Saving the Tasmanian Devil: Recovery through Science-based Management

By Samantha Fox and David Pemberton

The Tasmanian devil is threatened by Devil Facial Tumour Disease (DFTD), a transmissible form of cancer that has reduced the population by over 80%. Persecution, extreme climate events, vehicle collision and habitat destruction also put pressure on this endangered species. The recovery effort to save the Tasmanian devil commenced over 15 years ago as a collaborative initiative between the Tasmanian government, the Australian government, the Zoo and Aquarium Association Australasia, and many research institutions.

Saving the Tasmanian Devil documents the journey taken by partner organisations in discovering what DFTD is, the effect it has on wild devil populations, and the outcomes achieved through research and management actions. Chapters describe all aspects of devil conservation, including the captive devil populations, applied pathology, immunology and genetic research findings, adaptive management, and the importance of advocacy and partnerships. This book will provide management practitioners and conservation scientists with insight into the complexities of undertaking a program of this scale, and will also be of value to researchers, students and others interested in conservation.

Certificate of Commendation, The Royal Zoological Society of NSW 2020 Whitley Awards: Science & Conservation

• Language: English
• Publisher: CSIRO PUBLISHING
• Release date: Aug 1, 2019
• ISBN: 9781486307203

Book preview

SAVING THE

TASMANIAN DEVIL

This book is dedicated to all the people (past and present) involved with the conservation of the

Tasmanian devil, and their families/partners/significant others/fur-babies,

who stand behind and support them.

SAVING THE

TASMANIAN DEVIL

RECOVERY THROUGH SCIENCE-BASED MANAGEMENT

EDITORS:

CAROLYN J. HOGG, SAMANTHA FOX, DAVID PEMBERTON AND KATHERINE BELOV

© Department of Primary Industries, Parks, Water and the Environment, Dr Carolyn Hogg and Professor Katherine Belov 2019

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.

The authors and editors each assert their moral rights, including the right to be identified as the author or editor.

A catalogue record for this book is available from the National Library of Australia.

ISBN: 9781486307180 (pbk.)

ISBN: 9781486307197 (epdf)

ISBN: 9781486307203 (epub)

Published by:

CSIRO Publishing

Locked Bag 10

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Website: www.publish.csiro.au

Front cover: Tasmanian devil standing on a fallen tree (photo: Heath Holden)

Back cover: (top to bottom) Devil with DFT1 (photo: DPIPWE); advocacy devil (photo: Zoos Victoria); adult female devil (right) with dependent young at maternity den entrance (photo: William E. Brown)

Set in 10.5/14 Palatino and Optima

Edited by Adrienne de Kretser, Righting Writing

Cover design by James Kelly

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Index by Max McMaster

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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.

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CONTENTS

Foreword

About the editors

Contributing authors

1Carnivore conservation: the importance of carnivores to the ecosystem, and the value of reintroductions

Chris R. Dickman, Aaron C. Greenville and Thomas M. Newsome

2The Tasmanian devil: a uniquely threatened animal

David Pemberton

3Pathology and diagnostics of DFTD and other devil diseases

Judy Clarke, Sarah Peck, Colette Harmsen and Graeme Knowles

4Revealing the origin and evolutionary trajectory of DFTD using genetics and genomics

Belinda Wright, Beata Ujvari, Janine Deakin, Elizabeth P. Murchison and Katherine Belov

5Tasmanian devil immune genes and their function

Yuanyuan Cheng and Katrina Morris

6Genetic tools: maintaining genetic diversity in the Tasmanian devil metapopulation

Catherine E. Grueber and Elspeth A. McLennan

7Microbiomes, pouches and milk: natural solutions?

Emma Peel and Rowena Chong

8Immune strategies to combat DFTD

A. Bruce Lyons and Gregory M. Woods

9Devils and disease in the landscape: the impact of disease on devils in the wild and on the Tasmanian ecosystem

Menna E. Jones, Rodrigo K. Hamede, Tracey Hollings and Hamish I. McCallum

10 Conservation status drives management: what is happening in wild populations and why?

Billie T. Lazenby, Nicholas J. Mooney, Clare E. Hawkins, Greg J. Hocking and Samantha Fox

Colour plates

11 DFTD is a killer but what about other threats?

Clare Lawrence and Holly F. Wiersma

12 Remote detection and monitoring methods for Tasmanian Devils

William E. Brown and Jodie Elmer

13 Wild devil recovery: managing devils in the presence of disease

Samantha Fox and Philip J. Seddon

14 Use of scent ecology to improve reintroduction outcomes: applications for Tasmanian devils

Debra M. Shier, Elizabeth Reid-Wainscoat and Ronald R. Swaisgood

15 A One Plan Approach to saving the devil: population and habitat viability assessment

Caroline M. Lees, Paul Andrew, Rebecca Spindler, Richard Jakob-Hoff, Kathy Traylor-Holzer and Onnie Byers

16 Managing a metapopulation: intensive to wild and all the places in between

Carolyn J. Hogg, Andrew V. Lee and Chris J. Hibbard

17 Advocates and ambassadors: the devil is real

James R. Biggs, Amanda Embury, Chris J. Hibbard, Camille Goldstone-Henry and Carolyn J. Hogg

18 Managing and maintaining wild temperament and behaviours in captivity

Stephen Izzard, Olivia Barnard and David Schaap

19 Conservation introduction of Tasmanian devils to Maria Island: a managed response to DFTD

Phil Wise, Sarah Peck, Judy Clarke and Carolyn J. Hogg

20 The depopulation and reintroduction of devils on the Forestier Peninsula

Stewart J. Huxtable and William E. Brown

21 Captive research: working together for the common good

Marissa L. Parrott, Emily Dowling, Tim Faulkner, Channing Hughes, Tamara Keeley, Androo Kelly, Kimberly A. Miller, Beth Pohl, Justine K. O’Brien and Carolyn J. Hogg

