Ecology and Management of the Grey-Headed Flying-Fox Pteropus Poliocephalus

The Ecology and Management of the Grey-Headed Flying-Fox Pteropus poliocephalus

Author Roberts, Billie

Published 2013

Thesis Type Thesis (PhD Doctorate)

School Griffith School of Environment

DOI https://doi.org/10.25904/1912/1723

Downloaded from http://hdl.handle.net/10072/366934

Griffith Research Online https://research-repository.griffith.edu.au

The ecology and management of the grey-headed flying-fox Pteropus poliocephalus

Photo © Vivien Jones

Billie Roberts BSc (Hons)

A thesis submitted in fulfilment of the requirements of the degree of Doctor of Philosophy

Griffith School of Environment Griffith University September 2012

This work is dedicated to the researchers, wildlife carers and community members trying to conserve ‘unpopular’ threatened species. May you be inspired to learn more about these species and work harder to prevent their demise.

Abstract

Effective conservation and management of many highly mobile animal species, including flying-foxes of the genus Pteropus, are constrained by lack of knowledge of their ecology, especially of movement patterns over large spatial scales.

This study deals with the conservation ecology of the grey-headed flying-fox (Pteropus poliocephalus), a highly mobile colonial-roosting mammal endemic to eastern Australia. Like many flying-foxes in the Asia-Pacific, this species frequently comes into conflict with humans for raiding commercial fruit crops, establishing roost sites in urban areas, and because it is a vector for some diseases of humans and their commensal animals. For these reasons, P. poliocephalus has been the subject of numerous control attempts, mostly conducted at the local scale (killing of individuals at feeding sites and roosts; attempts to destroy or relocate roosts). These attempts have rarely been successful in reducing conflict between humans and flying-foxes over the long term. Partly as a result of these actions and partly because of a loss of habitat, P. poliocephalus is considered a threatened species in some jurisdictions. The conservation and management of P. poliocephalus is therefore a difficult problem. The broad objectives of this thesis are to provide new information on the ecology of P. poliocephalus, particularly in relation to distribution, movement patterns and roosting behaviour, in the hope that this information will better inform the management and conservation of the species.

Historical changes in the distribution of P. poliocephalus and another Australian flying-fox (P. alecto), whose range overlaps with P. poliocephalus, were assessed from locality records (dating from 1843 to 2007) obtained from a wide range of sources, filtered for reliability and spatial accuracy. Analysis of these records did not support previous claims that the distributions of these species had shifted in a manner driven by climate change. First, neither the northern or southern range limits of P. poliocephalus (Mackay, Queensland and Melbourne, Victoria respectively) have changed over the past century. Second, while the southern range limit of P. alecto extended southward by over 1000 km (more than 10 degrees latitude) during the twentieth century (from Rockhampton, Queensland to Sydney, New South Wales), the rate of expansion was much greater than observed changes in climate. The range of P. alecto expanded southward at about 100 km/ decade, compared with the 10–26 km/ decade rate of isotherm change. Analyses of historical weather data show that the species consequently moved into colder regions than it had previously occupied.

Abstract ii

To quantify the movement patterns of P. poliocephalus, fourteen adult male P. poliocephalus were satellite tracked for 2–40 weeks (mean 25 weeks). Collectively, these individuals utilised 77 roost sites in an area spanning over 100,000 km2. The study showed that movement patterns of flying-foxes varied greatly between individuals and within individuals over time. The tracked flying-foxes exhibited a range of movement patterns, from relatively sedentary to frequent long distance travel (>300 km) between multiple roosts. Migrating flying-foxes were capable of rapid sustained long-distance flight, including one movement of 500 km within 48 hours. Seasonal movements were consistent with facultative latitudinal migration in part of the population. Flying-foxes shifted roost sites frequently: 64% of roost visits lasted <5 consecutive days, although a small proportion of roost stays were of >2 months’ duration (maximum stay at a roost was 133 days).

Data from the 14 satellite tracked flying-foxes were then used to examine the feeding movements of P. poliocephalus and to analyse the landscape characteristics of their feeding and roosting sites. Tracked individuals of P. poliocephalus used a wide range of habitats from highly urbanised areas to substantial tracts of intact forest. The landscape-scale habitat characteristics within 2 km surrounding roosting and feeding sites differed statistically. Pteropus poliocephalus tended to select roost sites in landscapes containing a higher proportion of built and cleared habitats than expected from their occurrence in the environment. By contrast, they showed some avoidance of built areas for feeding. The distances moved from roosts to feeding sites were typically less than 20 km (mean 12 km), although there was a large amount of variation within and between individuals (the range of distances moved from roosts to feeding sites was 2 - 56 km).

The final data chapter in this thesis reviews the outcomes of 10 attempts by public authorities to relocate roosts of flying-foxes, with a detailed examination of one long-term relocation attempt at Maclean in north-east New South Wales. Such relocations are often attempted when flying-foxes roost in or near human settlements. However the success (or otherwise) of this approach to managing conflict between humans and flying-foxes has not previously been systematically assessed. The review found that, while some relocation actions have succeeded in moving flying-foxes from their original roost sites, in most cases the effect has been temporary, and ongoing programs of dispersal have been required to prevent re- establishment of the original roosts. When disturbances were used to disperse flying-foxes from roosts, many flying-foxes did not join pre-existing roosts, instead establishing one or

Abstract iii more new roosts, usually close to the original site. These new roosts were rarely at ‘predetermined’ target sites (i.e. likely roost sites identified by proponents of the relocation); and frequently the locations of new roost sites were no more acceptable to the broader community than the original roost site. Although seldom systematically recorded, the costs of relocation could be high; for the two instances where details were available the costs were thousands at Maclean, and millions at a site in Melbourne.

The results of this research have important implications for the management of P. poliocephalus. Data from the satellite tracking study show that flying-foxes are highly mobile, with individuals conducting frequent, often long-distance movements among roosts. Therefore, it is not surprising that past attempts at resolving conflicts between humans and flying-foxes, which have involved local-scale actions such as culling and disturbances at particular ‘problem’ roosts, have rarely succeeded over the long-term. In addition, the review of relocation attempts has shown that the quantum of costs and resources required for relocations are beyond the means of most small rural and regional communities.

This study and related research show that P. poliocephalus displays a preference for establishing roost sites within built environments. While the factors driving this preference are not well understood, it seems likely that the location of flying-fox roosts within human settlements will continue to be an issue of community conflict into the future. The management of this conflict is complex, involving consideration both of human welfare and the ecology of a highly mobile, threatened species. Therefore, robust approaches to conservation and management of flying-foxes need to be informed by a sound understanding of the species’ movement patterns and habitat preferences. The information provided in this thesis should therefore contribute to better conservation and management outcomes for P. poliocephalus and flying-foxes in general.

Abstract

Statement of Originality

I, Billie Roberts, certify that this work has not previously been submitted for a degree or diploma in any university. To the best of my knowledge and belief, the thesis contains no material previously published or written by another person except where due reference is made in the thesis itself.

Billie Roberts

September 2012

Statement of Originality vi

Contents

Abstract ...... i

Statement of Originality ...... v

List of Tables ...... x

List of Figures ...... xii

List of Plates ...... xv

List of Appendices ...... xvi

Acknowledgments ...... xvii

Research permits and animal ethics ...... xx

Publications produced from this research ...... xxi

Chapter 1 – General Introduction ...... 1

1.1 Animal movement in dynamic landscapes ...... 1

1.2 Managing long-distance movements ...... 2

1.3 Ecology of Pteropus – a highly mobile genus...... 3

1.3.1 Status and distribution ...... 3 1.3.2 Roosting behaviour and habitat requirements ...... 4 1.3.3 Feeding behaviour ...... 6 1.3.4 Movement capability ...... 7 1.3.5 Management of Pteropus ...... 9

1.4 Australian flying-foxes ...... 12

1.5 Aims and structure of this thesis ...... 12

Contents vii

Chapter 2 – Latitudinal range shifts in Australian flying-foxes: a re-evaluation ...... 15

2.1 Introduction ...... 15

2.2 Methods ...... 17

2.2.1 The species and their distributions ...... 17 2.2.2 Construction of distributional database ...... 18 2.2.3 Distributional changes in Pteropus alecto and P. poliocephalus ...... 19 2.2.4 Analysis of climate within range of P. alecto ...... 20 2.2.5 Trends in the abundance of flying-foxes within specific roosts ...... 20

2.3 Results ...... 21

2.3.1 Number and distribution of observations ...... 21 2.3.2 Distributional changes in Pteropus alecto and P. poliocephalus ...... 22 2.3.3 Climate dynamics at P. alecto’s changing southern limits...... 26 2.3.4 Abundance trends in the Currie Park roost...... 27

2.4 Discussion...... 27

2.4.1 Species-specific range dynamics and their possible causes ...... 27 2.4.2 Interactions between the species ...... 31

2.5 Conclusions ...... 32

Chapter 3 – Long-distance and frequent movements of the flying-fox Pteropus poliocephalus: implications for management ...... 34

3.1 Introduction ...... 34

3.2 Methods ...... 35

3.2.1 Study species ...... 35 3.2.2 Study area and capture sites ...... 36 3.2.3 Satellite telemetry ...... 37 3.2.4 Data manipulation and analysis ...... 38

3.3 Results ...... 40

3.3.1 Long-term and long-distance ranging behaviours ...... 40 3.3.2 Quantitative patterns of movement and roost site use ...... 45

Contents viii

3.4 Discussion...... 52

3.4.1 Patterns of movement and roost site use ...... 52 3.4.2 Comparison with other flying-foxes ...... 53 3.4.3 Caveats to this study ...... 54 3.4.4 Management implications ...... 55

3.5 Conclusion ...... 56

Chapter 4 – Feeding movements and landscape use by P. poliocephalus ...... 58

4.1 Introduction ...... 58

4.2 Methods ...... 60

4.2.1 Capture and satellite telemetry ...... 60 4.2.2 Feeding sites ...... 61 4.2.3 Roost sites ...... 62 4.2.4 Landscape measurements ...... 63 4.2.5 Data analysis ...... 64

4.3 Results ...... 65

4.3.1 Habitat characteristics of feeding and roost sites ...... 67 4.3.2 Movement between roosts and feeding sites ...... 69 4.3.3 Factors influencing distance moved ...... 72

4.4 Discussion...... 76

4.4.1 Roost sites ...... 76 4.4.2 Feeding sites ...... 78 4.4.3 Comparison between feeding and roosting sites ...... 79 4.4.4 Factors influencing feeding movements ...... 79

Chapter 5 – The outcomes and costs of relocating flying-fox roosts: insights from the case of Maclean ...... 83

5.1 Introduction ...... 83

5.2 Study region and its flying-foxes ...... 84

5.2.1 Flying-fox roost sites in the Lower Clarence region ...... 84

Contents ix

5.1.2 Maclean flying-fox roost relocation ...... 86

5.3 Methods ...... 89

5.3.1 Response of Maclean flying-foxes to relocation: survey methods ...... 89 5.3.2 Determining financial costs and disturbance effort ...... 89

5.4 Results ...... 90

5.4.1 Disturbance method ...... 90 5.4.2 Disturbance of flying-foxes at the Maclean roost ...... 90 5.4.3 Cost of the relocation...... 92 5.4.4 Assessment of flying-fox roost sites used since the relocation ...... 93

5.5 Discussion...... 94

5.5.1 Effect of disturbances on site use by flying-foxes ...... 94 5.5.2 Cost-effectiveness of relocation attempts ...... 97 5.5.3 Managing flying-fox relocations in the future ...... 98

5.4 Conclusion ...... 100

Chapter 6 – General Discussion ...... 103

6.1 Key findings of each data chapter ...... 103

6.2 Patterns of roost usage and mobility by flying-foxes ...... 107

6.3 Ecology and management of flying-foxes in human dominated environments 110

6.4 Research directions ...... 116

References ...... 118

Appendices ...... 135

Contents x

List of Tables

Table 2.1 Correlations (Spearman rank, N = 8 time-periods) between parameters describing the latitudinal distribution of Pteropus alecto and P. poliocephalus and time using point and grid records...... 23

Table 2.2 Differences in four climatic variables at four latitudinal locations representing the lower quartile and most southern limit of grid records of Pteropus alecto at two time-periods, 1921–50 and 2001–07...... 26

Table 3.1 Net displacement moved by flying-foxes among roosts in time-periods of 1‒ 30 weeks duration...... 48

Table 3.2 Cumulative displacement moved by flying-foxes among roosts in time-periods of 1‒ 30 weeks duration...... 49

Table 4.2 Correlations (Pearson) between the feeding distances moved and roost population size (log transformed), feeding visit duration (days) and feeding forest patch size (ha) using five different units as replicates; all feeding records, independent feeding records, individuals (with more than 10 feeding records) and within two individual flying-foxes which had large (>20) numbers of feeding records together with high variation in feeding distances (Bat 5 and Bat 10)...... 73

Table 4.3 Correlations (Pearson) between the feeding distances moved and four landscape attributes within 2 km radii of roosts at two different sampling units; all feeding records (N=173) and independent feeding records (N=112)...... 75

Table 5.1 Estimated costs of the relocation of flying-foxes from the Maclean Rainforest Reserve and the Melbourne Royal Botanical Gardens...... 93

Table 5.2 Summary of known documented attempts to relocate Australian flying-fox roosts using non-lethal methods, during 1990 to 2009...... 96

List of Tables xi

Table A2.1 Summary of the key records of P. poliocephalus in its northern range (north of latitude 26oS)...... 139

Table A2.2 List of recent (2008) records of P. poliocephalus in the northern part of its distribution...... 140

List of Tables xii

List of Figures

Figure 2.1 Locality (point) records for (a) Pteropus alecto (N = 870) and (b) P. poliocephalus (N = 2,506) in coastal eastern Australia from 1843 to 2007...... 22

Figure 2.2 Box plots showing the latitudinal distribution of Pteropus alecto (upper; grey) and P. poliocephalus (lower; white) in eastern Australia between 1843–2007 using (a) point records and (b) 50 x 50 km grid data...... 24

Figure 2.3 Percentage of point records of flying-foxes in different latitudinal bands within eastern Australia that were Pteropus poliocephalus at four time-periods; 1843– 1950, 1951–1990, 1991–2000 and 2001–2007...... 25

Figure 2.4 Population estimates of Pteropus alecto and P. poliocephalus in the Currie Park roost, Lismore, during two time-periods, January 1988 – July 1990 and July 1998 – April 2004...... 27

Figure 3.1 Roosts used by 14 satellite-tracked Pteropus poliocephalus between October 2007 and April 2009...... 42

Figure 3.2 North-south movement patterns of 13 satellite-tracked Pteropus poliocephalus from their points of capture...... 43

Figure 3.3 Weekly movement patterns of 3 satellite-tracked Pteropus poliocephalus from their points of capture...... 44

Figure 3.4 Frequency (%) distributions of the duration of roost visits and the distances between consecutively-recorded roosts...... 47

Figure 3.5 Frequency distribution of net and cumulative displacements by flying-foxes among roosts in different time-periods...... 50

Figure 3.6 Number of roosts used by flying-foxes in relation to cumulative displacement during different time-periods...... 51

List of Figures xiii

Figure 4.3 Frequency distribution (%) of the feeding distances moved by the 14 P. poliocephalus; (a) all 173 feeding records and (b) 112 independent feeding records ...... 70

Figure 4.4 Feeding distance (km) moved by each of the 14 P. poliocephalus; (a) all records and (b) independent records...... 71

Figure 4.5 Frequency distribution of the duration of feeding visits by 14 Pteropus poliocephalus (N = 110 visits to different sites)...... 72

Figure 4.6 Relationships between the feeding distances moved (km between roost and feeding sites) and feeding visit duration (days) for cases where there was a relatively strong (P < 0.10) correlation; (a) all feeding records (N = 173), (b) individual flying-foxes (N = 9), and (c) Bat 5 (N = 24)...... 74

Figure 4.7 Mean monthly feeding distances (+SD) of 14 Pteropus poliocephalus...... 75

Figure 5.1 All known flying-fox roost sites in the Lower Clarence region that were occupied during the period of licensed disturbances (April 1999 to December 2007) ...... 85

Figure 5.2 Roost habitat occupied by flying-foxes in the Maclean township ...... 87

Figure 5.3 Documented disturbance effort (person-hours) required to disperse flying-foxes from the Maclean Rainforest Reserve during the period of licensed disturbances (April 1999 to December 2007)...... 91

Figure A2.1 Distribution of the grey-headed flying-fox (Pteropus poliocephalus) in eastern Australia ...... 138

List of Figures xiv

Figure A2.2 Photo of a museum specimen stated to be a grey-headed flying-fox (P. poliocephalus) collected by A.J. Boyd in 1895 from the Herbert River in Qld . 138

Figure A10.3 Distribution of the flying-foxes in Australia ...... 152

List of Figures xv

List of Plates

Plate 1. Pteropus poliocephalus hanging at roost; and with a satellite transmitter attached ...... xxii

Plate 2. Urban flying-fox roosts in the Botanical Gardens of Sydney; and Woodend, Ipswich ...... xxiii

Plate 3. Author holding Pteropus poliocephalus while detangled from a mist net; and collaring an anaesthetised bat in the field...... xxiv

Plate 4. The North Stradebroke Island and Fraser Island capture sites...... xxv

Plate 5. The Stafford and Canungra capture sites...... xxvi

Plate 6. Disturbances of flying-foxes at Maclean; and a volunteer creating noise...... xxvii

List of Plates xvi

List of Appendices

Appendix 1 Data sources, time-period of records and number of records of Pteropus alecto and P. poliocephalus...... 135

Appendix 2 A re-evaluation of the northern distributional limit of the grey-headed flying- fox, Pteropus poliocephalus ...... 137

Appendix 3 Grid records for Pteropus alecto (N = 222) in coastal eastern Australia over four time-periods; 1843–1950, 1951–1990, 1991–2000 and 2000–2007...... 142

Appendix 4 The distribution of Pteropus poliocephalus (N = 368) in coastal eastern Australia in 50 x 50 km grids (‘grid records’) over four time periods; 1843–1950, 1951– 1990, 1991–2000 and 2000–2007...... 143

Appendix 5 Orientation of solar powered satellite transmitters on flying-foxes...... 144

Appendix 6 Data summary: individuals’ characteristics, distances moved and use of roost sites over several time-periods, for 14 satellite-tracked Pteropus poliocephalus. A ...... 145

Appendix 7 Frequency distribution of the weekly net displacement of all 13 individuals that had 12 or more weeks of data...... 148

Appendix 8 Data summary: individual’s characteristics, number of fixes and the feeding distances moved by 14 Pteropus poliocephalus at two different sampling units; all records and independent records...... 149

Appendix 9 Correlations (Pearson) between landscape attributes of roosts, feeding sites and random points in the landscape at two different sampling units; all feeding records and independent feeding records ...... 150

Appendix 10 Food for thought: Flying-foxes and bush regeneration ...... 151

List of Appendices

xvii

Acknowledgments

Supervisors and mentors

First and foremost I would like to thank my supervisors Professor Carla Catterall, Dr Peggy Eby and Dr John Kanowski for their constant encouragement, advice and friendship over the past six-plus years. I am deeply grateful for your intellectual input and forbearance through the duration of this PhD, without which this project would not have ever come to fruition. You were a truly wonderful supervisory team – thank you.

