although the edges of this area may be revised following additional surveys, this frogfree region appears to be both real and unique. No other significant part of the Australian continent entirely lacks frogs. Centres (all species) Range centres (all species) are the geometric centres of the polygons (extents of occurrence) of individual species of frog. Combined with range size and knowledge of habitat preferences, they provide an approximation of the range of environmental conditions tolerated by a particular species, reflecting the suite of ‘habitats’ under which it can survive and disperse. For example, a species with a presence across most of its range is likely to have its ecological preferences well represented by conditions at its range centre, whereas the range centres of species that occur only in small refugia scattered over a wide area of otherwise unsuitable habitat may hold little information on the species’ habitat preferences. The distribution of range centres (Plates 2.4, 2.6, 2.8, and 2.10) is also informative in being the end product of current and Quaternary (and probably earlier) environmental constraints (e.g. habitat, climate, seasonal

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extremes) that in turn reflect the recent history of occupation of a given species’ range. Species with range centres nearest the perimeter of the continent generally have smaller geographic ranges and are tolerant of a narrower range of environmental variables than those species with range centres farther from the coast, the latter implying a wider physiological tolerance to climatic and ecological extremes. The extent to which the current distribution of range centres reflects the temporal history of more ancient Pleistocene, or even earlier, invasions and radiations will only be determined when combined with timescaled phylogenies. Changes to any section(s) along the perimeter of a species’ extent of occurrence would immediately shift its range centre. Consequently, range centres might be expected to float around in response to both short-term and long-term changes in the boundaries of a species’ range (following local, regional, and continental climatic and other environmental fluctuations). Conversely, it may be that a range centre is a relatively stable mediumto-long-term centre of a polygon whose perimeter marks the geographic limits to a species’ ecological viability, despite areas within the polygon suffering periodic extirpation and reinvasion by the species during cycles of environmental change. However, any intrinsic biogeographic value of a range centre may depend upon the shape of a species’ range, because the range centre is merely the geometric centre of the points along the range’s boundaries. For example, in a range that is narrow and crescent-shaped, the range centre may even be outside its geographic range, even to the point of being located in an adjacent area of sea. However, this occurred in only four species in the current analysis – the remote froglet Crinia remota, javelin frog Litoria microbelos, and marbled frog Limnodynastes convexiusculus (each of which had its range centre in the lower Gulf of Carpentaria), and the southern toadlet Pseudophryne semimarmorata (with a range centre in Bass Strait). Such odd shapes can be imposed by topographic features, or by the distribution of preferred habitats, but all other species in this study had range centres within the boundaries of their areas of occurrence. While individual range centres contain little useful information, collectively they can be used to identify broad ecological trends – larger ranges tend to reflect higher ecological plasticity – and home ranges for frogs tend to cluster around the outer edges of the continent, reflecting the patterns of species richness in Plate 2.3. As

indicated above, and with the exception of species shared with New Guinea, the closer a range-centre is to the coast, the smaller its range is likely to be. It is tempting to attribute contemporary species’ distributions only to recent events, i.e. in the Holocene or late Pleistocene, or even to the short period (~12 000–15 000 years) since the last glacial period. Certainly, this brief period has seen extensive desertification of continental Australia that would surely have had dramatic impacts on the distributions of frogs, but phylogenetic studies of the Australian frog fauna have demonstrated that even closely related and geographically adjacent species or lineages may have diverged as recently as 1 million years ago, or as long as 10 million years ago (Donnellan et al. 1999; Hoskin and Aland 2011). The range centres (some of which are shared) of the 240 species of Australian native frogs are shown in Plate 2.4. Given the frequency and extended presence of land connections to New Guinea and some eastern Indonesian islands – the last as recently as ~15 000 years ago – one might expect numerous interchanges to have taken place between these two frog faunas during each period of connectivity. However, although some 16 native species of frogs are shared by these two land-masses, only two or three of these have range-centres located in New Guinea. This suggests that, although the precursors of today’s Australian microhylids probably invaded Australia via an early Torres Strait land connection, the more recent Holocene and late Pleistocene land connections resulted in few exchanges of currently present taxa of frogs, and then mostly of species from Australia’s seasonally wet savannahs to similar habitats in southern New Guinea. The arrival of the microhylid frog, the Northern Territory frog Austrochaperina adelphe, may have coincided with the earlier arrival of a ranid, the Australian wood frog Papurana daemeli, sometime during the presence of one of the broad, late Pleistocene land bridges between Australia and New Guinea. The geographic pattern of variation in species richness for all 240 Australian native species of frogs (Plate 2.3) anticipates that in this group of mostly water-dependent animals, species richness is highest along the mesic eastern coast and ranges (with maximum diversity in the more humid tropics and subtropics), and in northern Australia in the moist refugia provided especially in highly dissected ranges and monsoonal floodplains. Similarly, the map of range centres for all 240 Australian native frogs (Plate 2.4) shows that most of the range

2 – A brief demographic overview of Australia’s native amphibians

centres of Australian frogs are clustered along the northern and eastern seaboards, with a small group of regional endemics in far south-western Western Australia, and maximum clustering in the Wet Tropics and Cape York Peninsula. Only 16 of 240 Australian species are shared with Papua New Guinea (based on current taxonomies), despite extensive and extended land connections at various times during the late Pleistocene and Holocene (Voris 2000; various contributors to Walker 1972). Although the suggested times of these exchanges are debatable, they would indicate that the most recent of these connections, across the Torres Strait ~15 000 years ago, did not provide suitable conditions for other than a few ecologically labile species of frogs, none of which have their current range centres in New Guinea, to be exchanged between these two land masses (with the possible exception, if more data on their distribution in New Guinea were available, of the slender frog Austrochaperina gracilipes, white-lipped tree frog Litoria infrafrenata, marbled frog Limnodynastes convexiusculus, Australian wood frog Papurana damaeli, fringed tree frog Litoria eucnemis, bridled frog Litoria nigrofrenata, and the current two members of the dwarf rocket frog (Litoria dorsalis complex). However, it may be that some species exchanged between Australia and New Guinea at that time, or during previous extensive land bridges, may have become extinct on one side or the other. As indicated above, there are risks involved, from both biogeographic and conservation perspectives, in using patterns of overall species richness to postulate geographic origins or conservation priorities for the Australian frog fauna. In answering this question, however, it is important to know the extent to which areas of high species richness in one group of frogs coincide with, or reflect, those in other groups. Plates 2.5, 2.7, 2.9, and 2.11 illustrate the patterns of species richness at the familial level, in which species richness patterns are shown in each of the frog families present in Australia (except for the Ranidae, with its single Australian species). Family Myobatrachidae Diversity in the family Myobatrachidae (Plate 2.5), as expressed by species richness, is highest in eastern Australia, with greatest diversity on the coast and ranges of north-eastern New South Wales and south-eastern Queensland. Other areas of intermediate richness are in the Wet Tropics region, the tropical seasonally wet savannahs and stony ranges of northern Northern Territory

and the east Kimberley (Western Australia), and of the far south-west of Western Australia. The interior aridzone intrusion of this family in Western Australia results primarily from representatives of just two genera: Neobtrachus and Uperoleia. This pattern is consistent with the distribution of range centres in this family (Plate 2.6), with the great majority located in near-coastal areas, indicating that small geographic ranges predominate. Note also in Plate 2.5 that much of the arid interior appears to be lacking any representatives of this family. This may be in part the result of inadequate surveys that might otherwise extend the ranges of surrounding taxa well into this empty zone, or it may be real. It certainly points to the need for greater survey effort. Note that, as in the family Limnodynastidae below, richness-based range centres for all frog species (Plate 2.3) would seriously obscure the patterns in members of these two families. Family Limnodynastidae The pattern of species richness in this family (Plate 2.7) also shows a predominantly southern distribution, with maximum richness in temperate eastern Australia. The greatest number of species occurs in and near the ranges on the New South Wales/Queensland border, with the cell containing the greatest number of species found a little west of Lismore, New South Wales (10 of 40 species). The other major centre of limnodynastid species richness is in south-western Western Australia, with a maximum of 8 species/cell. Note that, although the previous family (Myobatrachidae) had the smallest mean range size among the three widespread families of Australian frogs (66.25 cells), the Limnodynastidae had the largest (243.52 cells). Thus, in the family Limnodynastidae, as in the Myobatrachidae, the distribution of range centres (Plate 2.8) reflects the distributional pattern of species richness, with the main clusters of range centres in south-eastern Australia and south-western Australia. Family Hylidae Plates 2.9 and 2.10 indicate that, as might be expected for primarily mesic-adapted treefrogs, a large proportion of continental Australia is unoccupied by members of this family, with only one or two species adapted to life in the arid continental centre or to the drier and colder southern regions. One of these species, the centralian tree frog

9

10

Status of Conservation and Decline of Amphibians

Litoria gilleni, is confined to relict mesic microhabitats within the mountain ranges of central Australia. Clearly, this family has its greatest diversity in the north and east. Similarly, the great majority of range centres in this family are clustered near the coastal regions (Plate 2.10), indicating a preponderance of smaller ranges around the more mesic perimeter of the northern half of Australia. The area of maximum concentration of range centres is in the Wet Tropics region of north-eastern Queensland, where the maximum number of hylid species/cell is 23 (out of 88), including three range centres. Other areas of especially high species richness of hylids are in the east and west Kimberley regions of north-western Australia (20 species/cell, including one range centre) and the mideastern coast of Australia (19 species/cell, including two range centres). Note that there is a large area of southern Australia in which hylid frogs apparently are absent. This appears to be a real absence, although its boundaries are likely to shift significantly following further surveys in this region. Again, the distribution of hylid range centres (Plate 2.10) reflects the family’s pattern of species richness, except that the clustering of range centres along the eastern seaboard implies that the sizes of ranges are small and/or elongate (i.e. many are restricted to the narrow coastal strip and adjacent ranges). Family Microhylidae The family Microhylidae has an extremely limited distribution in Australia, being confined to the wet, tropical parts of far-north Queensland (with a single species recorded from the northern parts of the Northern Territory) and widely regarded as a relatively recent Miocene arrival from New Guinea. It has the smallest mean range size (5.79 cells) and comprises two highly localised and speciose genera with maximum species richness (24 species) in north-eastern Queensland (Plate 2.11). Eleven (45%) of these 24 species have their range-centres located within a single cell. Although each of the above families, other than the Microhylidae, are considered ancient Gondwanan elements (Tyler and Lee 2006) that share common ‘hotspots’ of richness in mid-eastern Australia and in the far southwest of Western Australia, other concentrations of high species richness (e.g. the Wet Tropics region of northeastern Australia) that dominate a map of all frogs (Plate 2.3) are derived primarily from two families: the Hylidae and Microhylidae. Major species-rich sites for the family Limnodynastidae (Plate 2.7) are located in north-eastern

New South Wales and south-western Western Australia, while those for the family Myobatrachidae (Plate 2.9) are cells enclosing Brisbane and Maleny in south-eastern Queensland (each with 16 species). Two other myobatrachid centres with high-scoring cells are in south-western Western Australia (nine species) and in the North Queensland Wet Tropics, centred on Mt Molloy (10 species). The point to be made is that, although maps of overall species richness (Plate 2.3) may be highly informative about the limiting effects of current environmental factors on the distribution of frogs in Australia, they contain very little biogeographic information compared with that provided by the species-richness patterns in the component groups (e.g. families and genera). Nevertheless, species richness can have great utility in identifying areas of special biological interest or of conservation value based on endemism, threatened status (vulnerability), ecological/habitat preferences, or rarity (as expressed through range), and these are discussed below. Range centres in the three most speciose families (Plates 2.6, 2.8, and 2.10) also demonstrate the importance of looking to family rather than aggregated maps to interpret the patterns of frogs’ distributions in Australia. Hylid frogs tend to have range centres concentrated around the northern and eastern perimeters of the continent, limnodynastid range centres are mostly confined to the southern half of the continent, while myobatrachid frogs have range centres more widely distributed across the continent. Differences in these maps are visually striking and may well reflect fundamental family-level differences in the biological and ecological responses of their component species to Australia’s current and historic environmental and climatic fluctuations, at least from the Pleistocene onwards, and more especially to conditions during, and since, our last glacial period, ~12 000–15 000 years ago.