22 The road to recovery: a recipe for success?

Samantha Fox, Howel Williams, Billie T. Lazenby, Nicholas J. Mooney, Peter Latch, Andrew Sharman, Chris Hibbard, Jane McGee and David Pemberton

23 Balancing the needs of government, academia, zoos, the community and media in the messaging to Save the Tasmanian Devil

Michelle Nichols, Nadeen Burge and Warwick Brennan

24 Lessons learned and future directions

Carolyn J. Hogg, Samantha Fox, David Pemberton and Katherine Belov

Appendix 1. STDP Standard Operating Procedure: Tasmanian devil anaesthetics

Appendix 2. SOP: Blood collection from Tasmanian devils

Appendix 3. SOP: Blood collection from the peripheral ear vein in Tasmanian devils

Appendix 4. SOP: Live-trapping and handling wild Tasmanian mammals

Appendix 5. SOP: Tasmanian devil fieldwork biosecurity

Acronyms

Index

FOREWORD

The Tasmanian Government Gazette No. 21518, dated Monday 25 May 2015, states: ‘I, Professor the Honourable Kate Warner, Member of the Order of Australia, Governor in and over the State of Tasmania and its Dependencies in the Commonwealth of Australia, in exercise of the Royal Prerogative, and acting with the advice of the Executive Council, do by this my Proclamation, declare that the animal Sarcophilus harrisii (Boitard, 1841) known as the Tasmanian Devil be adopted as the Animal Emblem of the State of Tasmania. Given under my hand and the Seal of the State of Tasmania.’

While it may seem surprising that the island’s world-famous endemic marsupial carnivore lacked such recognition until recently, the proclamation was timely given the perilous future of the animal through the devastation caused to the wild population by DFTD, devil facial tumour disease.

As Governor, I felt particularly honoured to be associated with that proclamation, which transcends mere symbolism because the Tasmanian devil has endured and managed to survive a remarkably tough evolutionary story: mainland Australian extinction; bycatch to thylacine killing and arsenic and strychnine poisoning of rabbits; indiscriminate slaughter as a supposed threat to livestock; and from approximately 1996 the onslaught of DFTD.

Saving the Tasmanian Devil: Recovery through Science-based Management is a critically important new publication in respect of the Tasmanian devil, wildlife conservation more broadly and understanding of the fragility and complexity of our precious global environment. The Save the Tasmanian Devil Program (STDP) was established to conserve the species in the wild and understand more about the aetiology of the disease. This book provides the definitive history of the STDP, the disease, the captive breeding program and wild monitoring.

Over the past 15 years the STDP has made significant advances in understanding the biology of devils and DFTD. The many professional and volunteer personnel involved have undertaken extensive wild monitoring to better understand impacts of the disease on Tasmania’s ecosystem. An insurance metapopulation, built up necessarily through trial and error and now well-established, assists the Wild Devil Recovery project for the long-term maintenance of sustainable populations of devils in the presence of disease in the wild.

The STDP’s hard work and achievements have benefited significantly from bipartisan state and federal government funding and other support. Furthermore, international focus on the rare disease has helped galvanise on-the-ground efforts to save the Tasmanian devil from extinction. Yet great risks remain to be countered. Devils in the wild need to survive in the presence of the disease, and the species remains at risk from numerous additional threats including roadkill and loss of genetic diversity within small, fragmented populations.

Saving the Tasmanian Devil: Recovery through Science-based Management expertly describes and investigates the Tasmanian devil in ways that surpass analyses of virtually any other species in a single book: as remnant top-order carnivore; as host of as-yet incurable DFTD cancers; via genomic and genetic sequencing; through adaptive management and recovery techniques; potential natural solutions, vaccines and immunotherapies; long-term monitoring; the IUCN One Plan Approach; and more. As such, the book records a most important development in the international approach to and understanding of the natural world. Thus, in tragedy there is hope, that the existence of the Tasmanian devil is not over and that the lessons of DFTD will ensure this animal’s survival and be a case study for future imperiled species.

One of the great pleasures during my term as Governor has been gaining an understanding of this very special marsupial carnivore and its plight. A few months after the proclamation declaring the Tasmanian devil to be the state’s animal emblem, I met many of the scientists and volunteers associated with the STDP at a reception in their honour at Government House, which further stimulated my interest. Since that time I have been privileged to have been on two field trips with Dr David Pemberton and his staff.

The first trip was to wukalina/Mount William, a release site for Tasmanian devils bred on Maria Island. As well as watching the examination and checking of a recaptured devil, we had a briefing about the promising virtual fence program which is an aspect of the roadkill mitigation strategy. We were also shown a Tasmanian devil latrine and a maternal den, with an explanation of the rather intriguing mating habits of the devil!

The second trip was in May 2018 when my husband Dick and I were again invited by Dr David Pemberton and colleagues to undertake a field trip with the STDP, this time to country between Glenora and Fentonbury in the Derwent Valley. This trip involved accompanying David and his colleagues, Dr Sam Fox and Dr Billie Lazenby (all of whom have contributed to this publication), while Billie checked devil traps that had been set the night before. We were fortunate to see three healthy young devils being examined and released. To witness the response of the wild-bred devils to expert and gentle handling, to see them passively accepting being stroked, microchipped and sampled and then personally holding the devil and releasing it, was an experience I will never forget.

It was a great privilege to watch experts at work with this species – experts working across Australia and internationally in the one cause. In many ways this book is their story, as much as it is the story of the unique Tasmanian devil.