Thank you also to Dr Les Hall for his generosity of information, photos and for encouraging me to initially commence research on flying-foxes. He also opened up several opportunities for me at the beginning of my career including unforgettable field trips to Cairns (during a cyclone) and exploring the bat caves of Borneo.

Field work and technical support

I would like to mention Tim Holmes and Craig Walker from EPH for logistical support during the satellite-tracking component. John Kennedy and Allan Jeffery (OEH) also for supporting my research for three-plus years while I worked from Grafton NPWS office.

I am indebted to Dr Andrew Breed for field-work opportunities near Cairns, trapping and anesthesia advice and general bat chats. A huge thank you also to Craig Smith for providing initial advice on telemetry work, collar design, and the management and organisation of satellite data. Thanks to Guan Oon and Matthew Lecointe from Collecte Localisation Satellites (CLS) for additional Argos advice.

Many people assisted in the field with the trapping and collaring of flying-foxes. Thanks to Debbie Melville, Clare Hourigan, Tim Holmes, Annette Scanlon, Guy Bottroff, Trish Wimberley, Aki Nakamura, Drew Cook, Tahli Cook, Brian Roberts, Karen Roberts, Ivan Thrash and Linda Behrendorff. Debbie Melville also assisted greatly with the captive trials held at the Moggill Koala Hospital. Peter Theilmann and Allan McKinnon of Qld Department of Environment and Heritage Protection (DEHP) also provided invaluable technical help with anaesthetising animals and assisting with the original GPS collars (unfortunately these units were not viable for use on flying-foxes).

Acknowledgments xviii

Thank you to Dr Kerryn Parry-Jones and Dr Anja Divljan for additional advice on collar design, trapping and anesthetics. Anja also verified and provided advice on the identification of museum specimens. Murray Ellis and Michael Bedward, both of the NSW Office of Environment and Heritage (OEH), assisted with the ArcView script used in analyses on Chapter 2.

I am also grateful to the Lower Clarence flying-fox steering committee for their advice and expertise related to the management of the Maclean flying-fox roost (Chapter 5); Peter Baumann (NSW Department of Lands), Ken ‘Fox’ Laurie (Birrigan-Gargle Local Aboriginal Land Council), John Kennedy (OEH), Ian Tiley (Clarence Valley Council), Peter Wrightson (Valley Watch Inc.), Helen Tyas Tunggal (Valley Watch Inc.) and Dr Karl Vernes (University of New England).

Supplementary data

I am extremely appreciative to all data sources and collectors of flying-fox records for the analysis of range shifts in Chapter 2 including Dr Chris Tidemann, Dr Hugh Spencer, Dr Justin Welbergen, Dr Kerryn Parry Jones, Dr Stephan Klose, Dr Patrina Birt, Dr Les Hall, Tim Pearson, David Lowe, Greg O’Neill and Carol Palmer. Many of these records were from the Australia Bird and Bat Banding Scheme (ABBBS) and information was kindly coordinated by David Drynan. Various national and international museums provided additional records (see list of names in Appendix 1). Greg Richards provided personal records and records from Francis Ratcliffe. Peggy Eby provided numerous unpublished information on sightings of Pteropus alecto in NSW and abundance data from Lismore over 20 years.

I would also like to acknowledge the many people who contributed to the production of Chapter 5 by providing information related to the relocation of the Maclean flying-fox roosts and/ or usage of roost sites in the surrounding area including Gill Bennett, Carole West, Jennie Clowes, Bill Sansom, Mick Forester (Clarence Valley Council), Nigel Greenup (previously of Clarence Valley Council), and Mark Williams (formerly OEH). Thanks also to Joe Adair and Scott Sullivan (DEHP), Carol Palmer, Eddie Webber and John McCarthy (Northern Territory Government), staff at Billabong Sanctuary and Charters Towers Regional Council for providing information on relocation case studies elsewhere.

Acknowledgments

xix

Greg O’Neill and Mary Starky (both DEHP) provided roost location data for various sites in south-east Queensland and verified potential new roost sites used by tagged bats and the presence and abundance of known roosts – thank you for your assistance.

Significant others

Thanks for the support and friendship of Dr Adam Smith, all the wonderful ladies of Wildlife SOS, and the crew from carpool. These friendships have kept me laughing over the past several years. Vivien Jones for the use of her beautiful photographs and Louise Saunders for the illustrations throughout the thesis. A huge thanks to my parents for helping in any way they could throughout the project and for always believing that you should work with what you love (even if it makes you unpopular and sends you broke). Last, but not least thank you to my husband for supporting me over the many years and my beautiful children Tahli, Clay and Cedar – I love you all very much.

Funding

This study was funded by Griffith University and Queensland Department of Environment and Heritage Protection. Valley Watch Inc also contributed money to the research for Chapter 5. New South Wales National Parks and Wildlife Service (Grafton) provided additional in- kind support including use of vehicles, printing and office space.

Acknowledgments xx

Research permits and animal ethics

Three permits were required to observe, monitor and satellite track flying-foxes as part of this project including:

Organisation Permit applied for: Permit Date Number approved Griffith University Ethical Clearance to catch, release AES/ 17/ Nov 06 Animal Ethics and tag bats in Australia (including 06/AEC Committee during times of relocation attempts) NSW National Parks Scientific Licence for the Purpose of S12240 March 07 and Wildlife Service Science, Education or Conservation Qld Department of Scientific Research and Educational WISP04268207 Feb 07 Natural Resources Purposes Permit

Research permits and animal ethics xxi

Publications produced from this research

Included in Chapters 2, 3 and 5 of this thesis are published papers that are co-authored with other researchers. I was principally responsible for conducting all the research reported within these papers, and wrote, drafted and revised all papers for publication. However, each of these papers was also written with the support of my supervisors; Professor Carla Catterall (Griffith University), Dr Peggy Eby and Dr John Kanowksi. All of whom provided intellectual input, statistical guidance, and critical feedback on each manuscript. Therefore, they have been included as co-authors on each in recognition of their contribution. In Chapter 5, Gillian Bennett provided historical information and population counts for Maclean and therefore was also added as a co-author. The bibliographic details for these papers are:

Chapter 2: Roberts B.J., Catterall C.C., Eby P. and Kanowski J.K. (2012) Latitudinal range shifts in Australian flying-foxes: a re-evaluation. Austral Ecology, 37: 12–22.

Chapter 3: Roberts B.J., Catterall C.C., Eby P. and Kanowski J.K. (2012) Long-distance and frequent movements of the flying-fox Pteropus poliocephalus: implications for management. PloS ONE, 7(8): e42532. doi:10.1371/journal.pone.0042532.

Chapter 5: Roberts B.J., Eby P., Catterall C.C., Kanowski J.K. and Bennett G. (2012) The outcomes and costs of relocating flying-fox camps: insights from the case of Maclean, Australia, pp. 277-287 in The Biology and Conservation of Australasian Bats, edited by B. Law, P. Eby, D. Lunney and L. Lumsden. Royal Zoological Society of NSW, Mosman, NSW, Australia.

Appendix 2: Roberts B.J., Catterall C.C., Kanowski J.K. and Eby P. (2008) A re-evaluation of the northern distributional limit of the Grey-headed Flying-fox, Pteropus poliocephalus. Australasian Bat Society Newsletter, 31: 16-19.

Appropriate acknowledgements of those who contributed to the research but did not qualify as authors are included in each published paper and in the thesis acknowledgments (p. xvii). An additional research note that I co-authored has also been included in the Appendix. The bibliographic details for this are:

Appendix 10: den Exter K., Roberts B.J., Underwood A. and Martin L. (2011) Food for thought: Flying-foxes and bush regeneration. Big Scrub Landcare Newsletter, Lismore.

Publications produced from this research xxii

Plate 1. Pteropus poliocephalus hanging at roost (above, © B. Roberts); and with a satellite transmitter attached (below, © DEHP).

Plates xxiii

Plate 2. Urban flying-fox roosts in the Botanical Gardens of Sydney (above); and Woodend, Ipswich (below). Photos © Steve Parish collection.

Plates xxiv

Plate 3. Author holding Pteropus poliocephalus while detangled from a mist net (above); and collaring an anaesthetised bat in the field (below). Photos © DEHP taken in 2008.

Plates xxv

Plate 4. The North Stradbroke Island (above) and Fraser Island (below) capture sites. Image © Google Earth.

Plates xxvi

Plate 5. The Stafford (above) and Canungra (below) capture sites. Image © Google Earth.

Plates xxvii

Plate 6. Disturbances of flying-foxes at Maclean in 1999 (above); and a volunteer creating noise (below). Photos © G. Bennett.

Plates

Chapter 1 – General Introduction

1.1 Animal movement in dynamic landscapes

Ecology has been defined as the “scientific study of the distribution and abundance of organisms” (Andrewartha 1961), or more precisely as the “scientific study of the interactions that determine the distribution and abundance of organisms” (Krebs 2001). While few ecological studies are trivial, given the multitude of factors that may interact to influence patterns of distribution and abundance, studies of highly mobile animals are particularly demanding given variations in the factors that influence habitat suitability across large spatial scales.

Mobile animals exhibit a range of responses to variations in resource availability and other environmental factors (Gauthreaux 1982; Travis and Dytham 1999). In Australia, highly mobile animal taxa (birds and bats) have evolved large-scale, often complex movement patterns in response to the largely irregular and ephemeral patterns of resource availability characteristic of much of the continent (Chan 2001; Kingsford and Norman 2002; Traill et al. 2010). Many species exhibit a combination of migratory, nomadic and sedentary behaviour, depending on the spatial and temporal availability of resources (Eby 1996; Chan 2001).

For the purposes of this thesis, migration is defined as the periodic (usually bi-annual) movement to and from spatially disjunct seasonal ranges (Chan 2001; Roshier and Reid 2003; Mueller and Fagan 2008). Migratory species or populations usually inhabit landscapes with regular seasonal fluctuations in environmental conditions; migration is a widespread behaviour in many vertebrate and flying invertebrate taxa (Mueller and Fagan 2008). Sedentary or resident animals are those that remain within the same locality (as relevant to the scale of movement exhibited by a species) throughout the year or otherwise defined time period (Chan 2001; Roshier and Reid 2003; Mueller and Fagan 2008). Landscapes with little spatial or temporal variation in resource availability typically facilitate resident behaviour (Mueller and Fagan 2008). Nomadism, in contrast, refers to the behaviour of animals that are neither resident or migratory, but instead move across landscapes in routes that do not repeat faithfully each season or year (Mueller and Fagan 2008). Nomadic movements occur when resources are unpredictable in both space and time (Mueller and Fagan 2008).

Chapter 1 – General Introduction 2

Furthermore, many species cannot be clearly categorised as sedentary, migratory or nomadic (Roshier et al. 2008). For example, while almost 40% of landbirds breeding in Australia undertake migratory movements, a large proportion of these species include both migratory and resident populations (Chan 2001). There is increasing evidence of variation in movement patterns within species and amongst apparently ecologically-similar species occupying common landscapes (e.g. water birds, Kingsford and Norman 2002; Roshier et al. 2008). One of the current challenges for animal ecology - and therefore conservation and management - is the development of a better understanding of the range of movements undertaken by highly mobile species, particularly those that occupy landscapes where resources vary widely in time and space, and determining how these movement patterns are influenced by resource availability and behavioural factors.

1.2 Managing long-distance movements

Many vertebrates, including as noted above many species that occur in Australia, have the capacity to undertake long-distance movements, particularly those animals that can fly. For example, many species of birds are known to undertake journeys of thousands to tens of thousands of kilometres (e.g. Berthold 2001; Kingsford and Norman 2002; Gill et al. 2009). Many bats also undertake long-distance movements, although it is less common for bats to travel distances of more than a thousand kilometres (Fleming and Eby 2003). Birds, bats and other vertebrates that undertake large-scale movements do so to increase their access to mates, food and other resources, and to track favourable environmental conditions; the particular factors driving such movements may differ between species, as well as between sexes and age classes within species (Berthold 2001; Fleming and Eby 2003; Newton 2007).

The capacity for long-distance movement enables some species to access widely spaced and temporally variable food resources, while roosting in habitats and areas which differ from those used for feeding. Often, such species roost in colonies. Coloniality is common in birds, where about 13% of species roost in colonies and exploit spatially separated feeding sites (Rolland et al. 1998). For example, Northern Gannetts (Morus bassanus) roost in large breeding colonies on cliffs and rocky islands off the coasts of Great Britain and Ireland, while foraging up to 180 km from their colonies to obtain daily food resources (Montevecchi et al. 2002).

Chapter 1 – General Introduction 3

Most megachiropteran bat species (family Pteropodidae) are also colonial, roosting together during the day in groups of varying sizes and flying out to feeding sites at night (Pierson and Rainey 1992; Mickleburgh et al. 1992). In Africa, the straw-coloured fruit bat (Eidolon helvum) travels distances of more than 15 km from its colonial roosts (which can number into the millions) to feed on locally abundant fruit (Richter and Cumming 2006). A capacity for long-distance movement increases the resources and habitats available to bats and other mobile species at the cost of increased energy expenditure, vulnerability to predation during movements and time allocated to finding food in new habitats (Kunz 1982; Karasov 1992).

Establishing patterns of movements of highly mobile, colonially roosting species is crucial to understanding their ecology, life history and behaviour, and a prerequisite for their effective conservation and management. For example, species that move long-distances may be particularly sensitive to habitat destruction, not only because of the loss of resources at a local scale, but also because it increases the distances between remaining resources (Price et al. 1999; Warren et al. 2001; Wilcove and Wikelski 2008). For a successful conservation program, the species entire range (i.e. feeding and roosting locations) and stopover areas need to be considered. However, large-scale and frequent movements make the tracking of individuals and populations difficult. Therefore, knowledge of the key resources that require protection throughout a species’ geographical range is often limited. Conservation of these species is further complicated when movements occur across areas managed by different governments or agencies (e.g. Martin et al. 2007; Fleming and Eby 2003; Epstein et al. 2009).

1.3 Ecology of Pteropus – a highly mobile genus

1.3.1 Status and distribution

Flying-foxes (Old World fruit bats of the genus Pteropus) are large-bodied bats. With 61 species, Pteropus is the largest of the 42 genera represented in the Family Pteropodidae. The majority (around 63%) of species of Pteropus are highly colonial, often roosting in large groups numbering into the hundreds or thousands (Pierson and Rainey 1992; Mickleburgh et al. 1992; IUCN 2012). Some flying-foxes are considered to be highly mobile, moving daily between spatially separated feeding and roosting sites (in the order of tens of kilometres apart), and over longer time scales (weeks and months) moving frequently among different roosts (sometimes hundreds of kilometres apart) (Pierson and Rainey 1992; Mickleburgh et al. 1992; Breed et al. 2010a).