VARIATION IN SIZE OF RANGE On the projection of maps used in this exercise (Plate 2.1), as previously indicated, the 30’ × 30’ cells are equal, but on the ground they are significantly larger in area at lower latitudes than those at higher latitudes For example a cell of this size containing Hobart, Tasmania (latitude 42.88°S) has an area of ~2200 km2 , one containing Brisbane, Qld (latitude 27.47°S) has an area of ~2700  km2 , while one containing Cairns, Queensland (latitude 16.92°S) covers an area of ~3000 km2 . Thus, assigning an

2 – A brief demographic overview of Australia’s native amphibians

average value to all cells of 2500 km2 infers that a species distributed primarily in the northern half of Australia will have its extent of occurrence underestimated, while that of a species found mostly in southern Australia will have its extent of occurrence overestimated. It also was pointed out earlier that a concentration of peripheral range centres reflects the concentration of smaller ranges around the more mesic coastal regions of the continent. This is supported by an analysis of the median range size of the species found in each cell (Plate 2.12). There are also notable differences in mean range among the families of Australian frogs. In Plate 2.13, the variation in range sizes (as expressed by number of 30’ × 30’ cells contained within the polygon of a species’ range) is shown for all frogs combined and for each of four families: Myobatrachidae, Limnodynastidae, Hylidae, and Microhylidae. Plate 2.13 further indicates that there are also significant differences in mean range size among the families of Australian frogs. Mean range size (5.79 cells ± 9.19) is smallest in the family Microhylidae, followed by species in the Myobatrachidae (66.24 cells +/– 122.99). Both are significantly smaller than are those for the Limnodynastidae (243.52 cells +/– 344.49) and the Hylidae (176.25 cells +/– 306.7). Applying the proposed average cell size of 2500 km2 , mean range sizes (extent of occurrence) for each of the speciose families of Australian frogs are: Myobatrachidae: 165 600 km2; Limnodynastidae 608 880 km 2; Hylidae 440 625 km2; and Microhylidae 14 475 km2 .

THREATENED SPECIES To date, legislative and protective actions to conserve Australian frogs has been based almost entirely on the threatened-species concept, whereby individual species are assessed for their vulnerability to threatening processes, and estimates made of the extent and rates of any declines and the costs of actions needed to reverse those declines and to reduce vulnerability. This has led to the production of an Action Plan for Australian Frogs (Tyler 1997) to inform legislators and wildlife managers of priority actions (Recovery Plans) needed to conserve particular species and the approximate costs of implementing such plans. World Wildlife Fund (Australia), with the financial assistance of Rio Tinto Ltd, and a frog-specialist panel chaired by Dr Stan Orchard, produced a ranked assessment of threatened species of frogs to act as an update of the 1997 Frog Action Plan, but it has lain barely used since the funding by Rio Tinto ended in 2005.

At the level of the Australian Government, the Action Plan has resulted in particular species being listed under the Environment Protection and Biodiversity Conservation Act 1999 (EPBC Act), whose purpose is to regulate those actions, by the Federal Government and its agencies, and those by State Governments and private individuals and corporations, that are likely to impact deleteriously on species listed under the Act. This act also regulates the export of any listed species. At the State level, lists of protected species have been developed that regulate the taking of such species, the conducting of research and conservation programs involving these species, and the approval of any action that will impact significantly on a listed species. However, listings are determined by State boundaries and the status of a State’s population of any particular species will usually ignore the status of that species in other States. Both Federal and State Governments have been strongly influenced in their listings of protected species by the IUCN Red List of Threatened Species (IUCN Red List). At the time of writing, some 59 species of Australian frogs (~24%) are listed as either Extinct (3), Critically Endangered (15), Endangered (18), Vulnerable (14) or Near Threatened (9) on the IUCN Red List (IUCN 2017). Within Australia, some 28 species of frogs (~12%) are listed under the Australian Government’s EPBC Act (as at 26 January 2017 ), of which only one species and one subspecies are in addition to those on the IUCN Red List: Litoria littlejohni (Hylidae) and Litoria verreauxii alpina (Hylidae). Further, Skerratt et al. (2016) listed 22 of the species of frogs listed on the IUCN Red List (Table 2.1) as under significant threat from the amphibian disease chytridiomycosis, and added a further six species: Crinia nimbus (Myobatrachidae); Pseudophryne semimarmorata (Myobatrachidae); Uperoleia martini (Myobatrachidae); Litoria serrata (Hylidae); Litoria kroombitensis (Hylidae); and Litoria longirostris (Hylidae). The distribution and species richness of the 59 species of frogs listed as Extinct, Critically Endangered, Endangered, Vulnerable, or Near Threatened on the IUCN Red List are shown in Plate 2.14. These collectively occur over a relatively small proportion of the Australian continent, with the highest number of threatened species (13) found in three adjoining cells encompassing the ranges between the Hastings and Bellinger Rivers, New South Wales. Skerratt et al. (2016) pointed out that, to date, Australia has lost up to six species of frogs to apparent (and widely

11

12

Status of Conservation and Decline of Amphibians

Table 2.1.  IUCN Red-Listed species of Australian native frogs in the threatened categories Extinct, Critically Endangered, Endangered, Vulnerable, and Near Threatened. Source: The IUCN Red List of Threatened Species. Version 2017-1. (downloaded on 21 June 2017).

Family Myobatrachidae

Family Hylidae

Crinia tinnula (Vulnerable)

Litoria andirrmalin (Vulnerable)

Geocrinia alba (Critically Endangered)

Litoria aurea (Vulnerable)

Geocrinia lutea (Near Threatened)

Litoria booroolongensis (Critically Endangered)

Geocrinia vitellina (Vulnerable)

Litoria brevipalmata (Endangered)

Mixophyes balbus (Vulnerable)

Litoria castanea (Critically Endangered)

Mixophyes fleayi (Endangered)

Litoria cooloolensis (Endangered)

Mixophyes iteratus (Endangered)

Litoria daviesae (Vulnerable)

Pseudophryne australis (Vulnerable)

Litoria dayi (Endangered)

Pseudophryne bibronii (Near Threatened)

Litoria freycineti (Vulnerable)

Pseudophryne corroboree (Critically Endangered)

Litoria jungguy (Near Threatened)

Pseudophyne covacevichi (Endangered)

Litoria lorica (Critically Endangered)

Pseudophryne pengilleyi (Endangered)

Litoria myola (Critically Endangered)

Rheobatrachus silus (Extinct)

Litoria nannotis (Endangered)

Rheobatrachus vitellinus (Extinct)

Litoria nyakalensis (Critically Endangered)

Spicospina flammocaerulea (Vulnerable)

Litoria olongburensis (Vulnerable)

Taudactylus acutirostris (Critically Endangered)

Litoria pearsoniana (Near Threatened)

Taudactylus diurnus (Extinct)

Litoria piperata (Critically Endangered)

Taudactylus eungellensis (Critically Endangered)

Litoria raniformis (Endangered)

Taudactylus liemi (Near Threatened)

Litoria rheocola (Endangered)

Taudactylus pleione (Critically Endangered)

Litoria spenceri (Critically Endangered)

Taudactylus rheophilus (Critically Endangered)

Litoria subglandulosa (Vulnerable)

Family Limnodynastidae

Family Microhylidae

Adelotus brevis (Near Threatened)

Cophixalus aenigma (Vulnerable)

Heleioporus australiacus (Vulnerable)

Cophixalus bombiens (Near Threatened)

Philoria frosti (Critically Endangered)

Cophixalus concinnus (Critically Endangered)

Philoria kundagungan (Endangered)

Cophixalus crepitans (Near Threatened)

Philoria loveridgei (Endangered)

Cophixalus exiguous (Near Threatened)

Philoria pughi (Endangered)

Cophixalus mcdonaldi (Endangered)

Philoria richmondensis (Endangered)

Cophixalus monticola (Endangered)

Philoria sphagnicolus (Endangered)

Cophixalus neglectus (Endangered) Cophixalus saxatilis (Vulnerable)

accepted) extinction resulting from chytridiomycosis, while a further seven species are at imminent risk of extinction from the same cause. Other species (e.g. the Corroboree Frog Pseudophryne corroboree) have declined to such an extent that their continued presence in the wild is dependent (all or in part) on intensive (and costly) captive-breeding programs. Chytridiomycosis is clearly

the most immediate and pressing threatening process facing Australian frogs.

SUMMARY It is evident from the maps presented in this chapter that the analyses of distributional patterns within a given

2 – A brief demographic overview of Australia’s native amphibians

region become increasingly less informative at higher taxonomic rank: for example, compare Plate 2.3 with those of the individual families (Plates 2.5, 2.7, 2.9, and 2.11). Although many of the patterns, and the conclusions drawn from those patterns, are broadly predictable from knowledge of a taxon’s diverse ecological and physiological traits, any analysis of entire faunas at the level of order or higher, or at very large geographic scales (e.g. continental), will contain so much noise that patterns that might explain current and past changes in the distributions of taxa, and of the timing and patterns of vicariant or dispersal events, are lost in this noise. Consequently, examination of patterns of contemporary distribution and richness at the familial or generic levels are more reliable sources of biogeographic history. Although currently disputed phylogenies leave the histories of many taxa in limbo, only the development of rigorous phylogenies will test the predictive value of broad biogeographic analysis based on contemporary distributional patterns. It is also notable that the results of the present study, based on rounded-polygon approximations of species’ geographic ranges (extents of occurrence) have a rather high level of congruence with the results of site records and observation-based studies of the same taxa. Finally, in terms of conservation, analyses of species’ distributions might be expected to reveal not only hot spots but also cold spots resulting from losses or declines due to the activities of humans, such as the clearing of land, pollution of water, or the draining of wetlands. In a world of rapidly disappearing frogs, all such analyses are critical for identifying and assisting in the ranking of hotspots and other areas that, if conserved, will optimise our ability to retain the taxonomic and genetic diversity of Australian frogs.

REFERENCES

Anstis M (2013) Tadpoles and Frogs of Australia. New Holland Publishers, Sydney. Caley MJ, Schluter D (1997) The relationship between local and regional diversity. Ecology 78, 70–80. doi:10.1890/00129658(1997)078[0070:TRBLAR]2.0.CO;2 Cogger HG (2014) Reptiles and Amphibians of Australia. 7th Edition. CSIRO Publishing, Melbourne. Donnellan SC, McGuigan K, Knowles R, Mahony M, Moritz C (1999) Genetic evidence for species boundaries in frogs of the Litoria citropa species-group (Anura: Hylidae). Australian Journal of Zoology 47, 275–293. doi:10.1071/ZO99013

Doughty P (2016) Book Review: Reptiles and Amphibians of Australia. Seventh Edition. Harold G. Cogger. 2014. CSIRO Publishing. ISBN 9780-643100350. 1033 p. $148.95 (hardcover). Copeia 103, 1102–1107. Duellman WE, Marion AB, Hedges, SB (2016) Phylogenetics, classification, and biogeography of the treefrogs (Amphibia: Anura: Arboranae). Zootaxa 4104, 1–109. Frost DR (2017) Amphibian Species of the World: an Online Reference. Version 6.0 (27 May 2017). American Museum of Natural History, New York, USA, Hoskin CJ, Aland K (2011) Two new frog species (Microhylidae: Cophixalus) from boulder habitats on Cape York Peninsula, north-east Australia. Zootaxa 3027, 39–51. IUCN (2017) The IUCN Red List of Threatened Species. Version 2017-1. IUCN, Gland, Switzerland, . Lincoln RJ, Boxshall GA, Clark PF (1986) A Dictionary of Ecology, Evolution and Systematics. Cambridge University Press, Cambridge, UK. Menzies J (2006) The Frogs of New Guinea and the Solomon Islands. Pensoft Series Faunistica No. 48, Sofia, Bulgaria. Skerratt LF, Berger L, Clemann N, Hunter DA, Marantelli G, Newell DA, et al. (2016) Priorities for management of chytridiomycosis in Australia: saving frogs from extinction. Wildlife Research 43, 105–120. doi:10.1071/WR15071 Slatyer C, Rosauer D, Lemckert F (2007) An assessment of endemism and species richness patterns in the Australian Anura. Journal of Biogeography 34, 583–596. doi:10.1111/j.1365-2699.2006.01647.x Tyler MJ (1997) The Action Plan for Australian Frogs. Wildlife Australia (Environment Australia), Canberra. Tyler MJ (1999) Distribution of amphibians in the AustraloPapuan region. In Patterns of Distribution of Amphibians: a Global Perspective. (Ed. WE Duellman) pp. 541–563. Johns Hopkins University Press, Baltimore, MD, USA. Tyler MJ, Doughty P (2009) Field Guide to Frogs of Western Australia. 4th Edition, Western Australian Museum, Perth, WA. Tyler MJ, Knight F (2011) Field Guide to the Frogs of Australia. CSIRO Publishing, Melbourne. Tyler MJ, Lee MSY (2006) The origins of Australian frogs. In Evolution and Zoogeography of Australasian Vertebrates (Eds JR Merric, M Archer, G Hickey, and M Lee) pp. 237–240. Australian Scientific Publishing, Sydney. Vanderduys E (2012) Field Guide to the Frogs of Queensland. CSIRO Publishing, Melbourne. Voris HK (2000) Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. Journal of Biogeography 27, 1153–1167. Walker D (1972) Bridge and Barrier: the Natural and Cultural History of Torres Strait. Publication BG/3. Department of Biogeography and Geomorphology, Research School of Pacific Studies, Australian National University, Canberra. Williams PH (2000) WORLDMAP iv WINDOWS: Software and Help Document 4.2. Privately distributed, London, UK.