Her Excellency Professor the Honourable Kate Warner AC

Governor of Tasmania

ABOUT THE EDITORS

Carolyn J. Hogg is the Research Manager of the Australasian Wildlife Genomics Group at the University of Sydney. She has been working on the conservation of threatened species for over 20 years both in Australia and overseas. Working closely with academic and conservation management partners, she is developing better tools and technologies to integrate molecular genetics into real-time conservation management decisions.

Samantha Fox is a wildlife biologist with a focus on the conservation of threatened species. She is passionate about incorporating results from applied research into management decisions and has a strong collaborative emphasis in her work. While she has extensive field experience, Sam also manages a team of field staff and a number of large diverse projects. She is a strong believer in effective communication being key to successful outcomes.

David Pemberton is a wildlife biologist who has worked on a variety of wildlife management projects from seal interactions with fish farms to albatross bycatch on long liners. He is currently the Manager of the Save the Tasmanian Devil Program. He has published over 50 scientific papers and three books including co-authoring the book The Tasmanian Devil: A Unique and Threatened Animal.

Katherine Belov is the Professor for Comparative Genomics at the University of Sydney. She is a world leader in the genetics of immunity of Australian mammals and has developed new paradigms for the management of Australian wildlife populations threatened by disease. She has published over 150 papers on immunity and conservation.

CONTRIBUTING AUTHORS

Paul Andrew

Taronga Conservation Society Australia, Mosman, New South Wales 2088, Australia

Olivia Barnard

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Katherine Belov

School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales 2006, Australia

James R. Biggs

Zoo and Aquarium Association Australasia, Mosman, New South Wales 2088, Australia

Warwick Brennan

Corporate Communications Branch, DPIPWE, Hobart, Tasmania 7001, Australia

William E. Brown

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Nadeen Burge

Corporate Communications Branch, DPIPWE, Hobart, Tasmania 7001, Australia

Onnie Byers

IUCN/SSC Conservation Planning Specialist Group, Apple Valley, Minnesota 55124, USA

Yuanyuan Cheng

UQ Genomics Initiative, University of Queensland, St Lucia, Queensland 4072, Australia

Rowena Chong

School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales 2006, Australia

Judy Clarke

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Janine Deakin

Institute of Applied Ecology, University of Canberra, Canberra, Australian Capital Territory 2617, Australia

Chris R. Dickman

School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales 2006, Australia

Emily Dowling

Trowunna Wildlife Sanctuary, Mole Creek, Tasmania 7304, Australia

Jodie Elmer

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Amanda Embury

Wildlife Conservation and Science, Zoos Victoria, Parkville, Victoria 3052, Australia

Tim Faulkner

Devil Ark, Tomalla, New South Wales 2337, Australia

Samantha Fox

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Liz Gabriel

Devil Ark, Tomalla, New South Wales 2337, Australia

Aaron C. Greenville

School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales 2006, Australia

Camille Goldstone-Henry

University of Sydney, Sydney, New South Wales 2006, Australia

Catherine E. Grueber

School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales 2006, Australia; San Diego Zoo Global, San Diego, California 92112, USA

Rodrigo K. Hamede

School of Natural Sciences, University of Tasmania, Hobart, Tasmania 7001, Australia

Colette Harmsen

Tinderbox Rd, Tinderbox, Tasmania 7054, Australia

Clare E. Hawkins

School of Natural Sciences, University of Tasmania, Hobart, Tasmania 7005, Australia

Chris J. Hibbard

Sydney, New South Wales 2006, Australia

Greg J. Hocking

Game Services Tasmania, DPIPWE, Hobart, Tasmania 7001, Australia

Carolyn J. Hogg

School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales 2006, Australia

Tracey Hollings

Arthur Rylah Institute for Environmental Research, Department of Environment, Land, Water and Planning, Heidelberg, Victoria 3084, Australia

Channing Hughes

The Carnivore Conservancy, Ulverstone, Tasmania 7315, Australia; School of Life and Environmental Sciences, University of Sydney, Sydney, NSW 2006, Australia

Stewart J. Huxtable

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Stephen Izzard

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Richard Jakob-Hoff

Auckland Zoo, Auckland, 1245, New Zealand

Menna E. Jones

School of Natural Sciences, University of Tasmania, Hobart, Tasmania 7000, Australia

Tamara Keeley

Taronga Western Plains Zoo, Dubbo, New South Wales 7315, Australia; School of Agriculture and Food Sciences, University of Queensland, Gatton, Queensland 4343, Australia

Androo Kelly

Trowunna Wildlife Sanctuary, Mole Creek, Tasmania 7304, Australia

Graeme Knowles

Animal Health Laboratory, Diagnostic Services Branch, DPIPWE, Kings Meadows, Tasmania 7249, Australia

Alexandre Kreiss

Menzies Institute for Medical Research, University of Tasmania, Hobart, Tasmania 7000, Australia

Peter Latch

Threatened Species Unit, Department of Environment and Energy, Canberra, Australian Capital Territory 2601, Australia

Clare Lawrence

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Billie T. Lazenby

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Andrew V. Lee

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Caroline M. Lees

IUCN/SSC Conservation Planning Specialist Group, Auckland Zoo, Auckland 1245, New Zealand

A. Bruce Lyons

School of Medicine, University of Tasmania, Hobart, Tasmania 7000, Australia

Hamish I. McCallum

School of Environment and Environmental Futures Research Institute, Griffith University, Nathan, Queensland 4111, Australia

Jane McGee

Previously DPIPWE, Hobart, Tasmania 7001, Australia

Elspeth A. McLennan

School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales 2006, Australia

Kimberly A. Miller

Healesville Sanctuary, Zoos Victoria, Healesville, Victoria 3777, Australia

Nicholas J. Mooney

Honourable Curator of Vertebrates, Tasmanian Museum and Art Gallery, Hobart, Tasmania 7001, Australia