Chapter 1 – General Introduction 4

Flying-foxes inhabit the tropics and subtropics of Asia (including the Indian subcontinent), Australia, the Indonesian archipelago, islands off East Africa (but not mainland Africa), and a number of islands in both the Indian and Pacific Oceans (Rainey and Pierson 1992). Around 85% of flying-fox species are confined to a single island or group of islands, whereas seven species occur across large continental areas (four in Asia and three in Australia) (Pierson and Rainey 1992; Mickleburgh et al. 1992). Information on the movement capabilities of many Pteropus within oceanic islands is unknown, but it has been suggested that they are less mobile than species that occur on large continents (Pierson and Rainey 1992; Mickleburgh et al. 1992). The distributions of Pteropus species may be affected by recent changes in habitat and climate (Mickleburgh et al. 1992; Hughes 2003). However, knowledge of the distributions of flying-foxes is often based on limited information, for example specimens from museum collections which for many species are incomplete and may not reflect actual distributions (Mickleburgh et al. 2002).

Many Pteropus have undergone decreases in population size in recent times due to one or more of the following factors: overhunting, habitat loss, disturbance at roost sites and persecution at feeding sites (Mickleburgh et al. 1992; IUCN 2012). Currently, half of the world’s Pteropus species are classified as threatened by the IUCN (five are critically endangered, eight endangered and 18 vulnerable; IUCN 2012). Another nine species lack the basic data required to be able to assess their status (IUCN 2012). An additional four species are considered extinct (IUCN 2012).

1.3.2 Roosting behaviour and habitat requirements

Roost sites play a key role in the ecology of flying-foxes as they provide resting habitat and sites for social interactions (Kunz and Fenton 2003). Activities which may occur at these roosts include courtship and mating, mother-infant interactions, territorial defence, grooming and resting (Pierson and Rainey 1992; Kunz and Lumsden 2003). Flying-foxes spend most of the day within their roost sites, generally between the hours of dawn and dusk (Kunz 1982), although on occasions, individuals may return to the roost before dawn. For example, in Australia, adult male P. poliocephalus are known to return to the roost within a few hours of departure to defend territories during the mating season (Welbergen 2011).

The genus Pteropus typically roost openly on the branches of emergent trees or within forest canopies (Pierson and Rainey 1992; Mickleburgh et al. 1992). Only a few exceptions to tree

Chapter 1 – General Introduction 5 roosting have been reported: Pteropus alecto has been found roosting in a natural limestone tower in northern Australia (Stager and Hall 1983) and the extinct P. subniger of the Mascarene Islands roosted in caves, rock clefts and tree hollows (Cheke and Dahl 1981). In large flying-fox colonies, roost sites may include a number of adjacent trees (Ratcliffe 1931; Pierson and Rainey 1992). Roost site fidelity is generally high among communally roosting Pteropus (Mickleburgh et al. 1992), and some roost sites have documented histories of several decades. For example, roosting sites of P. vampyrus in the Philippines that first were reported in the early 1900s were still in use a century later (Mickleburgh et al. 1992; Brooke et al. 2000). Roosting sites of P. giganteus in India and of P. tonganus in American Samoa have been in use for at least 60 years (McCann 1934; Brooke et al. 2000), and several roost sites of P. poliocephalus in Australia have been used repeatedly for more than 80 years (Lunney and Moon 1997; West 2002).

From the limited information available it appears that Pteropus species roost in a wide variety of landscape and vegetation types within their ranges (Tidemann et al. 1999; Brooke et al. 2000; Mildenstein et al. 2005). Most information on the roost habitat of flying-foxes comes from Australia, where colonies form near food sources and individuals migrate to follow temporal shifts in fruit and flower resources (e.g. Eby 1991a; Richards 1990; Birt 2005). Pteropus alecto and P. poliocephalus from Australia roost in lowland coastal areas in rainforest, mangroves and other dense riparian vegetation (e.g. Loughland 1998; Tidemann 1999). In Malaysia and Indonesia, P. vampyrus has been recorded in mangrove and lowland forests (Heideman and Heaney 1992). Little is known about roosting behaviour of Pteropus species on islands except that colony size and the characteristics of roosting sites may vary among species greatly on different islands and are influenced by the amount of hunting pressure (Wilson and Graham 1992; Brooke et al. 2000; Wiles and Brooke 2009). For example, in American Samoa, roosts of P. tonganus are located in trees on cliff faces above the ocean or on steep mountainsides, locations that are either inaccessible to people or in protected areas where hunting is not allowed (Brooke et al. 2000). The roosting ecology of solitary flying-fox species is essentially unknown because they are often cryptic and hard to distinguish within their roost vegetation (Mickleburgh et al. 1992; Pierson and Rainey 1992).

The specific criteria that Pteropus species use to select roost sites are poorly understood (Kunz and Lumsden 2003). However, some habitat characteristics such as canopy structure, surrounding physical features and location of feeding habitat in relation to the roost appear to

Chapter 1 – General Introduction 6 be important (Kunz and Lumsden 2003). For example, the presence of waterways and nearby food resources appear to be major factors influencing roost selection in Australian Pteropus (Richards 1990; Loughland 1998; Tidemann et al. 1999; Eby 2002b; Roberts 2005). Canopy height and height of emergent roost trees were also found to be important variables explaining roosting sites of P. poliocephalus and P. alecto in Australia (Tidemann et al. 1999; Roberts 2005). A review of Pteropus worldwide by Pierson and Rainey (1992) suggested that protection from strong winds and access to updraft for flight were also important roost features.

Species of Pteropus show a range of tolerances to the alteration of their habitat by humans. In the Philippines P. vampyrus has been recorded roosting in commercial orchards (Heideman and Heaney 1992) and Thailand’s P. lylei roosts in trees within the grounds of Buddhist temples (Brown 2007). All four species of Australian flying-foxes (Birt et al. 1998; Hall and Richard 2000) and P. giganteus in southern India roost in both rural and urban areas (Molur et al. 2008). By contrast, some species such as P. hypomelanus from the Philippines show a strong preference for undisturbed forest types away from human activities (Mildenstein et al. 2005). It has been suggested that Australian flying-foxes in recent decades have been more frequently roosting and feeding in urban areas, due to both urban encroachment on traditional roosts and increased availability of urban food resources (Birt et al. 1998; Markus 2001; Parris and Hazell 2005). By contrast, on the Pacific islands, where there is active hunting, bats are extremely wary of people, roost in inaccessible locations, and abandon sites when disturbed by humans (Wilson and Graham 1992).

1.3.3 Feeding behaviour

A review of flying-fox ecology conducted in the early 1990s reported that baseline feeding information was available for around half the species within the genus Pteropus (Pierson and Rainey 1992), and little has changed since that time (Mickleburgh et al. 2002; Mildenstein 2002). The species that have been studied feed mainly on fruits and flowers (and sometimes leaves) from a diverse range of plants (>92 genera) (Marshall 1985; Mickleburgh et al. 1992; Pierson and Rainey 1992; Eby and Law 2008). Many Pteropus species rely heavily on figs in their diet; figs often bear abundant fruit for extended periods, and trees in an area often fruit asynchronously (e.g. Mickleburgh et al. 1992; Dumont 2003). Most other plant species used by feeding flying-foxes are more synchronous and seasonal in their production of fruit and flowers (Mickleburgh et al. 1992). Across their ranges, flying-foxes have also been successful

Chapter 1 – General Introduction 7 at exploiting a number of introduced plants and cultivated fruit as food resources (Marshall 1985; Wiles and Fujita 1992). Pteropus species contribute to the pollination and seed dispersal of more than 289 commercially and ecologically important plant species, including tropical hardwood trees (Fujita and Tuttle 1991; Utzurrum 1995; Eby 1996; Hodgkison et al. 2003; Southerton et al. 2004).

Most Pteropus are almost exclusively nocturnal, leaving their roosts at dusk to feed and typically not returning until dawn. Diurnal feeding activity may occur under unusual circumstances such as in the aftermath of cyclones, e.g. P. tonganus in Samoa (Pierson et al. 1996) and P. niger on Mauritius (Cheke and Dahl 1981), or as a more regular feature in the behaviour of some island taxa, e.g. P. samoensis in Samoa (Thomson et al. 1998) and P. melanotus on Christmas Island (Tidemann 1985).

Pteropus tend to feed on conspicuous, clumped and locally abundant food resources (Marshall 1985), and will often form noisy feeding groups, with intense displays of competition (Pierson and Rainey 1990). Australian flying-foxes can remain within a single feeding area for several weeks, in which long-term feeding territories may be established (McWilliam 1986; Eby 1996). Large aggregations of Australian flying-foxes at roost sites may be associated with an abundance of food such as flower pulses from nectar-rich Eucalyptus trees (Parry-Jones and Augee 1992; Eby 1991a; Eby 1996).

1.3.4 Movement capability

The amount of available information about flying-fox movements has increased in the last 20 years (e.g. Eby 1991a; Spencer et al. 1999; Epstein et al. 2009; Breed et al. 2010a). Daily, flying-foxes move between roosts and feeding sites. Some species typically roost singly close to food resources (e.g. P. samoensis in the South Pacific, Banack 1998; Brooke et al. 2000), whereas others may roost in large colonies and move distances of tens of kilometres to feed (e.g. Australian Pteropus, McWilliam 1986; Eby 1991b). Henceforth, these daily movements will be referred to as ‘feeding movements’.

The feeding areas used by flying-foxes are almost always separated from their roosting areas (Pierson and Rainey 1992; Mickleburgh et al. 1992). On large land masses, flying-foxes have been recorded moving one-way nightly distances up to 50 km from roosts to feeding sites (Marshall 1985; Eby 1991a; Pierson and Rainey 1992). Flying-foxes on islands are reported

Chapter 1 – General Introduction 8 as feeding more locally (Pierson and Rainey 1992). However, island flying-foxes are underrepresented in the literature and P. tonganus in America Samoa has been recorded travelling up to 47 km between feeding and roosting sites (Banack and Grant 2002).

Over a period of days and weeks, individual flying-foxes may move between different roost sites, sometimes tens to hundreds of kilometres apart (e.g. Pierson and Rainey 1992; Eby 1996; Spencer et al. 1999). However, the extent of movements between roosts is unclear as previous telemetry studies have typically only examined movements on weekly or fortnightly scales (Eby 1996; Tidemann and Nelson 2004). For example, two individual P. poliocephalus showed frequent interchange among several roost sites tens of kilometres apart over time- periods of seven or more days (Tidemann and Nelson 2004). Henceforth, these movements among roosts will be referred to as ‘inter-roost movements’. Over longer periods, some individuals may migrate hundreds to thousands of kilometres (Eby 1991a; Epstein et al. 2009; Breed et al. 2010a). Henceforth, net displacement (the shortest path between an individual’s first and final roost sites in a time-period) of over 300 km in a single month will be referred to as ‘long-distance movements’. Cumulative displacement (the sum of all recorded distances between consecutive roost sites) of up to 2000 km among roost sites in a single year have been recorded for an Australian flying-fox (P. poliocephalus, Tidemann and Nelson 2004). Two separate studies of P. vampyrus and P. alecto in south-east Asia showed cumulative movements of hundreds of kilometres within a year, including across international boundaries (Epstein et al. 2009; Breed et al. 2010a).

Despite these recent contributions to the understanding of flying-foxes’ movement capabilities, movement patterns remain poorly known for most species, particularly across broad scales. This is mainly due to the difficulty of monitoring larger-scale movements. Most movement studies have used techniques of banding individuals or radio-tracking (e.g. Nelson 1965; Eby 1991a; Markus and Hall 2004; Mildenstein et al. 2005). The limitation of these methods is that they require both initial capture and the recapture/ resighting of specific individuals or to be located using antenna and receiver; a difficult task as flying-foxes often roost in dense vegetation or inaccessible locations, and their whereabouts are often unpredictable and vary across long distances, between seasons and years (Nelson 1965; Tidemann and Nelson 2011). Despite these limitations, Nelson (1965) used dye sprayed from a light aircraft to mark around 2,000 P. poliocephalus, which revealed two individuals moving 100 km between roosts over times of three months in eastern Australia; based on

Chapter 1 – General Introduction 9 sightings reported by members of the public. Radio-tracking is labour intensive, but works well for local-scale studies (say, distances <50 km) (Kenward 2001). Eby (1991a and 1996), however, overcame some of these limitations by tracking P. poliocephalus from light aircraft, which revealed net displacements of over 610 km in 32 days as well as cumulative movements of up to 1800 km over 6 months for some individuals.

Since the 1990s, satellite telemetry has revealed the scale and complexity of the movements of many highly mobile animals (e.g. Cohn 1999; Shimazaki et al. 2004; Higuchi et al. 2005). Over that time, satellite transmitters have become increasingly lightweight and therefore more suitable for the study of bird and bat species (Tidemann and Nelson 2004; Wikelski et al. 2007). Satellite telemetry allows locations to be recorded remotely at relatively high spatial precision over large areas, repeatedly over a long time-period. However, this technology remains relatively expensive to purchase and deploy (Thomas et al. 2011). Since 2000, several studies have used satellite telemetry to monitor the movements of flying-foxes (i.e. Tidemann and Nelson 2004; Richter and Cumming 2008; Epstein et al. 2009; Breed et al. 2010a). The first satellite study by Tidemann and Nelson (2004) involved two individual P. poliocephalus, which both moved cumulative distances >2000 km and traversed four degrees of latitude (approx. 440 km) in Australia during one year. Epstein et al. (2009) satellite tracked seven adult male P. vampyrus and showed that these flying-foxes were highly mobile, travelling cumulative distances of hundreds of kilometres between roosting sites within a year and occupied home ranges that extended beyond Malaysia to include Indonesia and Thailand. Breed et al. (2010) used satellite telemetry on nine flying-foxes of three species (P. alecto, P. vampyrus and P. neohibernicus) from six different locations in Australia, Papua New Guinea, Indonesia, and Timor-Leste, which were recorded for a median 120 days (range 47–342) days with a median total cumulative distance travelled of 393 km (range 79–3,011 km) per individual. Richter and Cumming (2008) tracked four African straw-coloured fruit bats (Eidolon helvum) and demonstrated feeding movements as far as 59 km from the roost, net displacements of 370 km per night and cumulative distances of up to 2,518 km in 149 days.

1.3.5 Management of Pteropus

Flying-foxes across their range regularly come into conflict with humans for three main reasons. First, their feeding behaviour leads them into conflict with domestic and commercial fruit growers (Mickleburgh et al. 1992; Waples 2002). In areas where fruit is grown on a commercial scale and where fruit trees have replaced native forest, such as in parts of

Chapter 1 – General Introduction 10

Australia, India, Malaysia and Indonesia, flying-foxes have been the target of large-scale eradication campaigns (Mickleburgh et al. 1992; Hall and Richards 2000; Epstein et al. 2009). For example, in Malaysia, unrestricted culling of flying-foxes (P. vampyrus and P. hympomelanus) has been permitted as they are considered to be agriculture pests in fruit orchards (Epstein et al. 2009). In India, all five species of flying-fox present have been classed as ‘vermin’ due to the damage they can cause to fruit crops, enabling their unrestricted capture and killing (Singaravelan et al. 2009). Damage is caused when flying-foxes bite into fruits, or scratch their surfaces, making the fruit unmarketable. The level of fruit crop damage varies considerably among locations and years (Mickleburgh et al. 1992; Eby 1995). In Australia, cases of extensive use of commercial crops by flying-foxes have been linked with times when the availability of native food sources is low (Tidemann and Nelson 1987; DECCW 2009).

Second, flying-foxes are reservoirs of a number of zoonotic diseases which can infect livestock and humans, including newly described zoonotic viral diseases (e.g. Hendra and Nipah virus: Fraser et al. 1996; Halpin et al. 2000; Johara et al. 2001). These viruses can cause significant morbidity and mortality in humans and domestic animals such as pigs and horses (Field and Kung 2011). Since two viruses (Lyssavirus and Hendra virus) were discovered in Australian flying-foxes in the mid-1990s (Fraser et al. 1996; Halpin et al. 2000) there has been increased research into viruses associated with bats worldwide (Breed et al. 2010b). In Australia, the discovery of these bat associated viruses has also raised a negative profile of flying-foxes in the media (West 2002; Lunney and Moon 2011), with some commentators and politicians advocating that flying-foxes be reduced in number, either by shooting them or by moving them away from particular roost sites (West 2002; Hyne 2010; Lunney and Moon 2011). Pteropus in Thailand have been killed due to the perceived threats of retroviral disease transmission to humans; in addition to their persecution due to superstition (Brown 2007).