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3

Status of decline and conservation of frogs in the Wet Tropics of Australia Ross A. Alford and Jodi J. L. Rowley

THE DIVERSE AND ENDEMIC FROG FAUNA OF THE WET TROPICS The Wet Tropics bioregion in north-eastern Queensland encompasses 19 929 km2, of which approximately 8940 km2 is rainforest (Plate 3.1). Due largely to their high biodiversity and levels of endemism, the rainforests of the Wet Tropics were listed as a World Heritage Area in 1988 (Williams et al. 2003). More than 65% of the area now falls within protected areas (Australian Government 2017). The Wet Tropics has the highest species diversity of frogs in Australia (Slatyer et al. 2007). Despite covering only 0.12% of Australia’s land area, the region contains almost a quarter of Australia’s known species of frogs: at least 59 species are known from the region (Plate 3.2) and up to 45 species have been recorded within a single area of only 30  km2 (Slatyer et al. 2007). The areas of highest diversity are the uplands, including the Atherton, Carbine, and Thornton Uplands (Williams et al. 2008). These areas of high rainfall and high historical stability of habitats have acted as refugia for a number of species (Graham et al. 2006; Williams et al. 2008). The Wet Tropics is also the most important area of endemism for frogs in Australia (Slatyer et al. 2007) (Plate 3.2). This endemism is concentrated in the treefrogs (family Pelodryadidae) and microhylids (family Microhylidae) (Slatyer et al. 2007). Indeed, microhylid frogs account for more than half the species restricted to rainforest and have very high levels of regional endemism,

with several species restricted to one or two mountain tops (Williams et al. 2008). Fifteen species of microhylids in two genera occur in the Wet Topics, the more diverse of which is the genus Cophixalus, which is currently thought to be the only vertebrate genus to have radiated extensively within the Wet Tropics itself (Moritz et al. 2005). Our knowledge of the frog fauna of the Wet Tropics has been relatively slow to develop and may not be complete. The first species of frog known to be endemic to the Wet Tropics was described in 1897, more than a century after the first species of frog was described from Australia, and in the past decade there has been a rapid increase in the number of species described from the region, with seven described since 2000 (Table 3.1); six of these are restricted to rainforests and are endemic to the Wet Tropics.

THREATENED FROGS OF THE WET TROPICS Within the Wet Tropics, 16 species of frogs are listed as threatened (or extinct) under state, national, or global listings of threatened species (Table 3.2). The proportion of nationally threatened species of frogs in the Wet Tropics is 15% compared with 14% for Australia as a whole (Environment Protection and Biodiversity Conservation Act 1999; EPBC). The species of frogs endemic to rainforest are disproportionately at risk, with 30% of them considered nationally threatened. Only one of those in the

16

Status of Conservation and Decline of Amphibians

Table 3.1.  Species of frogs described from the Wet Tropics of Australia since 2000, listed chronologically by date of description. CR = Critically Endangered; LC = Least Concern, NA= Not Assessed NT = Near Threatened, VU = Vulnerable.

IUCN Red List Status

Restricted to rainforest

Microhylidae

VU

Yes

Pelodryadidae

NT

No

Myobatrachidae

LC

Yes

Species

Family

Cophixalus aenigma, Hoskin 2004 Litoria jungguy, Donnellan and Mahony 2004 Mixophyes carbinensis, Mahony, Donnellan, Richards, and McDonald 2006 Mixophyes coggeri, Mahony, Donnellan, Richards, and McDonald 2006

Myobatrachidae

LC

Yes

Litoria myola, Hoskin 2007

Pelodryadidae

CR

Yes

Cophixalus australis, Hoskin 2012

Microhylidae

NA

Yes

Cophixalus hinchinbrookensis, Hoskin 2012

Microhylidae

NA

Yes

Wet Tropics, the magnificent brood frog Pseudophryne covacevichae, is not restricted to rainforest (Table 3.2).

HISTORY OF DECLINES AND RESEARCH ON DECLINES The frogs of the Wet Tropics are likely to have suffered reductions in their ranges caused by modification of habitats, but the dramatic declines in frog populations observed in the late 1980s and early 1990s occurred in

relatively pristine forest. Eight species of endemic frogs associated with rainforest declined at upland sites; seven of these disappeared from all sites above ~400 m in elevation. Four species occurred only at higher elevations; three of these have not been seen since they declined, while another was recently rediscovered at a single site. During the 1990s, many hypotheses regarding the reasons for declines were suggested and investigated (Alford and Richards 1999; McDonald and Alford 1999), but none appeared to be likely. The frogs of the Wet Tropics were

Table 3.2.  Threatened species of frogs from the Wet Tropics of Australia and their categories of threat according to Queensland (Nature Conservation [Wildlife] Regulation 2006; Qld), Commonwealth (Environment Protection and Biodiversity Conservation Act 1999; EPBC) and global (IUCN Red List of Threatened Species; IUCN 2017). CR= Critically Endangered, EN= Endangered, EX= Extinct, NA=Not Assessed; VU= Vulnerable.

Species

Restricted to rainforest

Qld

EPBC

IUCN

Cophixalus aenigma

Yes

–

–

VU

Cophixalus concinnus

Yes

VU

–

CR

Cophixalus exiguus

Yes

VU

–

NT

Cophixalus monticola

Yes

VU

–

EN

Cophixalus neglectus

Yes

VU

–

EN

Cophixalus saxatilis

Yes

VU

–

VU

Litoria dayi

Yes

EN

EN

EN

Litoria lorica

Yes

EN

CR

CR

Litoria myola

Yes

EN

EN

CR

Litoria nannotis

Yes

EN

EN

EN

Litoria nyakalensis

Yes

EN

CR

CR

Litoria rheocola

Yes

EN

EN

EN

Litoria serrata

Yes

VU

–

NA

Pseudophryne covacevichae

No

VU

VU

EN

Taudactylus acutirostris

Yes

VU

EX

CR

Taudactylus rheophilus

Yes

EN

EN

CR

3 – Status of decline and conservation of frogs in the Wet Tropics of Australia

one of the first faunas from which the amphibian chytrid fungus (Batrachochytrium dendrobatidis) was isolated and described, and it has since become accepted that the declines observed in the 1980s and 1990s were caused by epidemic outbreaks of chytridiomycosis (Berger et al. 2016). The pathogen now occurs throughout the region. Fortunately, disappearances of frogs documented in 1994 seem to have been the last large-scale die-offs of vulnerable species in the Wet Tropics. Since then, a large body of research has shown how the die-offs happened and has begun to develop management tools that might help prevent or mitigate the severity of future mass mortalities. Disease Although it is now accepted that outbreaks of chytridiomycosis were the immediate cause of the declines of frogs in the Wet Tropics, the ultimate reasons for the timing of outbreaks and what determines the responses of species to chytridiomycosis are still unclear, despite almost 20 years of very intensive research. It is also not clear to what extent the disease may pose a future threat to frogs in the region. It is generally thought that B. dendrodbatidis was recently accidentally introduced into Australia, and rapidly spread to most climatically suitable areas of the continent (Berger et al. 2016). Although it is possible that initial epidemic outbreaks accompanied by species’ declines have occurred at the front of the pathogen’s increasing range, Phillips et al. (2012) pointed out that this hypothesis has never been tested in Australia. Some evidence, such as the lack of a clear spatio-temporal signal in the timing of declines in most of the Wet Tropics, and evidence of rising levels of stress before declines (Alford et al. 2007), suggests that epidemic outbreaks may not always have occurred immediately after the pathogen arrived in an area. Data from the Wet Tropics suggest that the severity, and possibly the timing, of chytridiomycotic epidemics may depend on weather. The spatial distribution of declines of the fauna in the Wet Tropics indicates that, in many species, the fate of frogs that become infected by B. dendrodbatidis is strongly affected by the external environment. The pathogen is present both at low and high elevations and fluctuates in abundance seasonally (Woodhams and Alford 2005). Some species with wide elevational distributions declined, often to apparent local extirpation in areas above 300–400  m elevation, while persisting, apparently unaffected at the population level, at low elevations (McDonald and Alford 1999). An early experiment (Woodhams et al. 2003) confirmed that short

exposures to 37oC cured frogs of B. dendrobatidis infections. These temperatures are reached by the air in lowland sites, and can be encountered by basking frogs at upland sites. There has been substantial additional work on how interactions between frogs and B. dendrobatidis are shaped by the behaviour of frogs and by the physical environment. McDonald and Alford (1999) established that species more closely associated with water are more likely to decline. Infections appear to be uncommon across all tested species of the family Microhylidae, which are terrestrial breeders with direct development and high sitefidelity (Hauselberger and Alford 2012). Interestingly, they can be experimentally infected, do not occupy microenvironments with high temperatures, and do not have more effective antimicrobial peptides than do species that frequently carry infections (Hauselberger 2010). Their very low prevalences of infection may reflect high philopatry and infrequent contact with water carrying infectious zoospores (Hauselberger 2010). In aquatic breeders, the vulnerability of individuals to becoming infected is likely dependent on their movements, degree of affinity with water, and aggregative behaviour (Rowley and Alford 2007). Once acquired, whether infections persist, are lost, or develop into disease, is likely to be affected by the effectiveness of antimicrobial peptides (Woodhams et al. 2006), by the composition of the skin’s microbiota (Daskin et al. 2014), and by individuals’ thermal histories (Rowley and Alford 2013). These can interact so that factors such as canopy-cover can affect the probability that individual frogs are infected, as occurred when a tropical cyclone reduced cover, followed by a lowered prevalence of infection at some monitored sites (Roznik et al. 2015). Sites with lower canopy cover may act as ‘environmental refuges’; for example, Puschendorf et al. (2011) reported the rediscovery of the armoured mist frog Litoria lorica, which had been extirpated at all known sites in the Wet Tropics in the early 1990s, at a site in open forest just outside the Wet Tropics. Chytridiomycosis poses a continuing threat to the frogs of the Wet Tropics, because it is present throughout the region (McDonald et al. 2005), and infections by B. dendrobatidis can reach prevalences greater than 50% during the winter (Sapsford et al. 2015). If those infections all developed into fatal chytridiomycosis, declines would certainly be ongoing. However, a mark–recapture study of the common mist frog Litoria rheocola, a WetTropics species that was severely affected by initial outbreaks of chytridiomycosis and that disappeared from all

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known sites above 400  m, failed to detect significant or substantial effects of infection by B. dendrobatidis on individual survival rates, even in upland populations that were initially extirpated by chytridiomycosis (Sapsford et al. 2015). They also found relatively high rates of recovery from infection by individuals. Another study (Phillott et al. 2013) found correlations between seasonal timing of higher prevalence and increased mortality rates, but no evidence that individuals’ status of infection affected their probability of survival, as estimated by mark–recapture. High prevalences but non-significant effects on survival rates suggest that, at present, chytridiomycosis has only minor effects on populations of this species, and possibly on populations of other species that have recovered or recolonised at sites from which they had been extirpated. Although a great deal is now known about host–pathogen interactions between B. dendrobatidis and frogs in the Wet Tropics, we still do not know why one species that declined (the green-eyed tree frog Litoria serrata) and two that were extensively extirpated (the common mist frog L. rheocola and the waterfall frog Litoria nannotis) have recovered and now coexist with the pathogen. The dynamics of infections may have changed because hosts have evolved behavioural adaptations, or changes in their antimicrobial peptides, or other aspects of their immune systems. It is also possible that selection has acted on the microbiota of frogs, favouring assemblages that confer greater resistance to infections. The initial outbreaks may have been initiated by highly specific local weather conditions that temporarily allowed populations of pathogens to reach fatal levels on hosts and disperse massive numbers of propagules, causing a spike in incidence of infections and development of disease, and these patterns may not have been repeated. Until we know more about the status of resistance to, or tolerance of, B. dendrobatidis infections by the frogs of the Wet Tropics, the possibility of future epidemic outbreaks, perhaps affecting more species and extending to lowland sites, will always loom. Loss and modification of habitat About 70% of the Wet Tropics is covered by native vegetation but this is unequally distributed, with lowland rainforests and the more fertile uplands disproportionately cleared for agriculture (Metcalfe and Lawson 2015). The Wet Tropics supported an important logging industry until the late 1980s (Laurance 1997) and about 70% of the lowland forests and large areas of upland forests, especially on the Atherton Tablelands, have been cleared since