Katrina Morris

Roslin Institute and R(D)SVS, University of Edinburgh, Easter Bush, Midlothian 0, UK

Elizabeth P. Murchison

Department of Veterinary Medicine, University of Cambridge, Cambridge, 0, UK

Thomas M. Newsome

School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales 2006, Australia

Michelle Nichols

Corporate Communications Branch, DPIPWE, Hobart, Tasmania 7001, Australia

Justine K. O’Brien

Taronga Conservation Society Australia, Mosman, New South Wales 2088, Australia

Marissa L. Parrott

Wildlife Conservation and Science, Zoos Victoria, Parkville, Victoria 3052, Australia

Sarah Peck

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Emma Peel

School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales 2006, Australia

David Pemberton

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Beth Pohl

Monarto Zoo, Zoos South Australia, Monarto, South Australia 5254, Australia

Ruth Pye

Menzies Institute for Medical Research, University of Tasmania, Hobart, Tasmania 7000, Australia

Elizabeth Reid-Wainscoat

San Diego Zoo Institute for Conservation Research, Escondido, California 92027, USA

David Schaap

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Philip J. Seddon

Department of Zoology, University of Otago, Dunedin, 9010, New Zealand

Andrew Sharman

Australian Antarctic Division, Department of Environment and Energy, Kingston, Tasmania 7050, Australia

Debra M. Shier

San Diego Zoo Institute for Conservation Research, Escondido, California 92027, USA

Rebecca Spindler

Bush Heritage Australia, Melbourne, Victoria 3000, Australia

Ronald R. Swaisgood

San Diego Zoo Institute for Conservation Research, Escondido, California 92027, USA

Kathy Traylor-Holzer

IUCN/SSC Conservation Planning Specialist Group, Apple Valley, Minnesota 55124, USA

Beata Ujvari

School of Life and Environmental Sciences, Deakin University, Geelong, Victoria 3320, Australia

John Weigel AM

Devil Ark, Tomalla, New South Wales 2337, Australia

Holly F. Wiersma

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Phil Wise

Save the Tasmanian Devil Program, DPIPWE, Hobart, Tasmania 7001, Australia

Howel Williams

Biosecurity Tasmania, DPIPWE, Hobart, Tasmania 7001, Australia

Gregory M. Woods

School of Medicine, University of Tasmania, Hobart, Tasmania 7000, Australia; Menzies Institute for Medical Research, University of Tasmania, Hobart, Tasmania 7000, Australia

Belinda Wright

School of Life and Environmental Sciences, University of Sydney, Sydney, New South Wales 2006, Australia

1

Carnivore conservation: the importance of carnivores to the ecosystem, and the value of reintroductions

Chris R. Dickman, Aaron C. Greenville and Thomas M. Newsome

Introduction

Carnivore populations are declining in most parts of the world, and concerns are held especially for the future survival of many large, charismatic and even formerly common species (Ripple et al. 2014). Because large carnivores typically sit at the top of their food chains and usually need extensive areas to hunt their prey, these species seldom achieve high densities. However, such carnivores are often reviled by humans due to their ability to attack and compete with us for food and space, and consequently are often culled, controlled or exploited directly to provide an economic return. On land, for example, several subspecies of leopard (Panthera pardus) and tiger (Panthera tigris) have been driven to critically low numbers over vast areas (www.iucnredlist.org), while in the marine environment populations of large sharks have suffered global declines of 90% or more (Myers and Worm 2005).

Yet, evidence is accumulating that the loss of carnivores – a process termed ‘trophic downgrading’ (Estes et al. 2011) – is not just depleting biological diversity at local, regional and global scales, but is also having damaging effects on the functioning and resilience of natural ecosystems. Indeed, Estes et al. (2011) argued that the loss of these animals may be humankind’s most pervasive influence on nature. Conserving carnivores, especially large species, is thus an urgent, albeit almost intractable, problem for managers and for society more broadly. Here we aim to first show, using a case study, that carnivores are critically important in maintaining functioning ecosystems and in enhancing the diversity of species these systems contain; and second, highlight the value of reintroducing carnivores to areas they once occupied or occupy now in low numbers. Although the term ‘carnivore’ may be taken to describe any animal that preys upon other animals, we restrict use of the term here to include vertebrates that feed principally on the flesh of other vertebrates.

The importance of carnivores

Large carnivores have long inspired awe (and fear) in people for their speed, power, grace and aesthetic appearance (Macdonald et al. 2015), as well as their ability to impinge upon human enterprises. Smaller species have been more likely to pass unnoticed, although the association between people and such carnivores as the domestic dog (Canis familiaris) and house cat (Felis catus) is long and well established. We acknowledge the importance of carnivores in human endeavours, but our primary focus here is on their effects on other species and the systems to which they belong.

Consumptive effects

Carnivores eat carrion or freshly killed prey, the most obvious effect of which is to reduce prey numbers. Yet, for a long time, this effect was thought to be trivial. Errington (1946), for example, suggested that carnivores had little influence on prey populations and took only individuals that would not survive anyway. Those individuals – the ‘doomed surplus’ – were considered to be largely young, old or sick, and would contribute little to overall population growth. More recent research has left no doubt that carnivores frequently do limit or regulate prey population growth. Some of the most compelling evidence for these effects comes from field experiments that manipulated carnivore numbers or tracked their populations over time. If such studies are conducted in a controlled and replicated manner, and prey populations respectively decrease or increase in response to changes in carnivore numbers, predatory impacts can be reliably inferred.