Third, the proximity of flying-fox roosts to human settlements can cause problems because of the noise and smell associated with roosts (Mickleburgh et al. 1992; Hall and Richards 2000; Eby and Lunney 2002a). This is particularly an issue for species that are strongly colonial (Mickleburgh et al. 1992). Some pre-existing roosts have become surrounded by urban development, while in other cases flying-foxes have set up new roosts in existing urban or suburban areas. For example, in Indonesia and Australia, planted trees such as in botanical

Chapter 1 – General Introduction 11 gardens in cities have provided new roosting opportunities for species such as P. vampyrus and P. poliocephalus (Mickleburgh et al. 1992; Richards 2002). In India and Pakistan, P. gigantus roosts in large colonies of hundreds to thousands of individuals in large trees in rural and urban areas, close to agricultural fields, ponds and by the sides of roads (Molur et al. 2008). In Australia, the level of conflict that arises has been related to the distance between flying-fox roosts and areas of human activity, and to the number of individuals in the roost (Eby and Lunney 2002b). Not all roosts near human habitation are sources of conflict and there are a number of examples of roosts in eastern Australia that are being managed successfully in urban settings (e.g. Pallin 2000; DECCW 2009).

Historically, people have used destructive management methods aimed at individuals or their roosts to manage conflicts. Methods have included the total removal of roost trees and draining of swamps inhabited by flying-foxes, shooting animals within roosts and while feeding, surrounding orchards with high-voltage electric grids, capturing animals at orchards and killing with chloroform, spraying animals with diesel, and the use of explosives and fire within roosts (e.g. Dolbeer et al. 1988; Mickleburgh et al. 1992; Tanton 1999; West 2002; Hall 2002). The aim of these actions has been to control or manage populations by either reducing population numbers or inducing the flying-foxes to move elsewhere. Following European settlement of Australia from the 1800s, shooting flying-foxes within their roosts was a common management practice to prevent damage to fruit crops, but this practice has been largely prohibited or restricted since the early 1990s (Ratcliffe 1931; Eby and Lunney 2002a).

Despite widespread use of these lethal techniques, flying-foxes have often continued to use roosts and feeding areas, perpetuating human-bat conflicts. Consequently there is a growing interest in the use of non-destructive methods of managing conflicts between flying-foxes and humans (Mickleburgh et al. 1992; Mickleburgh et al. 2002; IUCN 2012). In Australia, non- destructive techniques used to reduce crop damage from flying-foxes include the deployment of bright lights, scare guns, smoke, loud noise and bat distress calls (Eby and Lunney 2002a). Netting is effective in eliminating crop damage; however, its use is restricted because it is expensive to erect and maintain (Waples 2002). At roost sites, a variety of techniques have been used to harass the animals until they shift elsewhere, including the use of helicopters, bird-scare guns, smoke and loud continuous noise (Mickleburgh et al. 1992; Vardon et al. 1997; Tidemann 2002).

Chapter 1 – General Introduction 12

1.4 Australian flying-foxes

There are four Australian species of flying-fox: the little red flying-fox P. scapulatus, black flying-fox P. alecto, spectacled flying-fox P. conspicillatus and the grey-headed flying-fox P. poliocephalus. These species are all strongly colonial and roost in large aggregations which at times can exceed 100,000 individuals (Eby 1991a; Churchill 1998; Tidemann et al. 1999). In areas where their ranges overlap, these species may share daytime roost sites, although species are often stratified within the vegetation. For example, where P. scapulatus and P. alecto co-occur, P. scapulatus typically roosts lower in the vegetation, with P. alecto higher in the trees and at the roost periphery (Birt and Markus 1999; Roberts 2005). Roost fidelity is strong, with some of the roost locations described in the 1920s (Ratcliffe 1931) remaining in use in 2011 (pers. obs). Where flying-fox colonies occur near human habitation, residents have sometimes advocated for the flying-foxes to be relocated elsewhere (Birt et al. 1998; Hall and Richards 2000; Eby and Lunney 2002a). However, there has been frequent debate about the principle of relocation as well as the success of relocation methods in particular circumstances (Hall 2002; Tidemann 2002; West 2002).

Two of the Australian flying-fox species, P. alecto and P. poliocephalus, are similar in roost selection, diet and movement patterns (McWilliam 1986; Eby 1996; Tidemann 1999; Hall and Richards 2000; Markus and Hall 2004). These species also show substantial range overlap in eastern Australia, although they also have considerable parts of their ranges that are discrete. Both these species have been reported as undergoing distributional changes during the 20th century (Hughes 2003; Markus et al. 2008; Tidemann et al. 2008), with the southern range limit of P. alecto extending southward (Eby et al. 1999; Tidemann 1999; Markus et al. 2008), and both northern and southern limits of P. poliocephalus also being reported as shifting southward (Tidemann 1999; van der Ree et al. 2006; Tidemann et al. 2008). However, some of these inferences have been contested (van der Ree et al. 2006; DECCW 2009). Pteropus poliocephalus has been listed both nationally and internationally as Vulnerable resulting from the combined effects of habitat loss, agricultural control efforts, presumed competition with P. alecto and disturbance at roosts (Duncan et al. 1999; IUCN 2012).

1.5 Aims and structure of this thesis

The overarching aim of this thesis is to provide new information on the ecology of the grey- headed flying-fox (Pteropus poliocephalus), particularly its movement patterns. This study

Chapter 1 – General Introduction 13 uses satellite telemetry to examine the feeding movements and habitat use of P. poliocephalus across broad spatial scales. It tracks animals at a combination of a much finer temporal resolution (i.e. every few days) and over a longer time period (i.e., >6 months) than most previous studies. The methodology and results of this project are also relevant to the conservation and management of other wide-ranging flying-fox species, both within Australia and elsewhere.

More specifically, this thesis aims to:

• quantitatively re-assess the temporal dynamics of distributions of P. poliocephalus and its congener P. alecto in eastern Australia over 150 years, using historical locality records from a wide range of sources; • provide spatial and temporal information on inter-roost movements of P. poliocephalus across its range, using satellite telemetry; • quantitatively compare the selection of roosting and feeding habitat by P. poliocephalus, and describe its pattern of movement between feeding and roosting sites; and • examine the consequences of attempts to relocate flying-fox roosts across a range of sites in eastern and northern Australia and consider the effectiveness of such actions in resolving human–bat conflicts.

The thesis is divided into six chapters: four that address the four objectives listed above, this Introduction and a General Discussion. Chapters 2–5 are structured as manuscripts for publication.

Chapter 2 quantitatively re-evaluates the historical and present (from 1843 to 2007) distributions of P. poliocephalus and P. alecto in eastern Australia and considers the evidence that global warming has been the driver of distributional change.

Chapter 3 quantifies the pattern of inter-roost movement by P. poliocephalus at different spatial and temporal scales, using satellite telemetry of 14 individuals for up to nine months and an area spanning over 100,000 km2, and discusses the implications of the findings for management.

Chapter 4 quantifies the frequency distribution of feeding distances travelled during nightly feeding movements by P. poliocephalus, using satellite telemetry of 14 individuals. Chapter 4

Chapter 1 – General Introduction 14 also examines the landscape-scale factors associated with selection of both roost and feeding habitats.

Chapter 5 provides a quantitative summary of both the activities and financial costs involved in a series of public actions to relocate a flying-fox roost in the township of Maclean, eastern Australia. This Chapter also reviews the occurrence and outcomes of other relocation attempts, and considers the implications for relocation as a management tool to resolve conflict between humans and flying-foxes.

Chapter 6 summarises the major findings of the previous chapters and discusses the implications for current knowledge of flying-fox ecology and the effectiveness of different approaches to their management.

Chapter 1 – General Introduction 58

Chapter 4 – Feeding movements and landscape use by P. poliocephalus

4.1 Introduction

Understanding how species utilise landscapes is an important part of understanding the ecology of a species; this basic ecological information allows managers to identify areas and habitats that are particularly important for conservation of a species (Price et al. 1999; Berthold 2001; Fleming and Eby 2003). For highly mobile, colonially roosting species of flying vertebrates, identifying areas important for conservation is often complicated, because the habitats used for roosting and feeding are often spatially separated and may be chosen using different criteria (Berthold 2001; Kingsford and Norman 2002; Fleming and Eby 2003). Such species may also utilise distinct areas separated by hundreds or thousands of kilometres in the course of seasonal or annual cycles, as their feeding and roosting locations track the distribution of resources in the landscape (e.g. Roshier et al. 2001; Kingsford and Norman 2002). Highly mobile species can often tolerate some loss or alteration of habitat across their range because they are able to traverse areas providing few resources to reach feeding or roosting habitat (Law and Dickman 1998; Catterall et al. 1998; Fahrig 2003).

Australian flying-foxes (Pteropodidae) provide a good example of these issues. They have complex movement patterns because they feed on irregular and ephemeral resources (i.e. fruit and nectar) and form large communal day roosts often located many kilometres from feeding areas (Eby 1996; Markus and Hall 2004; Birt 2005). However, the specific criteria that flying- foxes use to select feeding and roosting sites and the factors predicting the distance animals will travel to feed are not well understood (Eby 1996; Kunz and Lumsden 2003; McDonald- Madden et al. 2005). For wide-ranging species, the landscape-scale habitat characteristics play an important role in their movement and site selection decisions; however, this also has not been an area of investigation for the highly mobile flying-fox.

Previous research into Australian flying-fox movements has utilised direct observations (McWilliam 1986; McDonald-Madden et al. 2005), banding techniques (Tidemann 1999), radio-telemetry (McWilliams 1986; Spencer et al. 1991; Eby 1996; Palmer and Woinarski 1999; Palmer et al. 2000; Markus and Hall 2004; Birt 2005) and, to a limited extent, satellite telemetry (Tidemann and Nelson 2004; Epstein et al. 2009; Breed et al. 2010a) to understand

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 59 the feeding behaviours of Australian flying-foxes. These methods have provided good baseline information, but with the exception of satellite telemetry are limited in their capacity to track the movements of individuals moving long-distances and therefore the habitats used by flying-foxes across broad spatial scales (see General Introduction). For example, radio- telemetry allows continuous, spatially accurate data to be collected throughout the night. However, the method is constrained to a relatively small study area, is biased toward relatively accessible habitat (as animals are generally tracked from the ground) and provides no information on study animals once they move out of the study region.

The recent availability of GIS data on land cover for Australian states, combined with developments in lightweight satellite-telemetry, provide an opportunity to quantitatively investigate the landscape scale characteristics of feeding and roosting sites of Australian flying-foxes across broad spatial scales. Satellite technology allows animals to be monitored through time regardless of their migratory movements, across all types of landscapes (unrestricted by accessibility) and across large spatial scales. Satellite telemetry has some limitations, including discontinuous data collection with limited control of timing, limited fine-scale spatial accuracy (McKeown and Westcott 2011) and lack of direct information on behaviour, as data are collected remotely. Despite these limitations, satellite telemetry has the potential to fill a number of knowledge gaps about feeding and landscape use of highly mobile species. This study uses satellite telemetry to improve knowledge of the broad scale feeding ecology and habitat use of Pteropus.

Specifically this study quantifies the feeding movements of P. poliocephalus, examines the landscape characteristics of their feeding and roosting sites and examines factors affecting the distance moved by individuals from roosts to feeding sites. Data from 14 satellite-tracked individuals collected over a period of two years and an area of 150,000 km2 are used to address the following questions:

(1) What are the landscape-scale habitat characteristics of roosts and feeding sites and how do they differ? (2) Do flying-foxes select roosts and feeding sites on the basis of landscape-scale habitat characteristics? (3) What distances are travelled between roosts and feeding sites?

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 60

(4) What are the roles of specific factors such as roost population size, duration of visits to feeding sites, size of forest patches, time of year, elevation and land cover in determining the feeding distances moved?

4.2 Methods

4.2.1 Capture and satellite telemetry

Fourteen adult male P. poliocephalus were fitted with satellite transmitters and released at four capture sites in subtropical south-east Queensland, Australia; in October 2007 and June 2008 as outlined in Chapter 3. The four capture points were located at Canungra (28.0oS, 153.2oE), Stafford (27.4oS, 153.0oE), Fraser Island (25.4oS, 153.1oE) and North Stradbroke Island (Dunwich) (27.5oS, 153.4oE). Study animals were sampled from the predominantly migratory or nomadic portion of the population (see section 3.2) by targeting: (1) roost sites used most of the year, but which had a large number of animals present at the time of capture in 2007, and therefore a high proportion of mobile individuals (Canungra and Safford, N = 4 individuals), and (2) seasonally used roost sites with large numbers of animals in 2008, where all animals were expected to be migratory or nomadic (Fraser Island and Dunwich, N = 10 individuals). The transmitters were programmed to a duty cycle of 10 hrs on alternating with 48 hrs off.

The raw data from the full transmission sequences of all 14 tagged flying-foxes comprised 4,356 location records, of varying presumed accuracy. Records for feeding sites were extracted using fixes that were obtained during the night, excluding times at dawn and dusk when flying-foxes are known to move between roost and feeding areas (the period one hour after sunset and before sunrise, data from the Geosience Australia website adjusted for geographical location). Cases where bats were recorded within 2 km of the day roost (which could have been due to low-accuracy records of night-roosting individuals) or cases where bats had returned to known day-roost locations before sunrise were excluded. From the resulting 1,913 feeding records, the 15% which fell within Argos accuracy classes A, B and Z were removed as they had no upper limit to their error margins, yielding 1,619 fixes for further analysis. An error in location accuracy of 2 km was assumed for all remaining fixes (LC>0) (McKeown and Westcott 2011).

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 61

An average of 3.1 night fixes of accuracy <2 km was recorded per 10 hour ‘on’ cycle (range 1–9, SD 1.4). These were mapped in ArcView 3.3, and manually scrutinised by overlaying geographical landmarks and known roost locations (Eby 2007; and data held by the author, P. Eby and management agencies).

4.2.2 Feeding sites

To exclude possible cases where the satellite fixes reflected larger-scale or migratory movements and to ensure that the roost location was known or reasonably assumed, records were only included in analyses if they consisted of sufficiently accurate position fixes at the same roost site on two consecutive days together with at least two sufficiently accurate night (feeding) fixes at the same place during the intervening night. Given the remote nature of satellite telemetry, it was not possible to confirm the behaviour of the animal at the time of individual night fixes (e.g. feeding or in flight). Feeding fixes were identified where two night fixes separated in time (by at least one hour) were located within an area of 2 km radius and more than 2 km from the roost. Each of these clusters of fixes is referred to as a flying-fox ‘feeding site’ and may have consisted of an individual feeding tree or a cluster of trees within that 2 km radius. The point locality of the feeding site was taken from the most accurate fix in the cluster (or in cases where there was more than one fix with the same accuracy, one was randomly chosen).

Radio-telemetry studies have shown that flying-foxes can use more than one feeding site per night, separated by several kilometres (Eby 1996; Birt 2005). In this study, the potential for identifying visits to different feeding sites within one night was restricted by uncontrolled technical considerations including the configuration of satellites and the level of charge in the battery. In circumstances where feeding sites were identified at two or more distinct time intervals and spatial locations on a given night, the site containing the most accurate fix was selected for analysis. Where there was more than one site with the same level of accuracy, one was selected randomly.

Fixes received from the same study individual at the same feeding site were treated as independent feeding sites if: 1) the feeding site was accessed from different roosting locations; 2) the feeding site was accessed from the same roost after an interval during which it had used a different feeding site; or 3) the feeding fixes were >7 days apart (an interval considered sufficiently long, given the movement patterns of flying-foxes (Chapter 3), to

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 62 constitute independent decisions by individuals about where to feed). Each resulting record, of a visit to feeding site in relation to a particular roost that was used on both the preceding and subsequent days, is termed a ‘feeding record’. There were 173 such feeding records (termed ‘all feeding records’) for which there was information on date and time, geographical coordinates, and accuracy (Argos Location Class) of the fix.

Some individuals were recorded at the same feeding site over several consecutive weeks. To examine any effect of non-independence of data collected from the same animal, consecutive records at the same feeding site from the same roost were also condensed into single records. This reduced the sample size to 112 ‘independent feeding records’, which were analysed separately from the dataset comprising all 173 feeding records.

From all 173 records, 110 were spatially distinct feeding sites (>2 km apart). This sample size differs slightly from the 112 independent feeding records as it does not incorporate the roost site used to access a given feeding site. Durations of visits by each individual to each of these 110 different feeding sites were calculated from data on ‘feeding visits’, defined by the dates of the first and last fixes in consecutive duty cycles from a particular individual at a particular feeding site (including some occasions when an individual used more than one feeding site per night). The visit duration was the elapsed number of days at that feeding site (including durations of one day only). Gaps in data collection of 2–4 days occurred due to the 48-hour ‘off’ segment of the duty cycle and dates when only day (roost) fixes were obtained. When a sequence of consecutive records at the same feeding site spanned these gaps, they were included in calculations of visit duration. Revisits to previously used feeding sites were counted separately; these occurred if an individual had meanwhile been recorded at other roost sites or for any time period had exclusively fed at a separate feeding site.