European settlement (Winter et al. 1987; Woinarski 2010). Largely because of these changes, the coastal lowland rainforest of the Wet Tropics recently has been assessed as Endangered (Metcalfe and Lawson 2015). The ability of frogs to persist in fragmented landscapes is likely to differ greatly among species. Stenotopic species displaying sedentary behaviour, such as the rainforest-restricted waterfall frogs (L. nannotis), are likely to be more vulnerable to extinction in human-modified landscapes, compared with more vagile and generalist species, such as the stony creek frogs L. jungguy and L. wilcoxii (Rowley and Alford 2007). Clearing and natural perturbations, such as cyclones, are likely to have an impact upon species known to occur only in small areas (e.g. many of the microhylids). Introduced species The amphibian chytrid fungus, B. dendrobatidis, is probably a recent invader in the Wet Tropics; the severe impacts it has had on the frog fauna of the region were discussed above. The Wet Tropics have been colonised by the invasive cane toad Rhinella marina, which apparently brought at least one lungworm parasite with it when it was introduced (see Chapter 10) (Dubey and Shine 2008). The cane toad may compete with, and prey upon, juveniles of native species, and its parasites could infect native populations of frogs. However, it appears that the cane toad has had little effect on populations of native frogs in other parts of Australia (see Chapter 10) (Shine 2010), and the species has been present in much of the Wet Tropics for many years, so it seems unlikely that it, or its parasites, are major threats. The Wet Tropics also are threatened by invasive species of other taxa, including highly aggressive ants, such as the yellow crazy ant Anoplolepis gracilipes and the little fire ant Wasmannia auropunctata, both of which have affected the diversity of small vertebrates in other areas they have invaded (Wet Tropics Management Authority 2017b). At least six species of non-native fish have established populations in the Wet Tropics (Kroon et al. 2015); predation or competition from these species may affect aquatically breeding frogs, although at present there is no evidence of this. Feral pigs (Sus scrofa) commonly are present in the Wet Tropics and are known predators of frogs (Richards et al. 1994), but research in the 1990s did not demonstrate serious effects on frog populations (McDonald and Alford 1999). At present, invasive species (other than B. dendrobatidis) do not appear to pose direct or immediate threats to the frogs of the Wet Tropics, but the invasive ants may eventually be a

3 – Status of decline and conservation of frogs in the Wet Tropics of Australia

major threat, particularly to the terrestrially breeding microhylids, which have minute terrestrial juveniles, relatively low fecundity, and are highly philopatric (Hoskin 2004). Finally, introduced pathogens of plants ultimately may threaten the frogs of the Wet Tropics by impacting the rainforests they require for habitat. The fungi Phytophthora cinnamomi and Puccinia psidii both pose major threats to many species of rainforest trees (Wet Tropics Management Authority 2017a,c). Climatic change Climatic change is likely to threaten many of the microhylid species of the Wet Tropics in the relatively near future. These frogs are highly philopatric, with relatively low rates of reproduction, and many species have small ranges at high elevations (Hoskin 2004). A warming climate may make areas with bioclimatic conditions suitable for these species disappear from the tops of the mountains on which most of these species of frogs now occur (Williams et al. 2003). These effects may be moderated by shifts in the use of microhabitats, but are likely to be severe if climatic change is rapid or extreme. In addition to contractions of range caused by shifts in local environmental conditions, climatic change may threaten the frogs of the Wet Tropics by altering host–pathogen relationships. A simplistic view suggests that a warming climate would be likely to improve the chance of frogs coexisting successfully with B. dendrobatidis, simply by moving upward the apparent 300–400 m elevational cutoff below which no species appear to be negatively affected. However, it is likely that seasonal patterns of rainfall and cloud cover will change, as well as temperatures, with rainfall becoming more seasonal, and with an increasing frequency of extreme events (Wet Tropics Management Authority 2008). If extreme events reduce the opportunities of frogs to regulate their body temperatures in times of increased rainfall, or bring about aggregation in moist retreats during drier times, the rates of transmission of infection and the development of chytridiomycosis (and thus the threat it poses to the frogs of the Wet Tropics) could increase. Changes in patterns of aggregation and in use of habitat also could cause the pathogen to spread to microhylids, possibly causing a new wave of extinctions among these species.

RECOVERIES AND REDISCOVERIES The declines that occurred in the Wet Tropics in the late 1980s and early 1990s were well documented by Richards

et al (1994) and McDonald and Alford (1999). Extensive searches and acoustic monitoring at historical localities and additional similar sites for the sharp-snouted day frog Taudactylus acutirostris, northern tinker frog Taudactylus rheophilus, mountain mist frog Litoria nyakalensis, and armoured mist frog L. lorica carried out during the late 1990s and early 2000s failed to discover extant populations, although acoustic monitoring suggested a few T. rheophilus might have remained at one site into the late 1990s (Northern Queensland Threatened Frogs Recovery Team 2001). Biologists working in the Wet Tropics have been aware since the late 1990s that populations of green-eyed tree frogs (L. serrata) recovered to pre-decline levels relatively rapidly (Richards and Alford 2005; Woodhams and Alford 2005), and that waterfall frogs L. nannotis and common mist frogs L. rheocola have reappeared at many (although not all) upland sites from which they apparently were extirpated in the late 1980s and early 1990s (e.g. McDonald et al. 2005; Woodhams and Alford 2005; Sapsford et al. 2015). There have been no systematic regional surveys documenting the timing and extent of these species’ reappearances. One species, L. lorica, that had last been seen in 1991, was rediscovered in 2008 during a study of the dynamics of a recovered rainforest population of the closely related L. nannotis (Puschendorf et al. 2011). The population inhabits a rocky, open-forest section of a stream flowing westward from Wet Tropics rainforest. Surveys of similar sites failed to locate any additional populations. Small-scale trial transplantations into some of these sites may be succeeding in establishing viable populations (C. Hoskin pers. comm.).

FUTURE OF FROGS AND RESEARCH DIRECTIONS The immediate crisis caused by outbreaks of chytridiomycosis in the late 1980s and early 1990s has passed, and populations of some species are recovering or recolonising many sites. At present, the batrachian fauna of the Wet Tropics appears to be free of immediate threats from this disease. However, future research aimed at understanding the causes of outbreaks seems warranted, because at present it is not clear whether fluctuations in weather conditions or climatic change could trigger future catastrophic outbreaks. If the species that have recovered and recolonised have acquired resistance to, or tolerance of, infection by B. dendrobatidis, they represent a resource in the form of a model system that is likely to

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have evolved repeatedly and separately, because gene flow over large distances between catchments in the Wet Tropics appears to be relatively rare (Hoskin et al. 2011). Discovering the mechanisms they have evolved may aid in conserving amphibians in other regions. The microhylid frogs of the Wet Tropics may be at the greatest risk in the near future, possibly from direct or indirect effects of a warming climate and of chytridiomycosis, and also from the threat of introduced predatory ants. As outlined earlier, many other potential threats face the frogs of the Wet Tropics in the future. A better understanding of their current status and ecology might aid in future efforts to conserve them. It seems likely that some interventions, via translocations or by bringing species into survivalassurance colonies, may be needed as the pace of climatic change increases and ecological change and invasive species make survival uncertain.

SUMMARY AND CONCLUSIONS The Wet Tropics contains the highest level of diversity and endemism of frogs in Australia (e.g. Plate 3.3), yet it is already relatively depauperate compared with the massive diversity of frogs seen in nearby New Guinea. Dramatic declines in frog populations and in extinctions occurred in the late 1980s and 1990s; three species are now likely extinct. New species continue to be described from the region, either split from existing species with the aid of molecular and/or bioacoustic data, or discovered in remote areas that still have not been fully explored for their amphibian fauna. Major threats exist, both from possible future outbreaks of chytridiomycosis and its spread into previously uninfected populations, as well as from the more direct effects of climatic change, introduced species, and loss of suitable habitat. Effective conservation of the frogs of the Wet Tropics will require a better understanding of their diversity and ecology, and probably will require intensive intervention as the 21st century progresses.

REFERENCES

Alford RA, Richards SJ (1999) Global amphibian declines: a problem in applied ecology. Annual Review of Ecology and Systematics 30, 133–165. doi:10.1146/annurev.ecolsys.30.1.133 Alford RA, Bradfield KS, Richards SJ (2007) Ecology: global warming and amphibian losses. Nature 447, E3–E4. doi:10.1038/nature05940

Australian Government (2017) World Heritage Places – Wet Tropics of Queensland – Outstanding Universal Value. Archived 26 April 2017, Department of the Environment and Energy, Canberra, https://web.archive.org/web/2017 0426062030/http://www.environment.gov.au/heritage/ places/world/wet-tropics/values Berger L, Roberts AA, Voyles J, Longcore JE, Murray K, Skerratt LF (2016) History and recent progress on chytridiomycosis in amphibians. Fungal Ecology 19, 89–99. doi:10.1016/j. funeco.2015.09.007 Daskin JH, Bell SC, Schwarzkopf L, Alford RA (2014) Cool temperatures reduce antifungal activity of symbiotic bacteria of threatened amphibians – implications for disease management and patterns of decline. PLoS One 9(6), e100378. doi:10.1371/journal.pone.0100378 Donnellan SC, Mahony MJ (2004) Allozyme, chromosomal and morphological variability in the Litoria lesueuri species group (Anura: Hylidae), including a description of a new species. Australian Journal of Zoology 52, 1–28. doi:10.1071/ ZO02069 Dubey S, Shine R (2008) Origin of the parasites of an invading species, the Australian cane toad (Bufo marinus): are the lungworms Australian or American? Molecular Ecology 17, 4418–4424. doi:10.1111/j.1365-294X.2008.03922.x Graham CH, Moritz C, Williams SE (2006) Habitat history improves prediction of biodiversity in rainforest fauna. Proceedings of the National Academy of Sciences of the United States of America 103, 632–636. doi:10.1073/pnas.0505754103 Hauselberger KF (2010) Ecology of microhylid frogs in the Australian Wet Tropics and implications for their vulnerability to chytridiomycosis. PhD thesis, James Cook University, Townsville, Australia, https://web.archive.org/web/2017 0 5 0 2 0 5 51 2 6 / h t t p s : //r e s e a r c h o n l i n e . j c u . e d u . au/18159/3/02whole.pdf Hauselberger KF, Alford RA (2012) Prevalence of Batrachochytrium dendrobatidis infection is extremely low in direct-developing Australian microhylids. Diseases of Aquatic Organisms 100, 191–200. doi:10.3354/dao02494 Hoskin CJ (2004) Australian microhylid frogs (Cophixalus and Austrochaperina): phylogeny, taxonomy, calls, distributions and breeding biology. Australian Journal of Zoology 52, 237–269. doi:10.1071/ZO03056 Hoskin CJ (2007) Description, biology and conservation of a new species of Australian tree frog (Amphibia: Anura: Hylidae: Litoria) and an assessment of the remaining populations of Litoria genimaculata Horst, 1883: systematic and conservation implications of an unusual speciation event. Biological Journal of the Linnean Society. Linnean Society of London 91, 549–563. doi:10.1111/j.1095-8312.2007.00805.x Hoskin CJ (2012) Two new frog species (Microhylidae: Cophixalus) from the Australian Wet Tropics region, and redescription of Cophixalus ornatus. Zootaxa 3271, 1–16. Hoskin CJ, Tonione M, Higgie M, MacKenzie JB, Williams SE, VanDerWal J, et al. (2011) Persistence in peripheral refugia promotes phenotypic divergence and speciation in a rain-