In addition to depressing prey populations, different species of co-occurring carnivores frequently interact and can mutually depress each other’s population size via competition. If two species differ in size, the smaller is almost always subordinate to the larger and – unless it is a social carnivore in a group – may be killed in direct encounters. The frequency and intensity of killing reach maximum when the larger species is two to 5.4 times the mass of the victim. Killing diminishes when the ratio of carnivore body sizes is less than two, due to the increased risks of injury to the combatants. It also decreases when the size ratio is >5.4, owing to the small benefit that large species could be expected to gain from killing smaller competitors (Donadio and Buskirk 2006). This situation, an extreme form of interference competition termed intraguild killing, becomes intraguild predation if the victim is eaten after being killed. If two species do not encounter each other directly but share similar food, habitat or other resources, the species that exploits those resources most efficiently will depress the population size of the other via exploitation competition. Both forms of competition can have profoundly negative effects on carnivore populations, distributions and resource use (Glen and Dickman 2005).

Although most encounters between carnivores are negative, at least for one of the species, some consumptive interactions have positive outcomes. For example, small carnivores may benefit from the presence of larger carnivores if the latter provide food for them. This situation can arise if the larger species flushes prey that are then accessed by the smaller species (e.g. the foraging activities of grey whales Eschrichtius robustus disturb fish and invertebrates in shallow marine sediments, making them available for a wide range of avian predators: Anderson and Lovvorn 2008); or if the larger species leaves the remains of prey that the smaller species can then use (e.g. carcasses that can be accessed by small species after larger species killed the animal or opened them up for scavenging). In rare situations, carnivores may confer mutual benefits on each other. Thus, the foraging activities of the dwarf mongoose (Helogale undulata) flush varied small vertebrates and invertebrates from cover, thereby increasing the prey-capture success of closely associated hornbills (Tockus flavirostris and T. deckeni). Mongooses benefit from the association by earlier and more efficient detection of predators; hornbills even respond to predators that potentially threaten only the mongoose, apparently learning the identities of specific predators from the responses of mongooses themselves (Dickman 1992).

Non-consumptive effects

Large carnivores and other predators have been termed ‘strongly interactive species’ because of their powerful and pervasive influence on other species (Soulé et al. 2003). As we have seen, carnivores often exert their effects on other species directly, by killing and eating them. This depletes populations of prey, but it can liberate both non-prey species by decreasing the levels of competition that they experience, and species in lower trophic levels by reducing populations of their own immediate predators. This latter situation is termed a ‘trophic cascade’. Conversely, carnivores may exert effects by modifying the behaviour of their prey and that of subordinate competitors. Scared or apprehensive prey and competitors often shift their activity or move to other habitats to avoid predators, and this in turn can liberate populations of other species with which they interact. Such non-consumptive effects are termed ‘ecological cascades’, and have been suggested to be more important than consumptive effects in shaping patterns of behaviour and foraging by prey (Laundré et al. 2001; Ripple and Beschta 2004). These cascades have been described in assemblages of placental and marsupial carnivores, as well as in assemblages of other vertebrates.

Case study

In the Australian context, the dingo (Canis dingo) provides a particularly helpful example of the pervasive effects that carnivores can have on other species and on non-living components of the environment. Space limits preclude citing all the research that has contributed to our current knowledge, but studies by Letnic et al. (2012), Newsome et al. (2015) and Lyons et al. (2018), and references therein, describe much of our current understanding.

The dingo was introduced to Australia from south-east Asia at least 4600 years ago, possibly on several occasions, and now occurs in virtually all terrestrial habitats across the continental mainland. It is absent from Tasmania. Its diet comprises a very wide range of prey, from insects to ungulates, although mid-sized and larger vertebrates such as rabbits, kangaroos, feral pigs, goats and emus feature prominently in many areas. It is the apex, or top, mammalian predator in Australia and, weighing up to 20 kg, is two to four times as heavy as the red fox (Vulpes vulpes) and feral cat (Felis catus) that were introduced following European settlement. Recent studies suggest that the long tenure of the dingo in mainland habitats has allowed sufficient time for coevolution with native mammals. Thus, these prey can detect and respond aversively to dingo scent cues, minimising their risk of being killed and eaten. Although controversial, the development of prey’s innate ability to detect and respond to cues to dingo presence provides strong support for the idea that the dingo should be considered a native – or at least naturalised – species (Steindler et al. 2018).

Irrespective of its ‘nativeness’, the dingo is persecuted in many areas owing to its attacks on livestock, especially sheep. Animals are shot, poisoned, trapped, deterred by larger guardian animals such as maremma dogs, or physically excluded from flocks by fencing. In south-eastern Australia a ‘dog fence’ runs for over 5600 km from Jandowae, Queensland, to Penong, South Australia, and acts as a barrier to the movement of dingoes into the continent’s south-east. Although dingoes do occur inside the exclusion zone, they tend to be more numerous in coastal areas and in pockets through the Great Dividing Range than they are on the western slopes of the Dividing Range and the rangelands. Dingoes are absent or present at low density inside the dog fence but occur commonly on the other side of the fence, in Queensland and South Australia. The marked difference in dingo abundance on different sides of the fence provides great insight into the powerful effects of this carnivore on the structure and functioning of rangeland ecosystems.

These effects can be viewed as flowing through two main pathways (Fig. 1.1). In the first, dingoes hunt large herbivores such as kangaroos and emus, suppressing their populations by up to two orders of magnitude outside compared to inside the dog fence. The paucity of dingoes inside the fence allows livestock to be run. Elevated populations of livestock, native herbivores and feral herbivores such as goats can place vegetation under heavy grazing pressure. In western New South Wales, for example, much of the native vegetation that provided nutritious fodder for herbivores was destroyed by overstocking of sheep in the two decades before 1900, and the region has never recovered. During dry periods in this region, such as the widespread drought in 2018, vast areas are turned into dust bowls with no grass or herbaceous cover and scant remaining shrubs and trees. Herbivore populations crash, and pastoral enterprises are placed under immense pressure. Outside the fence, by contrast, where dingoes continue to suppress herbivore populations, at least some native vegetation usually remains, even during long dry periods.