4.2.3 Roost sites

The 173 feeding records were associated with 45 different roost sites. This discrepancy occurred because: (1) multiple animals used the same roosting site; and (2) individuals used the same roosting site through time and to access different feeding areas. Roost sites were fixes that were either: (1) obtained during daylight hours (between sunrise and sunset, data from the Geosience Australia website adjusted for geographical location); or (2) cases where bats had returned to known roosts (Eby 2007; and data held by the author, P. Eby and management agencies) before sunrise. For each of the 173 feeding records, the name (if

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 63 known) and co-ordinates of the roost, the date when the individual arrived at and departed from each roost (see also Chapter 3), and the roost population sizes, were recorded. Roost population size data were compiled from static counts collected at most roosts on the third Friday of every month from September 2007 until the end of 2009 (unpublished data held by authors and the Queensland Environment Department). These roost population data were estimates made by researchers, wildlife carers and experienced government staff. Roost population data were available for 108 of the 173 feeding records. Time lags between roost estimates and feeding records ranged from 0 to 19 days.

4.2.4 Landscape measurements

To determine factors associated with the selection of roost and feeding sites, landscape attributes of those sites were compared with 100 stratified random points drawn from areas in which feeding and roosting were recorded, as described below. The 110 different feeding sites and 45 associated roosts were mapped in Google Earth Pro and a 20 km circle was drawn around each. This distance corresponds with the typical known nightly feeding distance of P. poliocephalus (Eby 1991a; Tidemann 1999); data from this study. Seven discrete clusters of sites were identified and a perimeter line was drawn around the outer boundary of all 20 km circles within each cluster (Figure 4.1). The number of random points selected within each defined region was determined by the proportion of feeding sites contained by that region (e.g. a region with 23 of the 173 weekly feeding sites was allocated 13% of the 100 random points; rounded off to the nearest unit). Two feeding sites and two roost sites were >100 km outside these seven discrete regions and were omitted from some analyses.

Four landscape attributes were measured at each of the three types of sites: feeding sites, roost sites and random sites. Landscape attributes were: (i) elevation (at the point co-ordinates of the site); and the percentages of three land cover categories; (ii) forest; (iii) built; and (iv) open within a 2 km radius (total area = 12.6 km2) of a site. For feeding sites, the size (ha) of the largest forest patch that fell in total or part within the 2 km radius was also measured.

Land cover measurements were taken from high-resolution aerial and satellite imagery in Google Earth Pro at an altitude of 4 km or less (accessed Nov–Dec 2011). The minimum size of any measured polygon was 5.0 ha. In cases when there were small amounts of a particular land cover scattered within a 2 km radius but the total amount was >5 ha a percentage was estimated. Forest refers to the amount of land that could be observed in the Google Earth Pro

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 64 imagery as continuous tracts of trees (crown cover >20%). Forest included both disturbed and intact stands of woody vegetation, regrowth and plantations (whether of native and exotic species). Built cover comprised built structures (e.g. human settlements ranging from suburban houses and gardens to highly urbanised areas) and impervious surfaces such as roads and industrial areas. Remaining types of land cover consisted mainly of agricultural land with scattered trees and bodies of water and were placed in the ‘open’ category.

4.2.5 Data analysis

To investigate intercorrelations among the four landscape attributes (land cover and elevation) at the 2 km scale, Pearson correlation matrices were calculated. The measured values of the four landscape attributes were compared among each of the three different types of sites using: (1) all 173 feeding records; and (2) the 112 independent feeding sites. Whether there was evidence for active selection for landscape attributes of either roost or feeding sites was tested by comparing their landscape values with those of the 100 random points, using Mann Whitney U-tests. Differences in landscape values between roost and feeding sites were tested with the Wilcoxon Matched-Pairs Signed-Rank test. Boxplots were constructed from both all 173 feeding records and 112 independent feeding records to describe the distribution of each of the four landscape measurements. Two roost and two feeding sites that fell outside the defined regions were excluded from these analyses.

For each of the 173 feeding records, the distance between the point locality of the feeding site and the centre of the associated roost site (feeding distance) was measured using the shortest straight path in Google Earth Pro. Quantitative summaries of frequency distributions of the feeding distances were made using either all feeding records or the independent feeding records as replicates. Analysis of variance (ANOVA) was used to test if the mean feeding distances differed between individuals, month and seasons. There were four seasons; summer (December–February), autumn (March–May), winter (June–August) and spring (September– November). Only individuals or months with more than 10 records were included in any of the feeding distance analyses. Pearson correlations were used to test for significance of relationships between the feeding distances of flying-foxes and the following attributes: roost landscape characteristics (at 2 km radii), roost population size (log transformed), feeding visit duration and feeding forest patch size. These analyses were conducted at four different levels of the dataset, which vary in breadth of focus, potential redundancy and units of replication: (1) all feeding records, (2) independent feeding records, (3) mean values for nine different

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 65 individuals with >10 feeding records, and (4) for each of two individual flying-foxes (Bats ‘5’ and ‘10’) which had large (>20) numbers of feeding records together with high variation in feeding distances.

4.3 Results

The 14 male P. poliocephalus used in this study were satellite-tracked from tagging to transmitter failure for a range of 13–277 days. The 173 feeding records were unevenly distributed across study animals and ranged from 1–24 per individual (average 12, SD 6.6; see Appendix 8). Approximately 97% of all feeding records had an Argos accuracy of <1.5 km (LC 1, 2 and 3) and 80% had an accuracy of <0.5 km (LC 2 and 3).

The recorded unique roost sites (N = 45) and discrete feeding sites (N=110) of study animals spanned a north-south distance of 1,065 km and an east-west distance of 138 km (Figure 4.1). Most records were concentrated broadly in three localities: around latitudes 24.5oS (14% of records), 25.5oS (22%), and 28oS (44%) (Figure 4.1).

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 66

0 24 Gladstone 100

250 Bundaberg 200

260 300

270 400 Brisbane 280 500

290

600 Kilometers

300

Coffs Harbour 700 Latitude(degrees south) 310 Port Macquarie 800

320 900 Newcastle 330 1000

Sydney 1520 Longitude (degrees east)

Figure 4.1 Map of the 45 different roost sites (triangles) associated with the 110 discrete feeding sites (circles) in use by 14 individuals of P. poliocephalus between October 2007 and April 2009. The east west line in the middle of map shows the border between New South Wales and Queensland. Polygons outline the seven discrete regions where random points were selected.

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 67

4.3.1 Habitat characteristics of feeding and roost sites

The study animals tended to roost and feed in landscapes characterised by high percentages of forested land and low percentages of built land, although the percentages of forest and built varied greatly, from <5% to >95% (Figure 4.2). Of the 45 roosts used by study animals, 40% were in areas where no built land occurred within 2 km of the site, whereas 20% were located in substantially built environments (>35% of the surrounding land) and 4% were embedded in highly urban (>45% built) landscapes. Also 69% of 112 independent feeding sites had no measurable built land cover within 2 km, compared with 7% that were in substantially built landscapes.

The patterns of difference in landscape characteristics between roost and feeding sites remained similar whether based on all or just the subset of independent records (Table 4.1, Figure 4.2). Roost sites had significantly less forest and more built land cover than feeding sites (Table 4.1, Figure 4.2). The elevation of roosting sites were significantly less than feeding sites (roost sites: median elevation 110 m; mean 101 m, SD 121; feeding sites: median elevation 99 m, mean 144 m, SD 138) (Table 4.1, Figure 4.2). Of the 171 records, 74% of roost sites were located at elevations <120 m, compared with only 58% of feeding sites, and 67% of 171 paired roost-feeding cases showed animals moving to higher elevations to feed.

Compared with random points, roosts were located at sites with less surrounding forest cover, and more built and open land (Table 4.1, Figure 4.2). In contrast, feeding sites were located in areas with less surrounding built cover, but with similar amounts of surrounding forest cover as random points in the landscape (Figure 4.2, Table 4.1). Neither the elevations of roosts nor feeding sites differed significantly from those in the random sample, due to the high variation of landscape data. When the inter-relationships of these landscape variables were examined there were a number of significant relationships (Appendix 9). However, most r values were not especially high (r < 0.5; i.e. r2 < 0.25) other than strong negative relationships between percentage open land and forest when feeding sites were considered (Appendix 9). Therefore, all variables were retained in the analyses.

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 68

(a) All records 97 73 82 100 50

80 40

60 30

40 Built % 20 % Forest%

20 10

0 0 R F L R F L 512 575 790 100 500

80 400

60 300

40 200

% Open% Elevation(m) 20 100

0 0 R F L R F L

(b) Independent records 97 73 82 100 50

80 40

60 30

40 Built % 20 % Forest%

20 10

0 0 R F L R F L 575 790 512 100 500

80 400

60 300

40 200

% Open% Elevation (m) Elevation 20 100

0 0 R F L R F L

Figure 4.2 Boxplots summarising the distribution (median, quartiles, range) of elevation (m) and the percentage of forest, built and open land within 2 km of roosts (R), feeding sites (F) and random points in the landscape (L) at two sampling units; (a) all records (R=171, F=171, L=100) and (b) independent records (R=110, F=110, L=100). Maximum values written above bars. Also see Table 4.1.

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 69

Table 4.1 A comparison of landscape attributes within 2 km radii of roosts (R), feeding sites (F) and random points in the landscape (L) at two different sampling units; (i) all feeding records and (ii) independent feeding records. Two roost sites and two feeding sites that fell outside the defined regions were excluded from this analysis. Table shows P values.

R vs. L1 F vs. L1 R vs. F2 Direction All feeding records3 % Forest 0.01 0.61 <0.001 F=L>R % Built 0.04 <0.001 <0.001 R>L>F % Open 0.05 0.37 0.68 R>L=F Elevation 0.27 0.14 <0.001 F>R=L* Independent feeding records4 % Forest 0.01 0.25 <0.001 F=L>R % Built 0.13 <0.001 <0.001 R=L>F % Open 0.05 0.85 0.03 R>F=L Elevation 0.45 0.28 0.006 F>R=L*

1 Mann-Whitney U- tests 2 Wilcoxon Signed-Rank test 3 All records; Roost = 171, Feeding = 171, Landscape = 100 4 Independent records; Roost = 110, Feeding = 110, Landscape = 100 * Based on median values (see Figure 4.2). Note that medians of the roost and feeding did not differ significantly from the landscape medians because of the high variation in the latter.

4.3.2 Movement between roosts and feeding sites

The feeding distances (i.e. distance from roost to feeding site) moved were typically (85%) less than 20 km (range 2–56 km) and were similar between all 173 feeding records and the 112 independent feeding records (Figure 4.3, Figure 4.4). However, there was a large amount of variation in the feeding distance moved, both within and between individuals (Figure 4.4). ANOVA tests showed statistically significant variation in mean feeding distance among the nine individuals with ≥10 feeding records when using all records (ANOVA F=3.085, P=0.003), but mean feeding distance was not significant among the five individuals with ≥10 independent records (ANOVA F=1.913, P=0.121) (Figure 4.4). LSD tests showed that Bats 2 and 4 differed significantly from Bats 9 and 11–14; although no clear pattern was seen when all records were considered.

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 70

40 (a) All records

Frequency (%) Frequency 10

0 <5 6-10 11-15 16-20 21-25 26-30 31-56 Feeding distance (km)

40 (b) Independent records

Frequency (%) Frequency 10

0 <5 6-10 11-15 16-20 21-25 26-30 31-56 Feeding distance (km)

Figure 4.3 Frequency distribution (%) of the feeding distances moved by the 14 P. poliocephalus; (a) all 173 feeding records (mean 12.3, median 9.8 km, SD 9.3 km); and (b) 112 independent feeding records (mean 13.4, median 10.9 km, SD 10.1 km).

Overall, the duration of time over which individuals revisited any particular feeding site was typically short, with 50% of feeding visits <5 days (Figure 4.5). However, the distribution of feeding visit durations was skewed, and 19% of visits were for periods >25 days (and up to 84 days, Figure 4.5). On 12 occasions, two different roosts were used by an individual bat to access the same feeding site.

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 71

60 (a) All records 50

Feeding distance (km) distance Feeding 10

0 0 1 2 * 3 4* 5* 6 7 8* 9 10* 11* 12* 13* 14* Bat

60 (b) Independent records 50

Feeding distance (km) distance Feeding 10

0 0 1 2 3 4* 5* 6 7 8 * 9 10* 11 12 13 14* Bat

Figure 4.4 Feeding distance (km) moved by each of the 14 P. poliocephalus; (a) all records and (b) independent records. Asterisks represent individuals with more than 10 feeding records that were included in analyses. Each point is the distance (km) separating the roost and feeding site. Solid lines show the mean for each data set. Bats ordered in rank-order of the mean feeding distances (all records). See also Appendix 8.

Using the 173 feeding records, study animals were recorded using more than one feeding site in a night on 54 occasions. In 13 of these, 3–5 feeding sites were used per night. The mean distance between successive pairs of within-night feeding sites was 7 km (SD 5 km, range 2– 21 km, N=54. Five fixes were received from one animal (Bat 8, 80188) as it migrated

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 72 overnight between roosts located 210 km apart, taking an indirect path, travelling at least 246 km, and making at least one feeding stop during the trip.

20 Frequency (%) Frequency 10

0 1-5 6-10 10-15 16-20 21-25 26-84 Days

Figure 4.5 Frequency distribution of the duration of feeding visits by 14 Pteropus poliocephalus (N = 110 visits to different sites). A feeding visit is the time from the first to last consecutive satellite fix for any individual at a particular site, with no data gaps of >5 days. Revisits were counted separately. Mean and median durations were 12 and 6 days, respectively.

4.3.3 Factors influencing distance moved

Feeding distance was significantly negatively correlated with the duration of feeding visits when all 173 feeding records were analysed, (r=-0.224, P=0.003) (Table 4.2, Figure 4.6). This relationship was no longer significant when using the subset of independent records (r=- 0.097, P=0.309, Table 4.2). However, across the nine individuals with sufficient data (i.e. with more than 10 feeding records) there was a negative correlation between feeding distance and the duration of feeding visits (r=-0.638, P=0.065) and a negative trend was also seen for Bat 5 (r=-0.368, P=0.077) (Table 4.2, Figure 4.6).

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 73

Feeding Log roost Feeding visit N forest patch population duration (days) (ha) Expected +,- - + All records1 173 0.216 -0.224* 0.085 Independent records2 112 -0.124 -0.097 0.114 Individuals 9 0.470 -0.638x 0.110 Bat 53 24 -0.071 -0.368x 0.096 Bat 104 21 0.288 -0.180 0.057

* P < 0.05; x Strong trend P <0.1 1 N = 173 for all correlations except roost population size, where N = 108 2 N = 112 for all correlations except roost population size, where N = 67 3 N = 24 for all correlations except roost population size, where N = 22 4 N = 21 for all correlations except roost population size, where N = 11

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 74

60 (a) All records 50

10 Feeding (km) Feeding distance

0 0 20 40 60 80

25 (b) Individual flying-foxes

5 Feeding (km) Feeding distance

0 0 10 20 30 40

35 (c) Bat 5

Feeding (km) Feeding distance 5

0 0 10 20 30 40 Feeding visit duration (days)

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 75

Feeding distance did not vary with month (Figure 4.7, ANOVA F=0.673, P=0.695) or season (ANOVA F=1.194, P=0.314). Neither elevation nor type of land cover surrounding roosts were significantly associated with the distances that flying-foxes travelled to feed (Table 4.3).

Variable name r P All feeding records % Forest 0.07 0.38 % Built 0.02 0.80 % Open 0.06 0.42 Elevation 0.03 0.68 Independent feeding records % Forest 0.05 0.62 % Built 0.03 0.75 % Open 0.09 0.35 Elevation 0.06 0.57

30 22 25 25 16 26 26 23 10 20 15 7 4 5 15 1 10

Mean feeding distance (km) distancefeedingMean 0 Dec Jan Feb Mar Apr May Jun Jul Aug Sep Oct Nov (6) (7) (4) (4) (2) (1) (5) (10) (9) (9) (11) (10)

Figure 4.7 Mean monthly feeding distances (+SD) of 14 Pteropus poliocephalus. Numbers above bars are sample sizes. Number of animals transmitting each month are in parentheses beneath the y axis.

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 76

4.4 Discussion

4.4.1 Roost sites

This study is the first to examine feeding distances and landscape use of flying-foxes using satellite telemetry. This technology allowed a more comprehensive assessment of the movements of animals than has been possible, due to the capacity to track movements in remote or otherwise logistically difficult areas.