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forest frog. American Naturalist 178, 561–578. doi:10.1086/ 662164 IUCN (2017) The IUCN Red List of Threatened Species. Version 2017-1. IUCN, Gland, Switzerland, . Kroon F, Phillips S, Burrows D, Hogan A (2015) Presence and absence of non-native fish species in the Wet Tropics region, Australia. Journal of Fish Biology 86, 1177–1185. doi:10.1111/ jfb.12614 Laurance WF (1997) Responses of mammals to rainforest fragmentation in tropical Queensland: a review and synthesis. Wildlife Research 24, 603–612. Mahony MJ, Donnellan SC, Richards SJ, McDonald KR (2006) Species boundaries among barred river frogs, Mixophyes (Anura: Myobatrachidae) in north-eastern Australia, with descriptions of two new species. Zootaxa 1228, 35–60. McDonald KR, Alford RA (1999) A review of declining frogs in northern Queensland. In Declines and Disappearances of Australian Frogs. (Ed. A Campbell) pp. 14–22. Environment Australia, Canberra. McDonald K, Mendez D, Muller R, Freeman A, Speare R (2005) Decline in prevalence of chytridiomycosis in frog populations in North Queensland, Australia. Pacific Conservation Biology 11, 114–120. doi:10.1071/PC050114 Metcalfe DJ, Lawson TJ (2015) An International Union for Conservation of Nature risk assessment of coastal lowland rainforests of the Wet Tropics Bioregion, Queensland, Australia. Austral Ecology 40, 373–385. Moritz C, Hoskin C, Graham CH, Hugall A, Moussalli A (2005) Historical biogeography, diversity and conservation of Australia’s tropical rainforest herpetofauna. In Phylogeny and Conservation. Series 8 (Eds A Purvis, GI Gittleman, and T Brooks) pp. 243–264. Cambridge University Press, Cambridge, UK. Northern Queensland Threatened Frogs Recovery Team (2001) Recovery plan for the stream-dwelling rainforest frogs of the Wet Tropics biogeographic region of north-east Queensland 2000–2004. Report to Environment Australia, Canberra. Queensland Parks and Wildlife Service, Brisbane, . Phillips BL, Puschendorf R, VanDerWal J, Alford RA (2012) There is no evidence for a temporal link between pathogen arrival and frog extinctions in north-eastern Australia. PLoS One 7, e52502. doi:10.1371/journal.pone.0052502 Phillott AD, Grogan LF, Cashins SD, McDonald KR, Berger L, Skerratt LF (2013) Chytridiomycosis and seasonal mortality of tropical stream-associated frogs 15 years after introduction of Batrachochytrium dendrobatidis. Conservation Biology 27, 1058–1068. doi:10.1111/cobi.12073 Puschendorf R, Hoskin CJ, Cashins SD, McDonald K, Skerratt LF, Vanderwal J, et al. (2011) Environmental refuge from disease‐driven amphibian extinction. Conservation Biology 25, 956–964. doi:10.1111/j.1523-1739.2011.01728.x

Richards SJ, Alford RA (2005) Structure and dynamics of a rainforest frog (Litoria genimaculata) population in northern Queensland. Australian Journal of Zoology 53, 229–236. doi:10.1071/ZO03036 Richards S, McDonald K, Alford R (1994) Declines in populations of Australia’s endemic tropical rainforest frogs. Pacific Conservation Biology 1, 66–77. doi:10.1071/PC930066 Rowley JJ, Alford RA (2007) Movement patterns and habitat use of rainforest stream frogs in northern Queensland, Australia: implications for extinction vulnerability. Wildlife Research 34, 371–378. doi:10.1071/WR07014 Rowley JJL, Alford RA (2013) Hot bodies protect amphibians against chytrid infection in nature. Scientific Reports 3, 1515. doi:10.1038/srep01515 Roznik EA, Sapsford SJ, Pike DA, Schwarzkopf L, Alford RA (2015) Natural disturbance reduces disease risk in endangered rainforest frog populations. Scientific Reports 5, 13472. doi:10.1038/srep13472 Sapsford SJ, Voordouw MJ, Alford RA, Schwarzkopf L (2015) Infection dynamics in frog populations with different histories of decline caused by a deadly disease. Oecologia 179, 1099–1110. doi:10.1007/s00442-015-3422-3 Shine R (2010) The ecological impact of invasive cane toads (Bufo marinus) in Australia. The Quarterly Review of Biology 85, 253–291. doi:10.1086/655116 Slatyer C, Rosauer D, Lemckert F (2007) An assessment of endemism and species richness patterns in the Australian anura. Journal of Biogeography 34, 583–596. doi:10.1111/ j.1365-2699.2006.01647.x Wet Tropics Management Authority (2008) Climate Change in the Wet Tropics. Impacts and Responses. Wet Tropics Management Authority, Cairns, . Wet Tropics Management Authority (2017a) Myrtle Rust. Wet Tropics Management Authority, Cairns, . Wet Tropics Management Authority (2017b) New Feral Animals. Wet Tropics Management Authority, Cairns, . Wet Tropics Management Authority (2017c) Phytophthora cinnamomi. Wet Tropics Management Authority, Cairns, . Williams SE, Bolitho EE, Fox S (2003) Climate change in Australian tropical rainforests: an impending environmental catastrophe. Proceedings of the Royal Society of London. Series B, Biological Sciences 270, 1887–1892. doi:10.1098/ rspb.2003.2464 Williams SE, Isaac JL, Graham C, Moritz C (2008) Towards an understanding of vertebrate biodiversity in the Australian Wet Tropics. In Living in a Dynamic Tropical Forest Land-

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scape. (Eds NE Stork and SM Turton) pp. 133–149. Blackwell Publishing, Oxford, UK, doi:10.1002/9781444300321.ch10 Winter JW, Bell FC, Pahl LI, Atherton RG (1987) Rainforest clearfelling in northeastern Australia. Proceedings of the Royal Society of Queensland 98, 41–57. Woinarski JCZ (2010) Biodiversity conservation in tropical forest landscapes of Oceania. Biological Conservation 143, 2385–2394. doi:10.1016/j.biocon.2009.12.009 Woodhams D, Alford RA (2005) Ecology of chytridiomycosis in rainforest stream frog assemblages of tropical Queens-

land. Conservation Biology 19, 1449–1459. doi:10.1111/ j.1523-1739.2005.004403.x Woodhams DC, Alford RA, Marantelli G (2003) Emerging disease of amphibians cured by elevated body temperature. Diseases of Aquatic Organisms 55, 65–67. Woodhams DC, Rollins-Smith LA, Carey C, Reinert L, Tyler MJ, Alford RA (2006) Population trends associated with skin peptide defenses against chytridiomycosis in Australian frogs. Oecologia 146, 531–540. doi:10.1007/s00442005-0228-8

4

Frogs of the monsoon tropical savannah regions of northern Australia Graeme R. Gillespie and J. Dale Roberts

INTRODUCTION Northern Australia is dominated by the largest region of monsoon tropical savannah ecosystem in the world, extending from the Pilbara and Kimberley coasts in Western Australia, across the Top End of the Northern Territory, to the western fall of the Great Dividing Range in North Queensland (Plate 4.1). This biogeographic region is defined climatically by areas that receive more than 85% of their annual rainfall between November and April (Bowman et al. 2010). Major rainfall events are associated with disturbances in the monsoon trough (McBride and Keenan 1982). The region is warm yearround with daily temperatures typically exceeding 30oC. The environment is characterised by extensive lowland woodlands and grasslands, interspersed with rocky escarpments and dissected plateaus sheltering small remnant patches of monsoon rainforest, and bisected by large rivers with extensive, seasonally inundated, flood plains (Bowman et al. 2010). This region also encompasses a large proportion of Australia’s offshore islands in the Kimberley region of Western Australia, Top End of the Northern Territory, and Torres Strait Islands between Cape York and Papua New Guinea. Seventy native species of frogs from five families, and the introduced cane toad (Rhinella marinus), have been recorded in this region. This number is expected to rise, however, as new species continue to be discovered and previously described taxa become subdivided in light of

new molecular information. No species are known to be endemic to offshore islands.

THREATENED SPECIES Only one species currently is listed as threatened in this region – the Howard River toadlet Uperoleia daviesi. It is listed as Endangered nationally by the Environment Protection and Biodiversity Conservation Act 1999 (EPBC), Vulnerable under the Northern Territory Parks and Wildlife Conservation Act 2000 and by the International Union for the Conservation of Nature (IUCN) (2012). Uperoleia daviesi has a highly restricted distribution (less than 200  km2) in the catchments of the Howard River and Elizabeth rivers in the outer Darwin area of the Northern Territory (Fisher et al. 2011). It is associated with Sand-Sheet Heath: a vegetation community that occurs on seasonally inundated sandy soils (Dostine et al. 2013). Little is known about its ecology but the species calls from inundated low vegetation during the wet season and presumably disperses into surrounding heathland and woodland habitats at other times, as found for some other species of Uperoleia (Westgate et al. 2012). Much of the habitat of Uperoleia daviesi is in Darwin’s peri-urban area of growth, and is threatened by the city’s urban expansion (Woinarski et al. 2007). Some habitat has also been lost or disturbed by sandmining (Price et al. 2005). Impacts on the species include direct loss of habitat

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and changes in sub-catchment hydrology from disturbances adjacent to, or upstream of, areas of habitat. There is no evidence of population declines in the species in areas of intact habitat, but no systematic monitoring is in place to properly evaluate such declines. The Northern Territory Environment Protection Authority (2015) recently recommended the creation of a protected area covering significant proportions of the remaining intact Sand-Sheet Heath with a surrounding buffer of woodland habitat to protect a range of threatened species restricted to this habitat. The low number of threatened amphibian species in Australian monsoon tropical savannah compared with those along the mesic eastern coastal fall of the Great Dividing Range and southwestern Western Australia (see other chapters), may be due to several factors: (1) native vegetation, catchments, and wetlands are mostly intact, although small areas have been cleared and fragmented from limited intensive agriculture or silviculture; (2) ambient daily temperatures exceed 28oC year-round throughout most of this region, thereby greatly limiting potential impact of the amphibian chytrid fungus Batrachochytrium dendrobatidis (Woodhams et al. 2003; Berger et al. 2004; Retallick and Miera 2007; Andre et al. 2008), which has been implicated in declines of numerous species elsewhere in Australia and globally (Berger et al. 1998; Skerratt et al. 2007); (3) there are few stream-breeding species, an ecological characteristic that has been associated with predisposing other Australian species of frogs to high risk of extinction (Hero et al. 2005); (4) the life histories of most species reflect the warm climate and the highly unpredictable nature of monsoonal rains – many are explosive breeders (Anstis 2013), and they probably have short generation times with relatively high intrinsic rates of increase of their populations; (5) the sparsely distributed human population across the region may reduce the risk of dispersal of disease and invasive predators (Daszak et al. 2001; Crowl et al. 2008). However, higher levels of uncertainty exist in conservation assessments of frogs in this region compared with other parts of the continent (Gillespie et al. 2011). This uncertainty arises in part because of: the sparse human population; remoteness and difficulty in accessing many areas during the wet season; incomplete knowledge of systematics, as reflected by recent species discoveries and revisions (Doughty and Anstis 2007; Doughty 2011; Catullo et al. 2011), limited surveys of species’ distributions, less knowledge of ecological requirements of many species, and virtually no monitoring to evaluate population

trends (Gillespie et al. 2011; Pusey et al. 2011; Dostine et al. 2013).

DATA DEFICIENT SPECIES Three species in the region are considered Data Deficient under the IUCN (2012): the marbled toadlet Uperoleia marmorata, Alexandria toadlet Uperoleia orientalis, and the Kimberley rocket frog Litoria axillaris. Uperoleia marmorata is known from a single specimen suspected to have been collected in the Prince Regent River region, west Kimberley, Western Australia in 1841 (Anstis 2013). Subsequent surveys have failed to locate any specimens of Uperoleia resembling this taxon in the region, and to date it has not been possible to extract suitable molecular material from the sole museum specimen to evaluate its relationships to other conspecifics (Catullo et al. 2011, 2014). Whether U. marmorata is/was a highly rangerestricted species or synonymous with another described species in the region remains unknown. Uperoleia orientalis has been reported infrequently from the Barkly region of the Northern Territory and north-western Queensland. However, despite comprehensive survey and molecular work on this genus (Catullo et al. 2011, 2014; Catullo and Keogh 2014), the taxonomic status of this species is uncertain. No confirmed specimens have been collected since the 1990s (Catullo and Keogh 2014). Specimens have been variously accepted and rejected as being this species (e.g. see Davies 1989) and museum specimens registered as U. orientalis cannot be confidently assigned to any taxon (P. Doughty pers. comm.). Litoria axillaris was discovered only recently (Doughty 2011) and is known from only two localities in the Kimberley’s Prince Regent River area. Little is known about this species’ ecology and its population size and current status are unknown.

RANGE-LIMITED SPECIES An additional five species of Uperoleia either have highly restricted ranges, or are represented only by a very small number of records within a larger range: the Derby toadlet U. aspera, fat toadlet U. crassa, tiny toadlet U. micra, small toadlet U. minima, and Mjoberg’s toadlet U. mjobergii in the Kimberley region of Western Australia. One treefrog, the masked frog Litoria personata, is also restricted to the Arnhem Land escarpment in the Northern Territory.