The effects of dingoes have further ramifications through the first pathway. By suppressing herbivore populations and facilitating increases in the biomass of grasses, herbs and shrubs, dingoes provide increased shelter and food resources for small mammals, birds and reptiles, as well as a high diversity of invertebrates (Fig. 1.1). These animals in turn are likely to facilitate the continuation of important ecological processes such as pollination, seed and spore dispersal, and the turning of soil that allows infiltration of rainwater and recycling of nutrients. Increased biomass of vegetation also leads to the formation of layers of leaf litter, which return organic material to the soil and provide rich microenvironments for microorganisms, fungi and diverse communities of animals. During dry periods, such habitats provide fuel for fires. Small-scale fires can generate mosaic landscapes that support diverse patches of different-aged post-fire vegetation and the animal communities that are associated with these patches, whereas large-scale fires may promote extensive stands of even-aged vegetation. In the absence of dingoes, these manifold and pervasive effects on plant and animal diversity and ecosystem functioning are muted or lost. Arguably, the dramatic effects of dingo absence would be less negative if livestock were absent from the rangelands. Whatever the case, there is little doubt that the vast, dry dingo-less sheep rangelands represent some of the most ecologically barren and degraded landscapes in Australia.

Fig. 1.1.   Conceptual model of interactions that might be expected in the presence of the dingo (Canis dingo), shown by solid arrows, in a rangeland environment. Numbers in parentheses represent the predicted sequence of events. For example, if dingoes suppress large herbivores such as kangaroos and emus, then grass and herb biomass would be expected to increase. If dingoes also suppress mesopredators such as the European red fox and feral cat, small mammals (e.g. mice), reptiles (e.g. goannas) and birds (e.g. parrots) should increase, although this response may take longer to manifest than the response of vegetation. Invertebrates may also respond to improved vegetation condition and contribute to soil health. However, the strength of all interactions may be influenced by the extent of rainfall and fires (dotted arrows). This example, taken from Newsome et al. (2015), focused on interactions expected in Sturt National Park, New South Wales, but should be applicable to rangeland environments more broadly. Reprinted with permission.

The second pathway through which dingoes exert their influence on ecosystems is via their suppression of the activity and abundance of the red fox and feral cat (Fig. 1.1). These smaller carnivores may be killed (but not necessarily eaten) upon encounter with dingoes, and hence are under pressure to detect the presence of dingoes and reduce the risk of meeting them whenever and wherever possible. The dingo-associated risks to both the smaller carnivores are probably related inversely to the structural complexity of the habitat, with open treeless habitats being most risky (foxes and cats are more easily detected in the open, and have fewer options to escape) and forested and topographically rugged habitats least risky. The most compelling studies of the interaction between dingoes and the smaller carnivores show that the red fox is less active locally and regionally where dingoes occur, whereas feral cats show both spatial and moment-to-moment avoidance of dingoes, especially in open environments (see Letnic et al. 2012 for a review). Reductions in the activity or abundance of the smaller introduced predators in turn provide a reprieve for the many native species that fall prey to them. This outcome is important to highlight because at least 30 species of native mammals have been extirpated in Australia in much less than 200 years, with the majority of losses attributable – at least in part – to the depredations of the introduced red fox and feral cat (Woinarski et al. 2015). The impacts of invasive carnivores are probably amplified because native prey are naïve to the hunting tactics deployed by the newcomers and do not have behaviours that allow them to effectively detect and avoid the predators. Initially dense populations of naïve prey can also be depleted very rapidly if the carnivores exhibit ‘surplus killing’ behaviour; that is, killing but not eating all the victims.

Fig. 1.2.   Conceptual model, based on empirical data, of mammal body size versus effect size arising from the presence of the dingo (Canis dingo) during conditions of low (solid line) and high (dashed line) resource availability. Positive effect sizes indicate species whose abundance is suppressed due to predation by dingoes. Negative effect sizes indicate species whose abundance increases in the presence of dingoes due to the suppression by dingoes of European red foxes, feral cats and herbivores. The suppressive effects of dingoes on medium-sized mammals is moderate during periods of high resource availability due to prey switching by dingoes to eruptive small prey such as rodents and locusts. The beneficial effects of dingoes on small mammal prey diminish during periods of high resource availability due to increased predation pressure from foxes, cats and dingoes, when top-down forcing effects of the dingo on the smaller carnivores are expected to weaken. Redrawn from Letnic et al. (2012).

Comparative studies on both sides of the dog fence also show that dingoes’ effects scale with the body size of their prey and those of the smaller introduced predator species (Fig. 1.2). In essence, potential prey that weigh up to ~3 kg achieve higher abundances in the presence than in the absence of dingoes, with positive effects being greatest for prey weighing 60–100 g. Prey in this size range are at most risk of predation from the red fox and feral cat but are too small to be eaten preferentially by dingoes; hence they benefit indirectly from the suppression of foxes and cats by the dingo. Prey weighing above ~3 kg derive less benefit from the presence of dingoes. They become negatively affected, as they form a greater part of the dingo’s diet and a smaller component of the diet of the fox and cat. Very large prey, such as swamp buffalo (Bubalus bubalis) and camel (Camelus dromedarius), are unaffected by the presence of the dingo as they are too large to be hunted on a regular basis (Fig. 1.2). The effects of dingoes can be expected to vary between habitats and times; for example, in Fig. 1.2 the positive effects of dingoes on small prey are reduced during periods of high resource availability as the suppressive effects of the apex predator on the smaller introduced predators diminish. Despite such variation in effects, it is clear that dingoes can markedly increase the abundance and diversity of a wide range of small vertebrate species, but decrease the abundance of much larger prey such as kangaroos.