While individual roosts were located in landscapes that ranged from highly urbanised areas (97% built) to substantial tracts of intact forest (100% forest), the majority were surrounded by mosaics of open, built and forested lands. Significant differences between the proportions of landscape attributes in the areas surrounding roosts and random points indicate that the animals were selective in the landscapes they used for roosting.

At roost sites P. poliocephalus selected landscapes with less forest cover and more open land than random, and these relationships were consistent in analyses of all feeding records and independent records. This trend might be associated with preference for roosting on level land or gentle slopes. Several previous studies have found the majority of P. poliocephalus roost sites in eastern Australia were on flat ground or that at least part of the roost site contained some level topography (<5o incline) (Eby 2002b; Peacock 2004; Roberts 2005). Clearing rates for urbanisation, agriculture and grazing have not been uniform across the east coast of Australia, with the steeper lands on hills and ranges retaining a higher proportion of their natural vegetation cover, whereas much of the vegetation along the flatter and more fertile coastal lowlands (< 100 m) has been cleared and fragmented (Catterall and Kingston 1993; Sattler and Williams 1999; Keith 2004).

When all feeding records were included in the analysis, flying-foxes used built areas for roosting at a significantly greater frequency than their occurrence in the environment; however, this preference was no longer significant when only independent records were included in analyses. Roberts (2005) found roost sites of flying-foxes (P. poliocephalus and P. alecto) in south-east Queensland were located in areas surrounded by a significantly greater proportion of urban development than was the case from random points. Roberts (2005) also found that roost sites used regularly by flying-foxes were surrounded, on average, by twice the amount of urban land, than those used less regularly. The weaker trend in the

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 77 present study may be explained by the use of satellite telemetry which provides better information on remote and inaccessible roost sites away from urban areas and reinforces the benefit of satellite telemetry in documenting movements across all landscapes.

Flying-foxes have been increasingly reported roosting in urban locations (e.g. Birt et al. 1998; Hall and Richards 2000; Hall 2002; Markus and Hall 2004; van der Ree et al. 2006). There is evidence that in some urban areas the numbers of roost sites are increasing (Birt et al. 1998; Hall 2002; Markus and Hall 2004; Roberts 2005) and that these sites may be used regularly by flying-foxes (Birt et al. 1998; Roberts 2005; van der Ree et al. 2006; Williams et al. 2006; this chapter). Nonetheless, this study has also shown that flying-foxes across their range will often roost outside urban areas. There is no evidence to suggest flying-foxes are abandoning rural locations to roost in urban areas, although, when present urban land appears to be a factor influencing roost placement at the local scale. Flying-foxes’ use of urban areas may have recently been over-emphasised because roost sites near built areas attract controversy (Eby and Lunney 2002a; Chapter 5), or because urban roosts are more readily documented than roosts in remote or inaccessible areas.

A number of studies have examined the characteristics of roost sites used by Australian flying-foxes (e.g. Richards 1990; Loughland 1998; Palmer and Woinarski 1999; Tidemann et al. 1999; Peacock 2004), although fewer have examined the landscape scale attributes of such sites (e.g. Roberts 2005). This study’s findings are consistent with previous observations that P. poliocephalus uses habitats with a wide range of tree cover characteristics for roosting (Tidemann 1999; Eby 2002b; Peacock 2004; Roberts 2005). The roost sites of P. poliocephalus are located within landscape types ranging from small remnant forest patches surrounded by open agricultural land to large tracts of continuous forest. In eastern Australia, P. poliocephalus appears to require forest patches at least 1 ha in size for roosting colonially in large groups (Eby 2002b; Roberts 2005).

This study did not find that elevation played a role in the selection of roost sites, however, flying-foxes did move to higher elevations to feed. Previous studies found a preference for roosts of Australian flying-foxes at low elevations (McWilliams 1986; Richards 1990; Tidemann et al. 1999; Eby 2002b; Peacock 2004; Roberts 2005). Again, it is possible that this difference reflects the capacity for satellite telemetry data to document movements across all landscapes. Roosts at high elevations are more likely to be found in areas easily accessible and roost locations are less likely to be recorded than that at lower elevations. In addition, it is

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 78 possible that the study did not have the statistical power to determine elevation preferences because of the high variability of elevation in the landscape data.

4.4.2 Feeding sites

Pteropus poliocephalus has previously been reported to use a variety of treed landscapes for feeding within its range (e.g. McWilliam 1986; Eby 1996; Parry-Jones and Augee 2001; McDonald-Madden et al. 2005), however, this is the first study where landscape characteristics of feeding sites have been systematically assessed. This is also the first study to look at preferences in feeding landscapes for flying-foxes. Consistent with previous suggestions (e.g. Parry-Jones and Augee 1991; Eby 1996; Markus and Hall 2004), this study found that the feeding sites of P. poliocephalus included areas of natural forest, disturbed forest, open areas with scattered trees and vegetation within the urban matrix.

Individual feeding sites were surrounded by landscapes that ranged from highly urbanised areas (82% built) to intact forest (100% forest). However, the majority comprised mosaics of landscape types. Pteropus poliocephalus was less selective of feeding landscapes than roosting landscapes. The proportions of forested and open land in the areas surrounding feeding sites did not differ from those surrounding random points. Nor was there evidence that P. poliocephalus selected feeding sites on the basis of elevation. However, there was a strong and significant negative relationship with the proportion of built land, suggesting the animals avoided built areas when feeding. This result was consistent in analyses of all records and independent records.

However, the flying-foxes tracked in this study showed no preference for feeding in large continuous tracts of forest. In urban areas, scattered native and exotic trees, small forest patches and larger remnants retained within the urban matrix provide feeding sites. Open areas were usually agriculturally altered landscapes containing scattered trees and thin strips of riparian vegetation. Regardless of the statistical preferences, the flying-foxes moved freely across modified and disturbed environments, to access individual productive trees in all habitats. The selection against built areas may reflect a lower density of productive trees there, although, further research would be needed to quantify likely food availability between forest, rural and urban areas. Potential differences in flying-fox habitat use between different regions, differing in the extent of urbanisation and forest cover, also warrant further investigation.

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 79

4.4.3 Comparison between feeding and roosting sites

There are alternative, but untested explanations why flying-foxes may prefer to roost in urban areas. First, some authors have concluded that an increased food supply provided by increase in garden and streetscape plantings of fruit and nectar-bearing trees could explain an increase in the occurrence of flying-foxes in urban areas (Parry-Jones and Augee 2001; Markus and Hall 2004; Birt 2005; McDonald-Madden et al. 2005; van der Ree et al. 2006; Williams et al. 2006). However, the present study has shown that when tracked across all landscape types, P. poliocephalus was primarily feeding away from built environments. This may be because food availability may actually be lower in urban areas, as discussed above. Second, the establishment of flying-fox roosts in urban areas may be driven by factors other than the availability of food. Since flying-foxes can travel tens of kilometres each night they do not need to locate roosts immediately adjacent to preferred feeding locations (also see Eby 1991a; Spencer et al. 1991; Law and Dickman 1998; Chapter 3). Urban areas may contain specific habitat features which make small urban forest remnants attractive as flying-fox roost sites. For example, highly illuminated features of urban areas such as roads and other infrastructure may make night time navigation by flying-foxes easier (Birt et al. 1998; Hall and Richards 2000). Alternatively, the persecution of flying-foxes by humans in rural areas (Lunney and Moon 1997; Hall and Richards 2000) may have led to the establishment of some roosts in human settlements. Other possible, speculative explanations for the apparent selection of built-up areas for roost sites include microclimate moderation, i.e. the urban ‘heat island’ effect (Parris and Hazell 2005), and the reduced likelihood of predation by some predators (e.g. raptors, varanids) in urban areas (Churchill 2008). Nevertheless, as flying is energetically expensive, reasonable proximity of roosts to food resources would be expected (as indeed was demonstrated in this study).

4.4.4 Factors influencing feeding movements

The extensive variation in the feeding distances of P. poliocephalus found in this study (2–56 km) is consistent with results of studies using both banding (Tidemann 1999; Tidemann and Nelson 2011) and radio-telemetry techniques (e.g. McWilliam 1986; Eby 1991a; Spencer et al. 1991; Eby 1996). Through the recovery of dead banded P. poliocephalus in urban Sydney, Tidemann (1999) concluded that 76% of flying-foxes foraged within 20 km of the roost, although the feeding range extending to 45 km. Spencer et al. (1991) reported roost-feeding site distances of 25 km for one flying-fox in regional Lismore and up to 17 km for two flying-

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 80 foxes in Sydney. Two additional radio-telemetry studies in Lismore reported direct distances between day roosts and feeding locations of up to 10 km (McWilliam 1986) and from 2.6 km to 37 km (Eby 1991b, 1996). When an animal’s entire flight path is tracked, flying-foxes can potentially travel considerably longer distances than their straight line path; with commuting distances of up to or greater than 50 km one way (Eby 1991a).

Similar feeding distances have been found in other species of flying-fox. Based on radio- tracking data, studies have found that P. alecto in northern and eastern Australia generally roosted within 15 km of feeding sites (range 0.1–29.3 km, McWilliam 1986; Palmer and Woinarski 1999; Palmer et al. 2000; Markus and Hall 2004); P. scapulatus in eastern Australia fed between 1 and 29 km from the roost (McWilliam 1986; Birt 2005); feeding distances for P. vampyrus and Acerodon jubatus in the Philippines ranged from 0.44 to 12.6 km (mean 5.0 km, Mildenstein et al. 2005) and P. tonganus in American Samoa travelled a mean distances of 22.8 km (Banack and Grant 2002).

This study adds to the body of information about longer-range feeding, showing that 15% of feeding movements were greater than 20 km from the roost (7% were >30km) and on three occasions two individuals travelled >50 km one way to feed. The limited fine-scale accuracy of satellite telemetry (see Methods 4.2; McKeown and Westcott 2011) precluded the identification of feeding sites <2 km from the roost. While this had the potential to skew results toward longer distance movements, there were too few examples of nocturnal movements < 2 km (N=7) to alter the results.

Various factors examined in this study including season, roost population size, size of feeding forest patch and landscape characteristics surrounding roosts did not explain the variation which occurred in feeding distances. However, flying-foxes that travelled shorter distances also remained for longer periods at particular roost site - feeding site combinations. Flying- foxes can minimise commuting costs by feeding close to the roost and hence it would be expected that individuals would use feeding sites near to roosts (or vice versa) for as long as possible. However, where the availability of food varies across the landscape (in particular, where food sources of relatively high nutritional and energetic value are located at comparatively long distances from roosts), the costs of flying extra distances for food may be small relative to the quality and quantity of resources that can be harvested (see also Karasov 1992). Where possible, it could be expected that flying-foxes should shift to new roost sites located close to productive feeding sites.

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 81

Two radio-telemetry studies of P. poliocephalus and P. alecto have suggested that food type may influence feeding distance, with flying-foxes traveling greater distances to use particular energy-rich nectar resources (Eby 1996; Palmer and Woinarski 1999). In the eastern Australian subtropics, Eby (1995; 1996) observed P. poliocephalus moving consistently greater maximum distances (up to 50 km) when feeding on blossom from eucalypts compared with fruit (up to 29.5 km). Flying-foxes feeding on blossom also used more feeding trees per night, and distances between feeding trees were greater (up to 20 km between feeding sites for blossom, compared with 8.3 km for fruit). A study in northern Australia found that the feeding distances of P. alecto changed seasonally, with individuals travelling further during the dry season when feeding on Eucalyptus species compared with the wet season when feeding on locally abundant rainforest fruit (Palmer 1997; Palmer and Woinarski 1999).

The feeding movements of P. poliocephalus varied considerably both among and within individuals. Similar wide variation in the distance moved by individuals to feed has been reported by other studies of this (e.g. Eby 1996) and other Australian flying-foxes (P. alecto Markus and Hall 2004; P. scapulatus Birt 2005). A study of P. poliocephalus in the eastern Australia subtropics found a negative relationship between the feeding distances moved and the individual’s fidelity to a roost site (Eby 1996), consistent with this study’s findings. Resident or sedentary flying-foxes persisted at the same roost throughout most of the year including periods when the roost population was low (Eby 1995; Eby 1996; Fleming and Eby 2003). Eby (1995; 1996) found that resident flying-foxes generally fed closer to the roost than the non-resident, migratory flying-foxes. Resident flying-foxes also used fewer feeding sites per night, rarely more than one, flew significantly shorter total distances per night and returned to specific feeding areas over longer periods (many weeks). The present study was not designed to identify the social status of individuals. In the present study, only one individual persisted at a particular roost for an extended period (Bat 5 spent 83% of days at one roost; Chapter 3). The remainder of the flying-foxes tracked in this study moved frequently among roost sites (Chapter 3).

The typical duration of feeding visits for P. poliocephalus tracked in the present study was generally less than that reported for other studies. Half of the visits to feeding sites were for less than one week (mean 12 nights, median 6 nights), although 19% were for periods of >25 nights (up to 84 consecutive nights). Previous studies have repeatedly reported that flying- foxes can maintain fidelity to feeding sites for an average of one month, although with

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 82 considerable variation (range 5-65 days) (McWilliam 1986; Spencer et al. 1991; Eby 1996; Palmer et al. 2000; Markus and Hall 2004). In the rural subtropical area of Lismore the maximum duration at feeding sites was 29, 37 and 23 nights for P. poliocephalus, P. alecto and P. scapulatus (McWilliam 1986).

The relatively short feeding durations found in this study may be explained in part by the migratory status of the study animals. Eby (1996) found that the duration at feeding sites of P. poliocephalus differed with the migration status of the individual, with resident animals remaining at individual fig trees Ficus spp. for more than 4 weeks (range 18-46 nights, mean 34.9, N = 8) and migratory animals never staying at one feeding site for longer than 18 nights (range 5 – 18, mean 11.6, N = 8). The present study was designed to target migratory individuals (see Methods 4.2.1) and our results are similar to those of migratory animals found by Eby (1996). The short duration stays at feeding sites were also consistent with the frequent movements among roosts (see Chapter 3).

Establishing how flying-foxes and other mobile species move across the landscape to feed, and establishing how they respond to different patterns of habitat alteration is an important requirement for effective conservation. This study has shown the value of using satellite telemetry to assess the habitat use of highly mobile species such as flying-foxes, as it allows a comprehensive examination of the all the landscapes used by individuals across their entire range including remote and inaccessible areas. It has been previously suggested that flying foxes may be tolerant to the urbanisation of their habitat because their mobility allows them to move freely across modified landscapes and to use resources within the urban matrix (Law and Dickman 1998; Birt et al. 1999; Markus and Hall 2004; Williams et al. 2006; Chapter 3). Our study confirms that P. poliocephalus respond positively to urbanisation around their roosts, but they do appear to be sensitive to urbanisation in terms of their selection of feeding habitat (i.e. they select for forest or ‘open’ habitats, at least within the study area). Therefore, conservation of P. poliocephalus is likely to benefit from the retention of forest patches within 20 km of roost sites. In addition, effective conservation of P. poliocephalus involves a landscape-based approach, which considers the different feeding and roosting preferences of the species and maintains connectivity between these habitats across the large geographical range of the species.

Chapter 4 – Feeding movements and landscape use by P. poliocephalus 103

Chapter 6 – General Discussion

In this chapter, I outline the main findings of the previous chapters of the thesis. I discuss how the work has contributed to knowledge of flying-fox ecology and the implications of the findings for conservation and management. I then discuss a series of questions that arise from the work, particularly questions in relation to patterns of roost use and mobility. Finally, I conclude this chapter with suggestions for the direction of further research.

6.1 Key findings of each data chapter

Historical shifts in the ranges of two Australian flying-fox species and their relationship with climate change.

In Chapter 2, a quantitative analysis of historical and present distributions of two species of flying-fox (Pteropus alecto and P. poliocephalus) in eastern Australia was undertaken. The results were used to evaluate evidence for (i) distributional shifts in these species and (ii) global warming being a driver of any such shifts. Recent range shifts towards higher latitudes have been reported for many animals and plants in the northern hemisphere and are commonly attributed to changes in climate (Walther et al. 2002; Parmesan and Yohe 2003; Root et al. 2003). Relatively little is known about such changes in the southern hemisphere, although it has been suggested that latitudinal distributions of the flying-foxes P. alecto and P. poliocephalus have extended polewards during the twentieth century in response to climate change in eastern Australia (Tidemann 1999; Hughes 2003). However, historical changes in these species’ distributions have not been examined systematically. In this study, I obtained historical locality records from a wide range of sources (including banding and museum records, government wildlife databases and unpublished records), and filtered them for reliability and spatial accuracy. The latitudinal distribution of each species was compared between eight time-periods (1843–1920, 1921–1950, five 10-year intervals between 1950 and 2000, and 2001–2007), using analyses of both point data (P. alecto 870 records, P. poliocephalus 2,506) and presence/absence data within 50 x 50 km grid cells.