4 – Frogs of the monsoon tropical savannah regions of northern Australia

Species with restricted ranges are considered to be more vulnerable to extinction due to greater risk of environmental stochasticity and limited opportunities for recolonisation after local extirpation (Purvis et al. 2000). The latter will be true particularly if species are distributed patchily within their ranges, although detailed distributions and dispersal capacity are rarely well described for most anuran species. Species with sparse records present a major problem. Are they rare, and/or patchily distributed, or rarely sampled? For example, Uperoleia micra was first collected in the vicinity of the Prince Regent River, but has since been collected at five other sites on the mainland and on an island off the Kimberley coast. This species may be widely distributed but in terrain that is generally difficult to access, let alone survey systematically, or it may be rare and very patchily distributed. The first collections were made in seepages, high on escarpments above Bachsten Creek (Doughty and Roberts 2008). Based on information about habitats from the database of the Atlas of Living Australia (accessed 22 November 2016), this species also has been collected from: temporary pools on sandstone, sandstone, and basalt pavements; a rock platform; and under a spinifex clump near rock. Uperoleia micra may therefore be widely distributed but poorly sampled. Most threatened species elsewhere in Australia have highly restricted distributions and are stenotopic (see other chapters). Various surveys over the past 10 years in the Top End and Kimberley regions have found no evidence of declining populations or contractions of range for any of the species discussed here (Department of Environment and Natural Resources, Northern Territory, unpublished data; Department of Parks and Wildlife, WA, unpublished data), but no systematic monitoring is in place for any of these species.

POTENTIAL AND EMERGING THREATS Despite the absence, or low prevalence, in northern Australian monsoon tropical regions of most of the threatening processes driving the declines of frogs elsewhere in Australasia, the environment and biota have undergone substantial change during European settlement. Until recently, biota of this region appeared more robust (e.g. Garnett et al. 2010). Secure populations of numerous species persisted here that elsewhere in Australia have declined or disappeared (Garnett et al. 2010). There is now compelling and increasing evidence that many

elements of the biota of the monsoonal tropics of northern Australia are in decline (e.g. Bowman and Panton 1993; Russell-Smith et al. 1998; Franklin 1999; Griffiths and McKay 2007; Woinarski et al. 2010; Ziembicki et al. 2015). The causes of these declines include: feral herbivores, omnivores (pigs), predators (cats), and cane toads (poisonings) (see Chapter 10); altered fire regimes; exotic weeds; livestock grazing; and their various interactions (Garnett et al. 2010; Ziembicki et al. 2015). To date, there is little evidence of significant adverse impacts of these ecological changes on the amphibian fauna of monsoon tropical regions. Adverse impacts on amphibians from several of these factors, have, however, been reported elsewhere, including fire (Driscoll and Roberts 1997; Hero and Morrison 2004; Bower et al. 2006), grazing (Jansen and Healey 2003; Bower et al. 2006), weeds (Bower et al. 2006), and feral pigs (WardellJohnson and Roberts 1991; Roberts et al. 1999; Office of the Environment and Heritage New South Wales 2012). Other emerging threats to amphibians in the region include expansion of intensive agriculture and associated irrigation schemes, invasion of exotic species of fish, and climatic change. There is renewed interest in developing and expanding more intensive agriculture across northern Australia (Commonwealth of Australia 2015). Loss of habitat from the clearing of land for agriculture and through new dams, and downstream hydrological changes may adversely affect some species. Several exotic freshwater species of fish have been detected in some northern Australian waterways, including mosquito fish Gambusia affinis and African mouthbreeder (Tilapia spp.) (D. Wilson, Department of Primary Industries, Northern Territory, unpublished data). These species have significant potential to adversely affect frogs (Gillespie and Hero 1999; Cucherousset and Olden 2011). The impacts of climatic change on amphibians in this region are difficult to predict, but may include increased temperature and evaporative loss (Hughes 2003), increased cyclonic activity (Walsh and Ryan 2000), increased frequency and intensity of fire (Williams et al. 2009), and further intrusion of salt water into floodplains and lowland wetland systems (Eliot et al. 1999). In contrast to birds and mammals (e.g. Woinarski et al. 2010, 2012), the few monitoring programs in this region that sample frogs typically lack adequate power to detect changes in populations or in areas of occurrence (e.g. L. Einoder, G. Gillespie, and A. Fisher, Department of Environment and Natural Resources, Northern

25

26

Status of Conservation and Decline of Amphibians

Territory, unpublished data), with the intensive monitoring of several floodplain species at Fogg Dam near Darwin being the only exception (Brown and Shine 2006, unpublished data). This situation reflects in part the logistical challenges of surveying many areas during the wet season, when most frogs are active (e.g. Dostine et al. 2013). Consequently, it is unlikely that adverse changes in distribution and population sizes of amphibian species resulting from any of these environmental pressures would be detected. Nevertheless, the explosion of knowledge about the taxonomy of frogs across the Kimberley and the Northern Territory is almost exclusively a consequence of focused field work in the wet season, initially in accessible locations (e.g. Tyler et al. 1981), followed by planned visits to more remote sites (e.g. Doughty and Roberts 2008). There may be ways to generate data on distribution and abundance that are of better quality. For example, automatic recording units coupled with effective software for recognising calls during multi-species choruses in noisy environments (e.g. Ramli and Jaafar 2016) could avoid some of the issues with accessibility during the wet season, provide raw data for modelling probabilities of detection and occupancy that could further refine conditions for targeted sampling of sites, and allow long-term monitoring of sites for presence /absence of particular species.

PRIORITIES FOR MANAGEMENT AND CONSERVATION A lot remains to be learned about the diversity and ecology of frogs in the monsoonal tropics, and how best to maintain viable populations in a changing environment. The following actions are considered to be the immediate priorities on which researchers and managers should focus their efforts: (1) more targeted surveys for Data Deficient species are required to ascertain their conservation status; (2) further resolution of the systematics of northern Australian anurans will improve understanding of the distribution of biodiversity throughout the region; and (3) establish monitoring programs in key biomes and areas with high amphibian biodiversity in order to track longterm trends across the region, especially in areas where threats and/or development-pressure are focused.

SUMMARY AND CONCLUSIONS Seventy native species of frog have been recorded in Australia’s northern tropical savannah region. Only one

species is considered threatened: the Howard River Toadlet Uperoleia daviesi. Its IUCN listing is Endangered and it has a highly restricted distribution in the peri-urban region of Darwin where it is associated with Sand-Sheet Heathlands. It is threatened by destruction and fragmentation of its habitat from sandmining and expanding urbanisation. Management proposals have been developed to protect part of its habitat from further disturbance. Three species are considered Data Deficient, and a further four species are extremely restricted in range. The low number of threatened species in this region, compared with elsewhere in Australia, may reflect lower levels of alteration of habitats across the region, climatic restriction/exclusion of the amphibian chytrid fungus, absence or highly restricted distribution of exotic amphibian predators, and a low population density of humans. However, higher levels of uncertainty exist in assessment of conservation in this region compared with other parts of the continent due to lower effort in conducting baseline surveys and to limited monitoring of species. Consequently, current assessments of conservation status may underestimate the risk of extinction. Potential and emerging threats to amphibians in the region include: the long-term pervasive effects of altered fire regimes; disturbance from introduced herbivores and pigs; agricultural intensification; and invasive, exotic species of fish. The impact of climatic change on amphibians in this region is unknown, but may include increased temperature and reduced soil moisture during dry seasons, increased severity of cyclones, increased frequency and intensity of fire, intrusion of salt water into floodplains and lowland wetland systems. Key priorities include surveys to better resolve species’ systematics and distributions, and establishment of monitoring programs to evaluate trends in populations.

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monsoonal tropics of northern Australia: implications for the design of monitoring studies. Wildlife Research 40, 393–402. Doughty P (2011) An emerging frog diversity hotspot in the northwest Kimberley of Western Australia: another new frog species from the high rainfall zone. Records of the Western Australian Museum 26, 209–216. doi:10.18195/ issn.0312-3162.26(2).2011.209-216 Doughty P, Anstis M (2007) A new species of rock-dwelling hylid frog (Anura: Hylidae) from the eastern Kimberley region of Western Australia. Records of the Western Australian Museum 23, 241–257. doi:10.18195/issn.0312-3162.23(3). 2007.241-257 Doughty P, Roberts JD (2008) A new species of Uperoleia (Anura: Myobatrachidae) from the northwest Kimberley, Western Australia. Zootaxa 1939, 10–18. Driscoll DA, Roberts JD (1997) Impact of fuel reduction burning on the frog Geocrinia lutea in south west Western Australia. Australian Journal of Ecology 22, 334–339. Eliot I, Finlayson CM, Waterman P (1999) Predicted climate change, sea-level rise and wetland management in the Australian wet-dry tropics. Wetlands Ecology and Management 7, 63–81. doi:10.1023/A:1008477110382 Environment Australia (2000) ‘Revision of the Interim Biogeographic Regionalisation of Australia (IBRA) and Development of Version 5.1’. Summary Report. Department of Environment and Heritage, Canberra. Fisher A, Mahoney T, Mackay L, Tynan C, Dostine P, Young S, Fegan M (2011) ‘Assessment of the terrestrial vertebrate fauna of the Weddell area’. Northern Territory Department of Environment, Recreation and Tourism and Sport, Palmerston. Franklin DC (1999) Evidence of disarray amongst granivorous bird assemblages in the savannas of northern Australia, a region of sparse human settlement. Biological Conservation 90, 53–68. Garnett ST, Woinarski JCZ, Crowley CM, Kutt AS (2010) Biodiversity conservation in Australian tropical Rangelands. In Wild Rangelands:  Conserving Wildlife while Maintaining Livestock in Semi-Arid Ecosystems. (Eds JT du Toit, R Kock, and J Deutsch) pp. 191–234. John Wiley & Sons, Chichester, UK. Gillespie GR, Hero J-M (1999) The impact of introduced fish upon Australian frogs. In Declines and Disappearances of Australian Frogs. (Ed. A Campbell) pp. 131–144. Environment Australia, Canberra. Gillespie GR, Scroggie MP, Roberts D, Cogger H, McDonald KR, Mahony MJ (2011) The influence of uncertainty on conservation assessments: Australian frogs as a case study. Biological Conservation 144, 1516–1525. doi:10.1016/j.biocon. 2010.10.031 Griffiths AD, McKay JL (2007) Cane toads reduce the abundance and site occupancy of Merten’s water monitor (Varanus mertensi). Wildlife Research 34, 609–615. Hero J-M, Morrison C (2004) Frog declines in Australia: global implications. The Herpetological Journal 14, 175–186. Hero J-M, Williams SE, Magnusson WE (2005) Ecological characteristics of declining amphibians: are they more sus-

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ceptible to extinction? Journal of Zoology 267, 221–232. doi:10.1017/S0952836905007296 Hughes L (2003) Climate change and Australia: trends, projections and impacts. Austral Ecology 28, 423–443. doi:10.1046/ j.1442-9993.2003.01300.x IUCN (2012) IUCN Red List Categories and Criteria: Version 3.1. Second Edition. IUCN, Gland, Switzerland and Cambridge, UK. Jansen A, Healey M (2003) Frog communities and wetland condition: relationships with grazing by domestic livestock along an Australian floodplain river. Biological Conservation 109, 207–219. doi:10.1016/S0006-3207(02)00148-9 McBride JL, Keenan TD (1982) Climatology of tropical cyclone genesis in the Australian region. International Journal of Climatology 2, 13–33. doi:10.1002/joc.3370020103 Northern Territory Environment Protection Authority (2015) ‘Environmental quality report. Biodiversity of the Howard Sand Plains Site of Conservation Significance’. Version 3.0. Northern Territory Environmental Protection Authority, Darwin. Office of the Environment and Heritage New South Wales (2012) National Recovery Plan for the Southern Corroboree Frog, Pseudophryne corroboree, and the Northern Corroboree Frog, Pseudophryne pengilleyi. Office of Environment and Heritage (New South Wales), Sydney. Price O, Milne D, Tynan C (2005) Poor recovery of woody vegetation on sand and gravel mines in the Darwin region of the Northern Territory. Ecological Management & Restoration 6, 118–123. doi:10.1111/j.1442-8903.2005.00228.x Purvis A, Gittleman JL, Cowlishaw G, Mace GM (2000) Predicting extinction risk in declining species. Proceedings. Biological Sciences 267, 1947–1952. doi:10.1098/rspb.2000.1234 Pusey B, Cook B, Georges A (2011) Amphibians and reptiles. In Aquatic Biodiversity in Northern Australia: Patterns, Threats and Future. (Ed. BJ Pusey) pp. 93–109. Charles Darwin University Press, Darwin. Ramli A, Jaafar H (2016) Peak finding algorithm to improve syllable segmentation for noisy bioacoustic sound signal. Procedia Computer Science 96, 100–109. doi:10.1016/j. procs.2016.08.105 Retallick RW, Miera V (2007) Strain differences in the amphibian chytrid Batrachochytrium dendrobatidis and non-permanent, sub-lethal effects of infection. Diseases of Aquatic Organisms 75, 201–207. doi:10.3354/dao075201 Roberts JD, Conroy S, Williams K (1999) Conservation status of frogs in Western Australia. In Declines and Disappearances of Australian Frogs. (Ed. A Campbell) pp. 177–184. Environment Australia, Canberra. Russell-Smith J, Ryan PG, Klessa D, Waight G, Harwood R (1998) Fire regimes, fire-sensitive vegetation, and fire management of the sandstone Arnhem Plateau, monsoonal northern Australia. Journal of Applied Ecology 35, 829–846.