Although these interactions have been illustrated as two separate pathways, the effects of dingoes are even more far-reaching. The presence of dingoes is associated with fewer large herbivores and reduced activity of red foxes and feral cats; the resultant increases in the biomass of vegetation and reduced predation pressure promote large populations of small prey species. In a series of elegant experiments carried out in the Strzelecki Desert, Mike Letnic and colleagues at the University of New South Wales showed that the suppressive effects of dingoes on red foxes and feral cats facilitate increased populations of small mammals that eat shrub seeds and seedlings (Letnic et al. 2012; Mills et al. 2018). Increased predation pressure on the seeds and seedlings reduces shrub recruitment, in turn promoting aeolian and sedimentary processes that result in greater soil erosion and mobility of the dominant landform: sand dunes. In the absence of dingoes, inside the dog fence, these processes are reversed. Large populations of red foxes and feral cats maintain small mammals at very low levels, reducing predation on seeds and allowing shrub recruitment. High shrub cover leads to higher dunes and greater dune stability, providing evidence that dingoes can indirectly effect large-scale changes in landscape geomorphology (Lyons et al. 2018).

In summary, top predators often have powerful and extraordinarily extensive effects on the ecosystems to which they belong. Their loss can have negative effects on local and regional biodiversity and ecological processes, and even lead to shifts in the physical environment. These pervasive effects have been best studied in canids such as the dingo and grey wolf, but can be expected to occur in any ecosystem with a top predator, irrespective of that predator’s taxonomic identity. In Tasmania, for example, the Tasmanian devil (Sarcophilus harrisii) is the top mammalian predator. Its loss would be disastrous from many perspectives, including the loss of ecological functions that its demise would be likely to trigger. To forestall such events, or to restore species and ecological functions if top predators have suffered local or regional extinctions, reintroductions may be attempted.

Indirect effects

When one species affects the interaction between two or more others, whether consumptive or non-consumptive, its effect can be considered indirect. Such interactions are surprisingly pervasive. On the one hand, indirect interactions can affect the population sizes, dynamics and resource use of individual species, as well as the composition of ecological communities. On the other, the effects can extend to altering the amount of carbon that is sequestered in marine and terrestrial environments, to shaping riverine dynamics and landscape form and function. The theory underpinning indirect interactions has been elaborated by many authors (see Glen and Dickman 2005 for a review), and interaction pathways have been described in several field studies. Among the best-known examples are the broadly positive and cascading effects that have been uncovered following the reintroduction of grey wolves (Canis lupus) to Yellowstone National Park in the US (Smith and Bangs 2009), and the complex interactions following exclusion of predators in large-scale experiments at Kluane in Canada (Krebs et al. 2001).

The value of reintroductions

Guidelines formulated by the International Union for Conservation of Nature (IUCN) define a reintroduction as ‘the intentional movement and release of an organism inside its indigenous range from which it has disappeared’ (IUCN/SSC 2013). The aim of reintroductions is to re-establish a viable population, or populations, of a focal species within its former range. The motivations for reintroductions include restoring species that are iconic (e.g. California condor, Gymnogyps californianus), aesthetically pleasing (e.g. southern corroboree frog, Pseudophryne corroboree), ecologically or economically important (e.g. sea otter, Enhydra lutris) or evolutionarily significant or unusual (e.g. Wollemi pine, Wollemia nobilis). Most reintroductions involve species that are of conservation concern, and seek to expand their numbers to reduce their risk of future extinction. Many species of carnivores satisfy all these considerations. If reintroduced, they could be expected to restore other components of biodiversity to local and regional landscapes via top-down forcing.

Despite the poor conservation prognosis of many carnivore species, there is often considerable resistance to reintroducing them. Large carnivores are likely to need expansive areas within their indigenous ranges to form viable populations; for many, there may now be insufficient habitat to allow this. In addition, large carnivores have the potential to kill or injure people, pets and livestock, thus further reducing the chances of potential reintroductions. In the US, for example, the grey wolf was reintroduced to central Idaho and Yellowstone National Park in 1995–96 – only after nearly 20 years of public consultation, debate and political interference (Smith and Bangs 2009). Small carnivores have been historically easier to reintroduce to their former ranges, and examples such as the black-footed ferret (Mustela nigripes) and European otter (Lutra lutra) provide well known and notable success stories.

On the mainland of Australia, carnivorous marsupials such as the eastern quoll (Dasyurus viverrinus), western quoll (D. geoffroii) and northern quoll (D. hallucatus) are being reintroduced to parts of their former ranges, and reintroductions of several smaller species (e.g. dibbler, Parantechinus apicalis, red-tailed phascogale, Phascogale calura), have already taken place. None of these species can be considered large or apex carnivores, and attempts to re-establish them generally have attracted either little attention or positive support from local communities. This situation differs sharply from that attending the two larger carnivores that have been suggested as candidates for future reintroductions: the dingo and the Tasmanian devil. Both species have been the subject of much debate about whether reintroductions should proceed. Below, we consider some of the arguments for and against this course of action.