The results did not support the hypothesis that either species’ range is shifting in a manner driven primarily by climate change. In the case of P. poliocephalus, neither its northern nor southern range limits (Mackay, Queensland and Melbourne, Victoria respectively) changed

Chapter 6 – General Discussion 104 over time. In contrast, there was good evidence that P. alecto’s range extended southward by over 1,100 km (approximately 10.5 degrees latitude) during the twentieth century (from near Rockhampton, Queensland to Sydney, New South Wales). Within this zone of southward expansion (25-29oS), records of P. alecto increased from 8% of flying-fox records prior to 1950 to 49% in the early 2000s; and local count data showed that its abundance increased from several hundred to >10,000 individuals at specific roost sites as range expansion progressed. However, the rate at which its range has expanded southward (an average of 100 km/decade) is much faster than the rate of isotherm change over the same period (10-26 km/decade). Consequently, the species expanded its range southward into colder regions than it had previously occupied. The more general implication of this analysis is that climate change should not be uncritically inferred as a primary driver of species’ range shifts without careful quantitative analyses.

Frequency and scale of movement among roosts and its implications for management.

Chapter 3 investigated four main questions in relation to the inter-roost movements of P. poliocephalus: (1) What patterns of movement (in terms of distances and directions) are exhibited over increasing time scales? (2) How much do these patterns vary among individuals? (3) What is the relationship between individuals’ movement patterns and their use of different roost sites? (4) What are the implications of these findings for management?

Fourteen adult males were tracked for 2‒ 40 weeks (mean 25 weeks). Collectively, these individuals utilised 77 roost sites in an area spanning 1,075 km by 128 km.

Movement patterns varied greatly between individuals, with some travelling long distances. Five individuals travelled cumulative distances >1,000 km over the study period. Five individuals showed net displacements >300 km during one month, including one movement of 500 km within 48 hours. Seasonal movements were consistent with facultative latitudinal migration in part of the population. Flying-foxes shifted roost sites frequently: 64% of roost visits lasted <5 consecutive days, although some individuals remained at one roost for several months. Modal 2-day distances between consecutive roosts were 21‒ 50 km (mean 45 km, range 3‒ 166 km). Of 13 individuals tracked for >12 weeks, 10 moved >100 km in one or more weeks. Median cumulative displacement distances over 1, 10 and 30 weeks were 0 km, 260 km and 821 km, respectively. On average, over increasing time-periods, one additional roost site was visited for each additional 100 km travelled.

Chapter 6 – General Discussion 105

The high mobility and frequent movements of these flying-foxes mean that the currently- advocated management approaches of culling animals and relocating them from roost sites have a high risk of failure. These methods are unlikely to permanently reduce local abundance of flying-foxes, because individuals have a high capacity to recolonise roosts in the short to medium term. Alternatives to local control measures, e.g. wholesale culling of flying-fox populations, run contrary to conservation objectives. More generally, the results of this chapter show that mitigation of conflict between humans and wide-ranging species such as P. poliocephalus is extremely complex and sound management of such conflicts must be built on a good understanding of species’ movement patterns.

Feeding movements and selection of feeding and roosting habitats.

Chapter 4 investigated four main questions in relation to the feeding movement and habitat selection of P. poliocephalus: (1) What are the landscape-scale habitat characteristics of roosts and feeding sites and how do they differ? (2) Do flying-foxes select roosts and feeding sites on the basis of landscape-scale habitat characteristics? (3) What distances are travelled between roosts and feeding sites? (4) What are the roles of specific factors such as roost population size, duration of visits to feeding sites, size of forest patches, time of year, elevation and land cover in determining the feeding distance moved?

Understanding how flying vertebrates move across the landscape to feed and how they respond to different patterns of habitat alteration enables managers to conserve important locations, and identify areas that meet species annual life cycle needs (Price et al. 1999; Berthold 2001; Fleming and Eby 2003). Satellite telemetry of 14 adult male P. poliocephalus utilising 45 roost sites and 173 feeding sites were used to quantify their feeding movement and landscape use.

The study found that P. poliocephalus selected roost sites in landscapes containing a higher proportion of built and open habitats than expected from their occurrence in the environment. By contrast, they were less selective of feeding landscapes, although showed some avoidance of built areas for feeding.

The distances moved from roost to feeding sites were typically (85% of feeding movements) less than 20 km. However, there was a large amount of variation in the feeding distance moved, both within and between individuals (range 2–56 km; mean 12.3, SD 9.3 km). The

Chapter 6 – General Discussion 106 visit duration spent at feeding sites was typically short: 50% of feeding visits lasted <5 days, although some individuals remained at feeding sites for up to 84 consecutive days (range 1- 84; mean 12 days; SD 14 days). Of the variables assessed in this study only the number of consecutive days during which individuals visited a particular feeding site was significantly correlated with feeding distances. Animals that remained at feeding sites for longer periods fed closer to roosts than individuals with short visit durations.

Protection of essential habitat for P. poliocephalus is a primary conservation goal for this threatened species (DECC 2009). However, its habitat requirements are complex, and this complexity has been largely attributed to variability in the distribution and flowering and fruiting characteristics of diet species (e.g. Eby 1991a; Eby and Law 2008). The importance of conserving paired feeding and roosting habitats has also been acknowledged (DECC 2009). This work adds to the discussion of habitat requirements, and in particular the need to conserve associated feeding and roosting sites that vary in landscape characteristics and which may be separated by several kilometres.

In addition, the finding that P. poliocephalus select roosting habitats near built and cleared areas emphasises the importance of developing improved methods for managing controversial roosts as part of conservation strategies for this species.

Roost relocation efforts and their success as a management strategy.

Chapter 5 examined the consequences and financial costs of a coordinated, government- sponsored attempt to relocate a flying-fox roost at Maclean in north-east New South Wales (NSW). The Chapter also reviewed the occurrence and outcomes of other relocation attempts in Australia, and discussed the utility of relocation as a management tool to resolve conflict between humans and flying-foxes.

Managing flying-fox roost sites in urban areas is an increasing challenge for government agencies along the east coast of Australia (Birt et al. 1998; Hall and Richards 2000; Eby and Lunney 2002b). In the township of Maclean, flying-foxes had used a roost as a maternity site for over 100 years. Due to a range of community concerns, flying-foxes were repeatedly induced to move from the Maclean roost during the period 1999–2007, by subjecting animals using the roost to periodic episodes of continuous loud noise.

Chapter 6 – General Discussion 107

Records compiled in this chapter show that the total cost of the Maclean relocation attempt was > $400,000 (if include cost of alternative land purchase), including 640 person-hours of effort. Flying-foxes made 23 attempts to return to the original roost location during the nine years of disturbance, although the frequency of attempts declined over time. Twelve other sites were used during this time as temporary roosts, including seven sites not previously occupied. In 2004, flying-foxes established a new continuously-occupied roost in the township of Iluka, 16 km north east of Maclean. Residents near the Iluka roost were by 2005 intensively lobbying governments to disperse the animals from this new location. Both the Iluka and Maclean roost sites were still in use in 2011. The outcome after nearly a decade of dispersal attempts at Maclean was that flying-foxes continued to return periodically to the original site, and there were more roost sites established in the region, over a wider area than previously known from historical records, and the number of affected residents experiencing conflict had increased.

The location of flying-fox roosts near human settlements is likely to continue to be an issue of community conflict and conservation concern in the future. The experience at Maclean raises questions of how, and at what spatial and temporal scales, the success of relocation attempts should be determined.

6.2 Patterns of roost usage and mobility by flying-foxes: questions arising from this work

Why does Pteropus poliocephalus move frequently among roosts?

The results of research conducted for this thesis, together with previously-published work by other researchers, show that the movement patterns of P. poliocephalus are far more complex and variable then that typically seen in north-south migrants in the northern hemisphere. Individual P. poliocephalus are highly mobile and exhibit a range of short- and long-distance movements over a range of temporal scales (Eby 1991a; Tidemann and Nelson 2004; Chapter 3). For example, it is common for some P. poliocephalus to regularly move among a number of roosts within a region or from one region to another over distances of several hundred kilometres (Eby 1996; Spencer et al. 1999; Tidemann and Nelson 2004; Chapter 3). Previous authors have argued that food availability is a major driver of the movement patterns of P. poliocephalus, as well as influencing the number of individuals within particular roosts at any given time (Eby 1991a; Parry-Jones and Augee 1992; Eby 1996). However, a clear

Chapter 6 – General Discussion 108 understanding of how the movement patterns of flying-foxes relates to the availability of food, particularly within a region, is still needed. If the drivers of flying-fox movement could be better understood, ecologists would be able to better predict patterns of roost occupation and inter-roost movements, contributing greatly to the management of flying-foxes in contentious locations.

The available evidence on drivers of flying-fox movement patterns is summarised as follows. McWilliam (1986) radio-tracked three species of flying-fox (P. poliocephalus, P. alecto and P. scapulatus) in subtropical eastern Australia. The results suggest that the movements between roost sites at a local scale were correlated with shifts in available food resources, and some individuals of P. alecto moved between neighbouring roost sites in order to reduce commuting distances to new food sources. Eby (1996) examined temporal and spatial patterns in resource availability for P. poliocephalus, related these trends to patterns of animal abundance and movement, and concluded that the movement among roosts of migratory individuals was closely associated with patterns of food availability. Abandonment of feeding areas could not consistently be attributed to resource depletion, but migratory individuals generally shifted roosts to areas of mass eucalyptus flowering (Eby 1991a, Eby 1996). Markus (2000) found that some radio-tracked individuals of P. alecto in urban Brisbane regularly moved between two or three roost sites and that each shift was to a roost closer to the current feeding area. Parry-Jones and Augee (1992) found that the patterns of occupancy of a P. poliocephalus roost in the eastern subtropics were correlated with fluctuations in food supply, and that local abundances of blossom of tree species such as Angophora floribunda and Corymbia maculata (syn. Eucalyptus maculata) were associated with large colony numbers of >80,000 flying-foxes.

Not all individual flying-foxes move regularly between roosts. Some show a high degree of fidelity to one roost, a behaviour which may also be associated with the availability of food. Both Eby (1996) and Markus (2000) found that both P. poliocephalus and P. alecto had a proportion of the population that were resident individuals which rarely shifted roost sites. They argued that this was made possible because the bats were roosting in locations where a high diversity of food plants provided a continuous food source, in particular, areas whose food supply included the availability of fruits such as Ficus.

By using satellite telemetry, this study was able to provide additional information on the frequency of movements among roosts by migratory P. poliocephalus (Chapter 3). Capture

Chapter 6 – General Discussion 109 sites targeted in this study were those that were either seasonal roosts or had a high number of flying-foxes present to ensure that most of the individuals present were likely to be migratory (see Chapter 3 and 4, Methods). No study animals displayed the roosting traits of residents in that none remained at a single roost for longer than 133 consecutive days. The study showed that at times P. poliocephalus moved frequently between roost sites across a broad landscape, but there was also a high amount of exchange between roosts in a local region. Individuals typically spent less than five days at roosts, although there were some extended stays at one site followed by frequent short-stays at a number of roosts. All long-distance movements (net displacement >300 km in one month) were to areas of intensive flowering of known food tree species (all Myrtaceae): Eucalyptus tereticornis, E. siderophloia, E. pilularis, Corymbia citriodora, C. intermedia or Melaleuca quinquenervia. In Chapter 3, I also argue that short stays at closely positioned roosts occurred in local areas that provided continuous food.

The duration of visits at feeding sites was typically short; half the visits were for around five days (Chapter 4), consistent with the short duration stays at roosts (Chapter 3). In some cases, individuals spent extended periods at one roost and used the same roost to access several feeding sites. Although not quantitatively analysed, inspection of the data suggest that only on rare occasions would individuals use different roosts to access the same feeding site, and these movements were usually associated with a reduction in feeding distances. This observation together with the significant negative correlation between individuals feeding distance from a roost site and the duration of its stay at feeding sites (Chapter 4) suggests that these flying-foxes selected roost sites as a consequence of their need to move among suitable feeding areas, while minimising flight distances from each roost. The energetic costs of flight constrain feeding distances (e.g. Eby 1991a; Eby 1996). In most locations, the food resources available to flying-foxes within nominal feeding distances of roosts fluctuate with time, and flying-foxes must move between roosts to access new food locations (see also McWilliam 1986; Markus and Hall 2004). The capacity to move long-distances over a period of days allows the species to utilise the ephemeral flower and fruit resources characteristic of Australia, across broad spatial scales (Eby 1991a; Eby 1996; Chapter 3). However, the mechanisms used by P. poliocephalus to track food over large areas or the proximal cues for flying-fox movement and causes of variation between individuals remain poorly understood.

Chapter 6 – General Discussion 110

6.3 Ecology and management of flying-foxes in human dominated environments

What is the behaviour of Pteropus poliocephalus in relation to built environments?

In this discussion the term ‘built environment’ is used with reference to human-made structures that provide the setting for human activities, particularly settlements, ranging in scale from rural residential (scattered houses on large blocks), villages (clusters of 100–999 people), towns (clusters of 1000–9999 people) to urban areas (clusters of >10,000 people) (Source: Australia Bureau of Statics 2006).

In eastern Australia, flying-foxes commonly roost in proximity to such built environments. Reports have suggested that, in recent times, there has been: (1) an increase in the number of roosts in villages, towns and urban areas (Birt et al. 1998; Hall 2002; Markus and Hall 2004; Roberts 2005); (2) an increase in the number of individuals within urban roosts, particularly in the southern part of the range of P. poliocephalus (van der Ree et al. 2006); and (3) an increase in the frequency of use of urban roosts, e.g. seasonally used roosts becoming continuously used (Birt et al. 1998; van der Ree et al. 2006; Williams et al. 2006). The presence of flying-fox roosts in or on the edge of built environments has been attributed both to the encroachment of human development on traditional roost sites (Birt et al. 1998; Hall 2002) and to a spatial shift of flying-fox populations into human settlements (Birt et al. 1998; Hall 2002; Parris and Hazell 2005; van der Ree et al. 2006; Williams et al. 2006). Roosts in close proximity to human settlements often generate conflict, with local communities becoming concerned about issues of noise, smell and disease transmission from bats to livestock and to humans (e.g. Hall and Richards 2000; Chapters 1 and 5). The increased presence of flying-foxes within human settlements also leads to a presumption that flying-fox populations are increasing, and hence that management actions should be undertaken to control their numbers, either by culling or by disturbance to roost sites (e.g. Eby and Lunney 2002a; Chapter 3). A better understanding of how and why flying-foxes use built environments is required to help resolve conflicts that occur between flying-foxes and humans in these locations.

Explanations for increases in the occurrence of flying-foxes in urban areas have generally cited recent increases in the availability and quality of food in these locations, combined with habitat loss elsewhere in the species’ range. For example, a study of P. poliocephalus by

Chapter 6 – General Discussion 111

Parry-Jones and Augee (2001) stated that the introduction of fruiting and flowering plants (native and exotic) to the Sydney region has provided an increased variety of foods for flying- foxes, permitting the continuous occupation of urban roosts. van der Ree et al. (2006) showed a significant increase in the total number of P. poliocephalus in urban Melbourne since the 1980s and a change from seasonal to permanent occupancy of a roost. The authors suggested that increased food availability within the urban landscape and loss of habitat elsewhere contributed, together with climate change, to the permanent establishment and growth of this colony. Similarly, Parris and Hazell (2005) argued that a combination of an increase in temperatures in Melbourne (primarily as a result of an ‘urban heat island’ effect) and an increase in the supply of food (due to the establishment of non-indigenous plant species) had created more favourable conditions for flying-foxes. In addition, Williams et al. (2006) demonstrated that plantings of favoured food plants in Melbourne have increased the temporal availability of food for P. poliocephalus in that city: prior to European settlement, only 13 species recorded in the range-wide diet of P. poliocephalus grew in the Melbourne area, but by 2006, an additional 87 diet species and over 300,000 individual trees had been planted on Melbourne’s streets. Increases in the number of roosts recorded in other Australian cities (e.g. Brisbane: Markus and Hall 2004; Roberts 2005) have also been attributed to an increase in food supply (Markus and Hall 2004).

However, it may be overly simplistic to conclude that: (1) changes in habitat usage by flying- foxes have only occurred in urban locations; or (2) the overall population of flying-foxes has uniformly increased in urban areas. First, there is some evidence that roosts outside urban areas have also exhibited an increased frequency of occupation. A shift from seasonal to continuous use has been reported for roosts at Susan Island and Bellingen, both in small rural towns in north-east New South Wales (Lunney and Moon 1997; Smith 2002; J. Thomas pers. comm.). Second, at least two long-established urban roosts have declined in population size concurrently with an increase in the number of local sites: Indooroopilly Island in Brisbane (Hall 2002) and Gordon in Sydney (M. Beck, Ku-ring-gai Bat Conservation Society unpublished). Hall and Richards (2000) stated that various large roost sites (>200,000) observed in south-east Queensland in the 1970s no longer existed by the 1990s, having instead been replaced by a number of smaller roosts in urban locations. They concluded that this change from a few large to many smaller roosts has led to the misconception that flying- foxes have actually increased in numbers in recent times. However, long-term data on the abundance of P. poliocephalus are limited at all but a few roost sites (Chapter 2). The lack of

Chapter 6 – General Discussion 112 long-term monitoring, and the naturally high temporal variability in roost populations associated with the high mobility of P. poliocephalus (Eby 1991a; Chapter 3), make it difficult to verify long-term change in abundance at any roost, or across particular roost types (e.g. urban or rural).