Skerratt LF, Berger L, Speare R, Cashins S, McDonald KR, Phillott AD, et al. (2007) Spread of chytridiomycosis has caused the rapid global decline and extinction of frogs. EcoHealth 4, 125–134. doi:10.1007/s10393-007-0093-5 Tyler MJ, Davies M, Martin AA (1981) New and rediscovered species of frogs from the Derby-Broome area of Western Australia. Records of the Western Australian Museum 9, 147–172. Walsh KJE, Ryan BF (2000) Tropical cyclone intensity increase near Australia as a result of climate change. Journal of Climate 13, 3029–3036. doi:10.1175/1520-0442(2000)013< 3029:TCIINA>2.0.CO;2 Wardell-Johnson G, Roberts JD, (1991) The survival status of the Geocrinia rosea (Anura: Myobatrachidae) complex in riparian corridors: biogeographical implications. In Nature Conservation 2: The Role of Corridors. (Eds DA Saunders and RJ Hobbs) pp. 167–175. Surrey Beatty and Sons, Sydney. Westgate MJ, Driscoll DA, Lindenmayer DB (2012) Limited influence of stream networks on the terrestrial movements of three wetland-dependent frog species. Biological Conservation 153, 169–176. doi:10.1016/j.biocon.2012.04.030 Williams RJ, Bradstock RA, Cary GJ, Enright NJ, Gill AM, Liedloff AC, et al. (2009) ‘Interactions between climate change, fire and biodiversity in Australia – a preliminary assessment’. Report to the Department of Climate Change and Department of Environment, Water, Heritage and the Arts, Canberra. Woinarski J, Pavey C, Kerrigan R, Cowie I, Ward S (Eds) (2007) Lost from Our Landscape: Threatened Species of the Northern Territory. Northern Territory Government Department of Natural Resources, Environment and the Arts, Palmerston. Woinarski JCZ, Armstrong M, Brennan K, Fisher A, Griffiths AD, Hill B, et al. (2010) Monitoring indicates rapid and severe decline of native small mammals in Kakadu National Park, northern Australia. Wildlife Research 37, 116–126. doi:10.1071/WR09125 Woinarski JCZ, Fisher A, Armstrong M, Brennan K, Griffiths AD, Hill B, et al. (2012) Monitoring indicates greater resilience for birds than for mammals in Kakadu National Park, northern Australia. Wildlife Research 39, 397–407. doi:10.1071/WR11213 Woodhams DC, Alford RA, Marantelli G (2003) Emerging disease of amphibians cured by elevated body temperature. Diseases of Aquatic Organisms 55, 65–67. doi:10.3354/ dao055065 Ziembicki M, Woinarski JCZ, Webb J, Vanderduys E, Tuft K, Smith J, et al. (2015) Stemming the tide: progress towards resolving the causes of decline and implementing management responses for the disappearing mammal fauna of northern Australia. THERYA 6, 169–226. doi:10.12933/ therya-15-236

5

An update on frog declines from the forests of subtropical eastern Australia David Newell

INTRODUCTION The forests of subtropical eastern Australia are some of the most biologically diverse ecosystems in Australia. These include a variety of forest types from littoral to cool temperate rainforests, as well as eucalypt-dominated sclerophyll forests and woodlands and the lowland swamp forests adjoining the wallum heathlands. In combination, these forests provide habitat for about 50 native species of frogs of which close to half are endemic to the region. Within the region, rainforests are particularly important with some 370  000  ha listed as World Heritage. These rainforests are second only to the Wet Tropics in terms of the diversity of frogs (Hines 2008). Some of the earliest documented declines and disappearances of amphibians occurred in subtropical eastern Australia, with the loss of the southern gastric brooding frog (Rheobatrachus silus) and the southern day frog (Taudactylus diurnus) in the late 1970s (Ingram and McDonald 1993; Laurance et al. 1996; Hines et al. 1999). As such, the region has been an important focus of research on the global phenomena of declining frogs. Nearly four decades have passed since the first declines were noted, so it is timely that a review of the conservation status of frogs from these forests be undertaken. For the purposes of this chapter, the region stretches from Gladstone in Queensland, to the Hunter River in New South Wales (NSW) (Plate 5.1). This area is defined

as the South East Queensland (SEQ) and New South Wales North Coast (NSWNC) bioregions in the Interim Biogeographic Regionalisation for Australia (IBRA Version 7). Overall, the SEQ and NSWNC bioregions have a highly diverse frog fauna with over one-quarter (64) of all Australian species likely to occur there (Anstis 2013). This concentration is in part because of the combination of temperate and tropical influences, as well as the range of elevations and diversity of habitats (not all of these frogs occur within forests). In the north, there are tropical species at the southern limits of their distribution; in the south, temperate species are at their northern limits. The region also has a high number of endemic species, particularly concentrated in the rainforests and wet sclerophyll forests of northern NSW and south-eastern Queensland (Hines 2008; Mahony 2010). Twenty-four species within the two bioregions are listed as being of conservation concern under State and/ or federal legislation (Table 5.1) and form the basis of the present discussion. The four threatened species from the coastal wallum habitats (Crinia tinnula, Litoria cooloolensis, L. freycineti, and L.  olongburensis) have been excluded because they do not predominantly occur in forests (see Chapter 7; Newell and Goldingay 2004), as well as four species from the New England escarpment and foothills (Litoria booroolongensis, L. subglandulosa,

30

Status of Conservation and Decline of Amphibians

Table 5.1.  Species of conservation concern within the South Eastern Queensland (SEQ) and New South Wales North Coast (NSWNC) according to Queensland (Qld; Nature Conservation (Wildlife) Regulation 2006), New South Wales (NSW; Threatened Species Conservation Act 1995), Commonwealth (Environment Protection and Biodiversity Conservation Act 1999) and global (IUCN Red List) threatened species listings. CR = Critically Endangered, EX = Extinct, EN = Endangered, EP = Endangered Population, VU = Vulnerable, NT= Near Threatened, LC = Least Concern. Dashes indicate that the species is not listed under that legislation and an asterisk indicates the species occurs in the bioregion but is not listed.

Species

Qld

Adelotus brevis Assa darlingtoni

Endemic to either bioregion

NSW

Commonwealth

IUCN Red List

VU

EP

–

NT

No

*

VU

–

LC

Yes

VU

VU

–

VU

Yes

Mixophyes balbus

–

EN

VU

VU

No

Mixophyes fleayi

EN

EN

EN

EN

Yes

Mixophyes iteratus

EN

EN

EN

EN

Yes

Philoria kundagungan

VU

EN

–

EN

Yes

Philoria loveridgei

*

EN

–

EN

Yes

Philoria pughi

–

EN

–

EN

Yes

Philoria richmondensis

–

EN

–

EN

Yes

Philoria sphagnicolus

–

VU

–

EN

Yes

Rheobatrachus silus

EX

–

EX

EX

Yes

Taudactylus diurnus

EX

–

EX

EX

Yes

Taudactylus pleione

EN

–

CR

CR

Yes

Crinia tinnula

Litoria aurea

–

EN

VU

VU

No

Litoria brevipalmata

*

VU

–

EN

Yes

Litoria booroolongensis

–

EN

EN

CR

No

Litoria cooloolensis

NT

–

–

EN

Yes

Litoria daviesae

–

VU

–

VU

No

Litoria freycineti

VU

*

–

VU

No

Litoria kroombitensis

EN

–

–

–

Yes

Litoria olongburensis

VU

VU

VU

VU

Yes

–

CR

VU

CR

No

Litoria piperata Litoria pearsoniana

VU

*

–

NT

Yes

Litoria subglandulosa

VU

V

–

VU

No

L. daviesae, Mixophyes balbus). These four may also occur in the NSW North Coast Bioregion, but have the bulk of their distribution within the New England tablelands (see Chapter 6) (Heatwole et al. 1995). The green and golden bell frog (Litoria aurea) also occurs in coastal habitats in northern NSW (Goldingay and Newell 2005; Goldingay et al. 2017) but most remaining populations occur south of the Hunter River (see Chapters 6 and 7; White and Pyke 2008). This review focuses on threatened species that occur within forests and is divided based upon biogeographical affinities.

BACKGROUND TO FROG DECLINES IN THE SUBTROPICS The sudden disappearance of the southern day frog (Taudactylus diurnus) and the southern gastric brooding frog (Rheobatrachus silus) from south-eastern Queensland in the late 1970s marked the start of a period of increased interest in the Australian frog fauna. Biologists began to examine frog populations in a variety of habitats across the eastern coast (Osborne 1989; Mahony 1993; Richards et al. 1994; Hollis 1995; Gillespie and Hollis 1996) but, before the early 1990s, frogs in the subtropics had received

5 – An update on frog declines from the forests of subtropical eastern Australia

scant attention in terms of monitoring. Without baseline data, it was hard to know which species were in decline or stable and therefore it was difficult to convince scientists, policy makers, and the general public that the declines were real. Indeed, it was not until 1991 that amphibians were protected in NSW by the Endangered Fauna (Interim Protection) Act 1991 (Lunney and Ayers 1993). With the benefit of hindsight, the time lost was crucial; however, debate about the extent and cause of declines continued well into the late 1990s (Campbell 1999), even after the identification of a likely cause. Murray et al. (2010) suggest that 1978 marked the year that the highly virulent amphibian chytrid fungus (Batrachochytrium dendrobatidis) arrived on Australian shores, somewhere near Brisbane. The disease chytridiomycosis, caused by infection with B. dendrobatidis (Berger et al. 1998; Longcore et al. 1999), has decimated amphibians globally in what has been described as ‘the most spectacular loss of vertebrate biodiversity due to disease in recorded history’ (Skerratt et al. 2007). Batrachochytrium dendrobatidis appears to have spread both north and south from the initial incursion near Brisbane; as such, the frog fauna of subtropical eastern Australia has likely been exposed to the impact of this disease longer than any other region in the country, and an examination of the population level responses is of interest.

Recovery Team 2002). This species was last seen in the wild in January 1979 on the Blackall-Conondale Ranges, where it was sympatric with R. silus, a species that also declined sharply that year (Czechura and Ingram 1990) and was last seen in the wild in 1981 (Richards et al. 1994). Despite targeted surveys within known habitats (Czechura and Ingram 1990; Ingram and McDonald 1993; Hines et al. 1999; Hines and the South-east Queensland Threatened Frogs Recovery Team 2002), no individuals of either species have been located subsequently. The timing and sudden nature of these disappearances suggest that these species were decimated by B. dendrobatidis (Scheele et al. 2017). The earliest known date for B. dendrobatidis in Australia is from a museum specimen of a frog collected in 1978 near Brisbane (Scheele et al. 2017). Close to 40 years later, the likelihood that either T. diurnus or R. silus will ever be seen again is slim, but continued targeted surveys should be undertaken (Skerratt et al. 2007, 2016). The rediscovery of the armoured mist frog (Litoria lorica) – a species thought extinct from the Wet Tropics – highlights the importance of targeted surveys and the need for searches in marginal habitats (Puschendorf et al. 2011). In addition, there is now strong evidence that some species appear to have recovered from a period of decline, despite the presence of B. dendrobatidis (Newell et al. 2013; Scheele et al. 2015).

THE FROGS ASSOCIATED WITH STREAMS

The barred river frogs (Mixophyes spp.)