Dingo

The dingo is not a species of conservation concern at the national level, although many populations – especially in south-eastern Australia – are considered to be at risk of losing their genetic purity due to hybridisation with domestic or feral dogs. Instead, the main argument for reintroducing the dingo is to restore biodiversity and ecological function to the extensive rangeland areas from which the dingo is currently banished. These benefits could be extensive. Using species distribution data and assumptions about the benefits that flow to threatened small mammals when dingoes are present, Letnic et al. (2012) estimated that these mammals would experience reduced predation pressure from the red fox over an area of more than 2.42 million km² if dingoes were reintroduced throughout the landscape. If the presence of dingoes also allowed the subsequent natural expansion or reintroduction of mid-sized ecosystem engineers such as bettongs (Bettongia spp.) and bandicoots (Isoodon, Perameles spp.), the opportunities to restore soil health, nutrient cycles and other ecological processes could be enormous (Letnic et al. 2012). The restoration of Australia’s rangelands from the reintroduction of the dingo, and the resulting increase in pasture, could also provide a net positive economic benefit to the cattle industry (Prowse et al. 2015).

The arguments against reintroducing the dingo are two-fold. First, some authors propose that the large body of evidence supporting the positive effects of dingoes is weak or flawed and hence that a reintroduction may not have clear benefits. In our opinion this view is poorly supported and, in itself, no barrier to thinking about how small-scale dingo reintroduction trials could be best carried out (Newsome et al. 2015). Second, dingoes attack and kill livestock, especially sheep, and any proposal to allow dingo reintroductions to rangeland areas needs to account for this. Cost–benefit analyses suggest that many solutions for livestock–dingo coexistence could be considered, including greater use of guardian animals to protect open-range flocks, physical, chemical and sonic deterrents to dingoes, insurance schemes and other financial incentives. Although all these methods are used currently in Australia, lethal control dominates to a greater extent in the country’s rangelands than anywhere else in the world despite limited evidence to support its use (van Eeden et al. 2018). Implementation of non-lethal management methods would need careful and extensive engagement with all stakeholders, but the successful integration of much larger carnivores with livestock enterprises globally shows that this should be possible (van Eeden et al. 2018).

Tasmanian devil

Largest of the surviving marsupial carnivores, the Tasmanian devil is listed currently as Endangered on the IUCN Red List of Threatened Species (http://www.iucnredlist.org/search). Although it occurs throughout Tasmania, an area of 64 500 km², this iconic species has suffered dramatic reductions in numbers since the mid-1990s owing to the emergence of an invariably fatal and highly infectious cancer: devil facial tumour disease (DFTD). Because animals are still present throughout most of the species’ current natural range, albeit at much reduced densities, reinforcement or supplementation rather than reintroduction per se is the most appropriate strategy to achieve population restoration. Reinforcement is defined by the IUCN as ‘the intentional movement and release of an organism into an existing population of conspecifics’ (IUCN/SSC 2013). As this book shows, Tasmanian devils have been the subject of an extraordinarily intense and innovative research and management program that has seen the ravages of DFTD understood and tempered, and insurance populations established behind fences and on islands. The immediate future of the Tasmanian devil thus seems assured. But, what of the longer term?

The Tasmanian devil occurred on the mainland of Australia until perhaps 3000 years ago, and appears to have had a Holocene distribution that covered much of the southern half of the continent. Based on this observation, calls have been made to consider the Tasmanian devil a candidate for reintroduction to the mainland, even if millennia have passed. On the pro side of this debate, species distribution modelling suggests that large areas of forest in south-eastern regions of the continent would provide suitable habitat for Tasmanian devils, and that a wide range of potential prey species is present (Hunter et al. 2015). Likely causes of the species’ disappearance from the mainland – competition and predation from the dingo, as well as Indigenous hunting – no longer operate, or do so at reduced intensity. The value of a successful reintroduction would be manifold: the Tasmanian devil would have an expanded geographical range and much larger population size, leading over time to increased genetic diversity and resistance to internal (e.g. disease) and existential threats. These changes would help to secure the long-term future of the species.

On the con side of the debate, large areas of south-eastern Australia have been recently and extensively modified for agriculture and human settlement, and their suitability as habitat for the Tasmanian devil is unclear. It is also unclear how Tasmanian devils might fare in environments where European red foxes and feral cats are now abundant, and how poison baiting regimes for the red fox – which are undertaken broadly throughout south-eastern Australia – might affect devil populations (Hughes et al. 2011). Social licence would need to be obtained if the Tasmanian devil were to be returned to mainland Australia, especially in farming areas where livestock flocks are run. The ecological case for reintroducing the Tasmanian devil to the Australian mainland remains controversial. Time will tell whether we can gain social acceptance and muster the political courage to take the next steps.

Mainland reintroductions aside, recovering the health and population status of devils in Tasmania is critical to ensuring the species’ continued persistence and, as described in the following chapters, the use of science-based management has contributed immensely to this objective. The debate about a potential mainland reintroduction will no doubt continue in the future (Chapter 24).

Conclusion

In recent years there has been a surge in our understanding of the powerful and pervasive roles that carnivores play in natural ecosystems. Carnivores scavenge or hunt and kill prey to make a living, and often suppress prey populations. Less obviously, they can scare prey simply by their presence, indirectly reducing the fitness of prey by restricting their times or places of activity and thus curtailing their access to resources. These effects flow or cascade through to other species that may never encounter carnivores directly, and can result in complex webs of interactions that influence the structure and function of both the living and abiotic components of ecosystems. The effects of carnivores are, arguably, more profound and important than those of any other trophic groups of animals, therefore making the accelerating global decline of these charismatic creatures an issue of grave concern. Although the plight of the world’s largest (≥15 kg) carnivores is perhaps best known (Ripple et al. 2014), many smaller mammalian carnivores, such as the Tasmanian devil, as well as non-mammalian carnivores, are considered to be at some risk of future extinction (www.iucnredlist.org).

In the Anthropocene, unfortunately, carnivores can be their own worst enemies. Their wide-ranging movements and need for large hunting ranges place them in frequent contact with people, pets and livestock, and their predatory behaviour in these situations consistently provokes conflict. Despite this, reintroductions, reinforcements and legal protections are increasingly used as means of returning carnivores