Association with upland stream environments, habitat specialisation, and small clutch sizes are prominent ecological traits among the declining frogs of eastern Australia (Mahony 1996a; Williams and Hero 1998; Hero and Morrison 2004). In the NSWNC and SEQ Bioregions, 17 threatened species are associated with streams. A number of these species appear to have recovered from a period of population decline, whereas others remain missing or vastly reduced in numbers.

Fleay’s barred frog (Mixophyes fleayi) and the giant barred frog (M. iteratus) are large, obligate, streambreeding frogs (Knowles et al. 2015) that declined sometime in the 1980s. It is difficult to say how abundant they were before the 1990s, because there are few published data (for M. iteratus see Mahony 1993; Ingram and McDonald 1993) and M. fleayi was only formerly described in 1987 (Corben and Ingram 1987), but anecdotal reports suggest that they were commonly encountered along streams (M. Mahony pers. comm.). Surveys in forests during the 1990s in the northern NSW and southeastern Queensland (Mahony 1993; NSW NPWS 1994; Hines et al. 1999; Goldingay et al. 1999) either failed to detect them at previously known locations or demonstrated that these species occurred patchily and in low abundance. Laurance et al. (1996) suggested that these two species had declined by up to 90% in the region. Hines et al. (1999) reviewed available data for these species and recommended that both be listed nationally as

Declined and recovered

Missing and probably extinct Taudactylus diurnus and Rheobatrachus silus are both narrowly distributed endemic species from the rainforests of south-eastern Queensland that remain missing and are likely to be extinct. Both species were associated with streams in rainforest. Taudactylus diurnus was known from a small range in elevation (350–800  m) within the Blackall, Conondale, and D’Aguilar Ranges near Brisbane (Hines and the South-east Queensland Threatened Frogs

31

32

Status of Conservation and Decline of Amphibians

Endangered because of their rarity, restricted distribution, and the (limited) evidence of decline. Newell et al. (2013) conducted intensive capture– mark–recapture (CMR) studies on M. fleayi at two separate locations in northern NSW and demonstrated a recovery in abundance, despite the presence of B. dendrobatidis. Quick et al. (2015) showed that the population at high elevations in the Border Ranges in NSW has remained stable. While this is encouraging and appears also to have occurred at other locations (H. Hines and M. Mahony pers. comm.), the species remains absent from some historic locations, or occurs at very low abundance. For M. iteratus, there has been an increased number of populations discovered over the past decade, particularly associated with the upgrade of the Pacific Highway in northern NSW. There is reason to suggest that this is indicative of a recovery rather than merely a lack of previous effort to survey. Mixophyes iteratus is a large (up to 110  mm in body size) and often vocal species that is unlikely to be overlooked during surveys (Mahony 1993). Even when males do not vocalise, they can be detected readily via eye-shine. Males do not move far from the stream and are active when temperatures are above 18oC (Lemckert and Brassil 2000; Koch and Hero 2007). This species was known historically from Terania Creek in Nightcap National Park, northern NSW (Smith et al. 1989), a location that has been intensively surveyed since the mid-1990s (Goldingay et al. 1999; Newell unpublished). Despite nearly annual visits, Mixophyes iteratus was not detected at this site until January 2017 when a large gravid female was discovered. This is one of only a few known sites that now supports the three local species of Mixophyes (M. fleayi and M. fasciolatus are sympatric). Hines (2008) also reported recolonisation at several upland streams in the Conondale Ranges from which this frog supposedly had vanished (Hines et al. 1999). The Litoria citropa species group This group of small to medium-sized treefrogs are streambreeding species occurring within the wet forests of south-eastern Australia that have been subject to genetic investigations (McGuigan et al. 1998; Donnellan et al. 1999) and recent taxonomic revisions (Mahony et al. 2001; Hoskin et al. 2013). The L. citropa group consists of two subgroups: namely the three medium-sized treefrogs (the Blue Mountains tree frog Litoria citropa, the New England tree frog L. subglandulosa, and Davies’ tree frog L. daviesae) and the smaller treefrogs in the L. phyllochroa subgroup

(Tyler and Davies 1985), which has been the subject of considerable confusion regarding nomenclature and taxonomy. The genetic analysis by Donnellan et al. (1999) revealed three distinct lineages, two of which were assigned to the names L. nudidigitus and L. phyllochroa, and a third that was recognised as an unresolved species of multiple highly divergent groups. Two of the lineages within the third group conformed to the overall distribution of the mountain stream tree frog (L. barringtonensis) and the cascade tree frog (L. pearsoniana) and another from Kroombit Tops was recently described as the Kroombit tree frog (L. kroombitensis) (Hoskin et al. 2013). The specimens examined by Donnellan et al. (1999) came from the general locality as the peppered tree frog L. piperata and was morphologically similar to it, but conformed to L. pearsoniana, providing further support to the assertion that this species is not distinct (Gillespie and Hines 1999). The validity of L. piperata as a species is likely to remain unresolved in the absence of genetic material from the type locality; targeted searches at the type locality have not located any additional individuals. Three of the species from this group are considered to have the core of their distribution within the SEQ and NSWNC bioregions, namely L. barringtonensis, L. kroombitensis, and L. pearsoniana. Litoria phyllochroa occurs from the Sydney region northward to about Coffs Harbour, and L. barringtonensis occurs northward from the Hunter River to approximately the Gibraltar Range (Gillespie and Hines 1999) and neither species is thought to have declined. Two other species (L. subglandulosa and L. daviesae) also occur on the western side of the NSWNC bioregion, but are predominantly known from the eastern drainages of the New England tablelands (Mahony et al. 2001). Litoria pearsoniana currently is listed as Vulnerable in Queensland (Hines and the South-east Queensland Threatened Frogs Recovery Team 2002) and was reported to have declined from the Conondale Ranges (McDonald and Davies 1990) and other localities in south-eastern Queensland (Ingram and McDonald 1993). Laurance et al. (1996) suggested that this species (along with Mixophyes fleayi and M. iteratus) had declined by up to 90% in south-eastern Queensland and northern NSW; however, Goldingay et al. (1999) and Hines et al. (1999) both reported the species to be locally abundant. Continued monitoring in the region (Newell unpublished) supports this conclusion. This species appears to have now recovered (Hines 2008) and it is likely that previous declines were due to the arrival and subsequent impact of

5 – An update on frog declines from the forests of subtropical eastern Australia

B. dendrobatidis (Scheele et al. 2017). It would seem that most populations of L. pearsoniana were large enough to withstand the initial impacts of B. dendrobatidis, but however, this may not hold true for small, isolated populations or for species that are restricted in range, such as the recently described sister taxon, L. kroombitensis.

THE ENDEMICS WITH NARROW RANGES There are a number of species within the two bioregions that have extremely restricted distributions and are referred to here as the narrow-range endemics. In the far northern section of the SEQ bioregion, Kroombit Tops provides an outstanding example of this (Hines 2014) and, farther south, the Gondwanan rainforest reserves are unique examples. These areas acted as refugia for rainforest species during cooling and drying events of the Pliocene/Pleistocene and provide relictual links to our Gondwanan rainforest fauna (Mahony 2010). Hero and Morrison (2004) noted that 77.5% of Australia’s threatened species are restricted in range. Kroombit Tops Populations of L. kroombitensis occur in the headwaters of just five streams within Kroombit Tops National Park and have an extent of occurrence of 32 km2 (Hines 2014). The species is recognised as Endangered within Queensland because of its limited distribution and evidence of declines. Hoskin et al. (2013) reported ongoing declines in this species since the mid-1990s and noted that moribund and dead individuals have been found and subsequently diagnosed with chytridiomycosis. Concurrently, the only population of Taudactylus pleione that was sympatric with L. kroombitensis disappeared. Taudactylus pleione is listed as Critically Endangered (Environment Protection and Biodiversity Conservation Act 1999) being known only from 12 discrete patches within Kroombit Tops National Park (20 males, a value of 30 for maximum and 25 for the median estimates was assumed.

Number of calling males

1995–1999

2000–2004

2005–2009

0

17

29

42

20

14

3

9

485

276

486

Median

663

555

698

Maximum

854

762

918

Estimate of the population of males Minimum

there is a growing risk of damage to the habitat caused by feral pigs across south-western Australia, where the distribution of pigs has been expanded by human-assisted dispersal (Spencer and Hampton 2005). White-bellied frog (Geocrinia alba) The white-bellied frog (Geocrinia alba) as of April 2017 was listed at the State level as Critically Endangered but federally as Vulnerable against the criteria for status set out in the EPBC Act. The difference between these listings critically depends on an overview of the patterns of decline and the timing of state and national reviews. The Recovery Plan of 2014 clearly supports a pattern of ongoing decline and loss of local, mostly very small (20 calling males) populations. Calling males are an adequate metric of population size for adults because the sex ratio in this species is 1:1, based on the ratio of calling males to number of egg masses deposited (Driscoll 1999a) and assuming females produce one clutch of eggs per year. Within the estimated, pre-European geographic range, declines in G. alba are associated with a long history of: (1) intensive logging at the Leeuwin-Naturalist Ridge, commencing in the 1850s and largely ending in the late 19th century (see http://www.amrshire.wa.gov.au/region/ local-history), and (2) the clearing of land, initiated in the 1920s but radically accelerated in the 1970s (Department of Parks and Wildlife 2014). The clearing of vegetation commonly changed broad, flat, heavily vegetated drainages into more incised channels in open terrain. As well

as clearing, there were associated changes in land use that impacted sites where Geocrinia alba occurred: such as heavy usage of water by blue-gum plantations adjacent to swamps inhabited by G. alba, particularly in the early stages of tree growth, which was associated with loss of populations in adjacent swamps, and, new impoundments of water for irrigation of vineyards have flooded some known populations. Populations of G. alba are intensively monitored on a ‘subpopulation’ basis with populations and subpopulations being defined pragmatically (see Appendix 8.1) in relation to features of the landscape and the use of adjacent land (and consequent, potential risks). Plate 8.4, drawn from data in Figure 3 of Department of Parks and Wildlife (2014), shows a decline in the discovery of subpopulations, and, the simultaneous, steady loss of subpopulations over the period from 2000 to 2012. Interpolating the data from Figure 4 of Department of Parks and Wildlife (2014) using three metrics – minimum, median, and maximum sizes of populations – Table 8.4 shows variation in the population size for adult males of G. alba during three 5-year periods: 1995–1999, 2000– 2004, and 2005–2009. Assuming a 1:1 sex ratio (justified by Driscoll 1996), the total adult population would be twice these estimates. This species is not in freefall but there is an ongoing pattern of loss demonstrated by declines in number of sites occupied, but less convincingly by estimated population size. Currently, direct management actions are limited. There are ongoing surveys, and a program of field-collection of egg masses, captive rearing of eggs, then rearing

83

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Status of Conservation and Decline of Amphibians

hatchling frogs to age 12 months and releasing the subadult frogs into the field. Those efforts have been hampered by crops of illegal drugs planted at some release sites and the associated use of fertilisers to promote growth of cannabis plants (Department of Parks and Wildlife 2014; Kim Williams pers. comm.). The purchase of a large area of uncleared, but heavily logged, land on the north-western bend of the Blackwood River, announced in 2000, contains some of the larger populations of this species. This purchase is now incorporated into managed forest and conservation estates (Forest Grove National Park, Blackwood River National Park, Leeuwin Naturaliste National Park, and intervening State Forest) with only one small, cleared gap on the western side of the Bussell Highway. The status of Geocrinia alba under the EPBC Act is under current review and may be changed to Critically Endangered. Orange-bellied frog (Geocrinia vitellina) At the time of writing, the orange-bellied frog Geocrinia vitellina was listed as Vulnerable both under Western Australian state legislation and the EPBC Act. Geocrinia vitellina has a small geographic range, ∼8  km2 , with an estimated actual area of occurrence (measured as area used by breeding frogs) of 0.08  km2 (Department of Parks and Wildlife 2014). This distribution is centred on Spearwood Creek, with isolated occurrences at several sites on five other small creeks draining into the northern side of the Blackwood River adjacent to Spearwood Creek. Egg masses were introduced into Adelaide Creek, east of Spearwood Creek (Department of Parks and Wildlife 2014) and resulted in low numbers (two to four) of calling males in 2009 but with no calling males reported since then. Integrating data from the current Recovery Plan indicates a population size of at least 400 frogs, assuming a 1:1 sex ratio (cf. Driscoll 1999a). This estimate is based on monitored subpopulations in Figure 7 of that plan, a subset of the known total populations/subpopulations (see Appendix 8.1 for definition of populations and subpopulations), using a population size of three for sites with 20 males. Population size was estimated at