The possible factors driving changes in the occupancy of roosts in rural residential areas, villages and towns are less clear than those in urban landscapes as the limited areas associated with these settlements provide much less scope for human structures to influence ambient temperature or for the abundance of diet plants to be substantially enhanced due to gardens or streetscapes plantings. Preferences for roosts within large cities, as well as within villages and towns, may perhaps be explained by factors such as protection from shooting and roost disturbances or assistance with navigation from illuminated features (Birt et al.1998; Hall and Richards 2000). Alternatively, the reduced likelihood of some predators (e.g. raptors, varanids) in built areas may explain the prevalence of flying-fox roosts. It is also possible that correlations between selection factors for human settlements and flying-fox roosts, i.e. level land near waterways, contribute to the selection of roosts in residents and urban areas (Roberts 2005).

Although flying-foxes use many roost sites in urban areas, they also continue to use a large number of roosts outside urban locations. This study examined roost and feeding preferences across all landscapes, including a range of built environments. Of the 45 roosts used by study animals, 40% were in remote areas where no built land occurred within 2 km of the site and 50% were in areas where <5% of the surrounds contained built land (rural residential or villages). By contrast 20% were located in substantially built environments where >35% of the surrounds contained built land (towns) and 4% were embedded in urban landscapes (Chapter 4). It is important to distinguish between the following two processes: (1) an increased use overtime of urban areas for either roosting or feeding; and (2) a preference for feeding or roosting in built environments. Results of the present study weakly support the notion that P. poliocephalus selects roosts near built areas. However, this study’s data also show that P. poliocephalus avoids feeding in built areas. It remains plausible that flying-foxes use of these built areas for feeding has increased in recent decades. But the built environment remains the less-preferred feeding habitat in spatial terms.

The mobility of flying-foxes allows them to roost within human settlements and traverse open or modified areas to find trees that bear nectar and fruit (Law and Dickman 1998; McDonald-

Chapter 6 – General Discussion 113

Madden et al. 2005). Human settlements may be providing alternative benefits to flying-foxes associated with the local characteristics of roost sites. However, further work is required to understand both this trend and the specific local on-ground characteristics by which P. poliocephalus select roost sites across their geographical range. Further quantification of feeding resources and their availability within both built areas, and open areas, compared with forests is also needed.

What leads to the success or failure of roost relocation attempts?

In Australia, the relocation of flying-fox roost sites has been frequently attempted to resolve human–bat conflict in urban and rural areas. Conflict arises when bats establish roosts close to human activities or when human development encroaches on established roost sites (Birt et al. 1998; Hall and Richards 2000; Chapter 5). Roost relocations refer to the intentional movement of entire colonies from one location to another, although exactly where flying- foxes may move to when relocated cannot be pre-determined. A number of different techniques have been used to harass flying-foxes until they shift elsewhere, including continuous loud noise, bird-scare guns, helicopters and light aircraft, spraying with water, smoke and habitat destruction (Vardon et al. 1997; Tanton 1999; Tidemann 2002; Chapter 5). Similar techniques are also used at flying-fox roosts worldwide to manage conflicts (Mickleburgh et al. 1992). However, few relocation activities have been systematically monitored and the success or otherwise of such projects have been debated (Hall 2002; Tidemann 2002; West 2002). A better understanding of the costs involved and long-term outcomes of these activities is required.

The few studies that have examined relocations have all been conducted within Australia, however these studies have only monitored short-term outcomes. They are summarised as follows. Vardon et al. (1997) reported on the success of a relocation attempt of more than 200,000 P. scapulatus from a roost at Mataranka, in northern Australia, during 1994-1995. Several methods were used including bird-scare guns and cattle crackers fired from shotguns, harassment by light aircraft (up to 12 passes per day), water jets and smoke. All methods were unsuccessful in moving flying-foxes more than 300 m from their original location and for periods of more than two days. Tidemann (2002, 2003) provided information on the dispersal of a P. poliocephalus roost in Maclean, northern NSW during 1999–2002. The study found that during this time there were 16 reoccupation attempts by flying-foxes to the original site, but the frequency of these attempts declined with time. However, the author noted that sub-

Chapter 6 – General Discussion 114 optimal monitoring of dispersal actions made it impossible to determine where animals moved to and additional monitoring over longer time periods was required to improve the success of relocation attempts. A review of the same dispersal attempt at Maclean by West (2002) stated that animals did not move to predetermined locations as anticipated and that financial costs of the operation were high and ongoing. Phillips et al. (2007) reported on the relocation of a small roost of 200 P. alecto in Batchelor, North Territory over five months in 2004. Flying-foxes were dispersed using a combination of smoke, non-lethal plastic shot and noise. Initial actions fragmented the population to new locations within the township and follow-up dispersal actions at both the original sites and the new roost locations were required. After five months the flying-foxes had shifted approximately 400 m to the town’s periphery but continued efforts were required to ensure that they did not re-establish in town. The author argued that the best longer-term solution to stop flying-foxes from trying to re- establish in town would be to remove the roost vegetation. Collectively, these studies indicate that severe roost disturbance may induce flying-fox roosts to shift short distances for short periods of time, but the longer-term success of these actions has often been limited, when flying-foxes return to their original roost sites.

In the Melbourne Royal Botanical Gardens after six months of disturbance action the flying- foxes left and began roosting at two separate locations, Yarra Bend Park and Geelong, 5 and 65 km respectively from Melbourne, but did not move to the target site identified in the relocation plan (Toop 2004; Department of Sustainability and Environment 2005; Chapter 5). Following negotiations with the land managers at these two new locations, the flying-foxes’ presence there was accepted. Since then, only one recorded attempt has been made by flying- foxes up to the time of writing (2012) to re-establish the original site (Chapter 5). The action required thousands of person-hours of effort and approximately $3 million including associated research and purchase of additional habitat at one of the new sites (Department of Sustainability and Environment 2005; Chapter 5).

To be consistent with the goals of minimising human-bat conflict, and with conservation and animal welfare objectives, a definition for success of relocations should include at least the following: (1) that conflict has been reduced within the broader community (not just the original site); and (2) there was minimal impact on the flying-foxes, in terms of animal welfare, population mortality or lowering reproduction. In Chapter 5, I examined the outcomes of 10 separate relocation attempts in Australia, during 1990–2009. This is the first

Chapter 6 – General Discussion 115 review of the long-term outcomes and costs of roost relocation attempts. The study found that relocations, regardless of the methods used, have had limited success in permanently resolving conflicts between humans and flying-foxes, and were costly. At Melbourne the relocation reduced the intense, continual conflict with the general community, however at the two new roost sites periodic noise disturbances were required to alter the extent of the roost to prevent the flying-foxes encroaching concerned neighbours (Department of Sustainability and Environment 2011a). In terms of welfare, Yarra Bend Park did not provide the same protection from high temperatures as was provided by Melbourne Botanical Gardens and thousands of P. poliocephalus died due to extreme heat events during 2004-2010 (Department of Sustainability and Environment 2011a and b). Given the high mobility of flying-foxes: a high frequency of movements between roosts, the large number of roosts used by individuals, the rate of return to specific roost sites and a capacity for long-distance movement (Eby 1991a; Eby 1996; Tidemann and Nelson 2004; Chapter 3), it seems very unlikely that relocation attempts could have a high probability of success in resolving human-bat conflicts over the long term.

In terms of animal welfare, little is known about the impact of relocations on flying-foxes, and a better understanding is required. Garnett et al. (1998) reported that roost dispersals can result in high mortality, particular if conducted during the breeding season as it can result in the death of dependent juveniles.

As past relocation attempts have failed to provide long-term solutions and have at times worsened conflict between humans and flying-foxes (e.g. by shifting flying-fox roosts to equally controversial areas), there is now an imperative to find new approaches to resolving such conflicts that are based on a sound understanding of the ecology of flying-foxes. Such approaches, and any future attempts at relocation, should be accompanied by an adequate long-term monitoring program, to allow evaluation of the success of the action. The success of relocation attempts or other approaches to managing human-flying-fox conflicts need to be considered over longer time frames than has so far been the case (years rather than weeks or months).

Lastly, as P. poliocephalus is one intermixing population and during a single year individuals can visit a number of roost sites within the jurisdiction of multiple governments, agencies and landholders, a range-wide or national approach (rather than local or state) is needed for their effective management. Management of flying-foxes is further complicated because they are

Chapter 6 – General Discussion 116 locally unwanted in most of the locations where they roost and feed. A consistent approach to the management of flying-foxes is required to ensure that management actions in one region do not have adverse impacts in another (e.g. increase numbers at other contentious sites). However, in Australia, there is not a uniform approach to the management of flying-foxes and their roost sites, and the threatened species legislation guiding management approaches varies between states (Eby and Lunney 2002a; Thiriet 2010).

6.4 Research directions

This thesis has addressed some key questions related to the ecology of Pteropus poliocephalus, and considered the implications of these results for management. It has provided new knowledge about the species’ distribution, foraging ecology and roost management. However, there are still unresolved issues related to each of these topics that require further information to improve management and conservation. Below I propose a series of potential future research directions under three key themes. The list is not intended to be comprehensive and is not in order of importance.

Species distribution

Clarify the western boundary of the range of P. poliocephalus and its patterns of occupation in inland areas. Investigate the location, composition and temporal usage patterns of P. poliocephalus roosts in the north of the range (north of 24oS). Obtain long-term data on the abundance of P. poliocephalus within that part of its range where P. alecto has expanded in historical times, together with more information on the ecology of each species, to increase understanding of the interactions between the two species where their ranges overlap. Determine the drivers of the southern range extension of P. alecto (this study found that climate change was not a sufficient explanation; alternative hypotheses such as habitat loss have yet to be investigated).

Movement and feeding ecology

Determine whether different sex and age classes of P. poliocephalus exhibit different movement patterns (this study was restricted to adult male flying-foxes, but advances in

Chapter 6 – General Discussion 117

satellite telemetry should mean that it will be possible to track smaller animals in the future). Conduct additional research examining factors such as food type and migratory status influence on the feeding distances moved by P. poliocephalus. Identify the mechanisms used by P. poliocephalus to track the availability of food resources over large areas/ spatial scales. Develop methods for monitoring short-term (i.e. weeks and months) trends in nectar supply at a landscape scale to understand the frequency of movements of P. poliocephalus among roosts in a local region.

Roost management

Determine the criteria involved in roost selection by P. poliocephalus, particularly at a local scale, and investigate whether these criteria vary between landscapes and regions. Examine the impacts of roost relocations on animal welfare, mortality and reproduction (at present, monitoring of relocation attempts has been largely restricted to the abundance of flying-foxes at ‘old’ and ‘new’ roost sites). Obtain long-term data on the abundance of flying-foxes at a range of urban and non-urban (rural, native forest) roost sites, to determine whether flying-foxes are increasing in abundance in urban areas at the expense of non-urban areas. Conduct research on social attitudes to flying-foxes and what actions could be most effective in mitigating conflict with humans. Examine the role politics and the media play in determining management outcomes.

Chapter 6 – General Discussion 118

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Appendices

Appendix 1 Data sources, time-period of records and number of records of Pteropus alecto and P. poliocephalus. Point records are those retained after screening for incomplete, unreliable, duplicate or misidentified information. Museum sources held specimen records; atlas sources held biological surveys, incidentals and literature records; and all other sources were based on biological surveys.

P. alecto P. poliocephalus Screened point Screened point Source Period Raw records Raw records total total Total Roost Other Total Roost Other Atlas of New South Wales Wildlife (New South Wales 1863–2007 110 76 0 76 1964 1212 0 1212 Department of Environment, Climate Change & Water) Atlas of Victorian Wildlife (Victorian Department of 1884–2005 0 0 0 0 1340 154 30 124 Sustainability & Environment) Australia Bird & Bat 1985–2007 1491 18 15 3 5831 186 98 88 Banding Scheme (ABBBS)† Australian Museum 1879–2005 109 40 1 39 176 95 1 94 Australian National Wildlife 1961–1995 47 17 0 17 41 17 0 17 Collection (CSIRO) International museums‡ 1843–1991 235 9 2 7 117 12 1 11 Published & unpublished 1878–2001 43 43 33 10 155 136 112 24 literature§ Queensland Museum 1905–2000 133 52 2 50 125 33 1 32 South Australian Museum 1905–1930 13 4 0 4 7 2 1 1 Surveys & incidentals†† 1975–2007 545 283 283 0 1058 429 429 0 Victorian Museum 1869–1996 12 5 0 5 121 41 0 41 Western Australian Museum 1960 116 1 1 0 3 1 0 1 WildNet Fauna Data (Queensland Department of 1924–2006 588 322 21 301 705 188 15 173 Environment & Resource Management) TOTAL 3442 870 358 512 11643 2506 688 1818

† ABBBS collectors who made records available were C. Tidemann, H. Spencer, J. Welbergen, K Parry-Jones, S. Klose and C. Palmer. The large reduction in the number of records for the Australian Bird and Bat Banding Scheme was due to multiple individuals being banded at the same location during the same year. ‡ International museums that held specimens were Smithsonian Institute National Museum of Natural History (Washington DC, USA), The Natural History Museum (London, UK), Field Museum (Chicago, USA), American

Appendices 136

Museum of Natural History (New York, USA), Zoologisches Museum Berlin (Berlin, Germany), Natural History Museum (Oslo, Norway), Museum of Comparative Zoology – Harvard University (Cambridge, USA), Los Angeles County Museum (Los Angeles, USA), Royal Ontario Museum (Toronto), University of Washington Burke Museum of Natural History and Culture (Seattle, USA) and University of Kansas Natural History Museum (Lawrence, USA). § References: Andersen 1912, Bartholomew et al. 1964, Birt 2005, Churchill 1998, Clancy 2001, Collett 1887, Dobson 1878, Eby 2002a, Eby 2003, Eby 2004, Eby & Palmer 1991, Eby et al. 1999, Hall 2002, Hall & Richards 2000, Lunney & Leary 1985, Nelson 1963, Nelson 1964, Nelson 1965, Pallin 2000, Ratcliffe 1931, Ratcliffe 1932, Ratcliffe 1938, Rhodes & Hall 1997, Strahan 1994, Tidemann 1999. †† Researcher and survey years (records not in any other data source) – P. Eby (1994–2006), G. Richards (1961–1990), L. Hall (1985–1995), P. Birt (1996–2005), B. Roberts (2005–2007), G. O’Neill (2000–2003), T. Pearson (2006–2007) and D. Lowe (2005–2007).

Appendices 142

Appendix 3 Grid records for Pteropus alecto (N = 222) in coastal eastern Australia over four time-periods; 1843–1950, 1951–1990, 1991–2000 and 2000–2007. Each grey cell is 50 x 50 km.

1843 – 1950 1951 – 1990

-15 500km

-20o

-25o

- 30o

-35o

1991 – 2000 2001 – 2007

-15o

-20o

-25o

- 30o

-35o

Appendices 143

1843–1950 1951–1990

o -15 500km

-20o

-25o

- 30o

-35o

1991–2000 2001–2007

-15o

-20o

-25o

- 30o

-35o

Appendices 144

Appendix 5

Orientation of solar powered satellite transmitters on flying-foxes.

A: Collar design 1, a 12 g solar powered PTT with the bottom of the unit mounted to the collar and the solar array facing down when the animal was roosting (Photo © T. Holmes). This orientation did not allow sufficient recharging of the unit and therefore number and accuracy of fixes were poor.

B: Collar design 2, a 12 g solar powered PTT attached to the collar on its side with the solar array orientated towards the sky with an angled antenna (Photo © G. Bottroff). This orientation reduced recharge time and improved power and accuracy and was the primary design used in this study.

A B

Appendices 145

Appendix 6 Data summary: individuals’ characteristics, distances moved and use of roost sites over several time-periods, for 14 satellite-tracked Pteropus poliocephalus. All distances are between day roost sites, except for the longest day-night step, which can be between day roost and night feeding sites

Flying-fox number 78188 78189 78190 78191 78186B 81072 81073 81074 80187 80188 80189 80190 80191 80192 Mean SD Capture site Stafford Stafford Canungra Canungra Dunwich Fraser Dunwich Dunwich Dunwich Fraser Fraser Fraser Dunwich Fraser - - Weight (g) 660 660 739 696 845 827 815 825 822 740 789 798 615 764 - - Forearm length 159 159 172 164 164 171 170 165 168 162 160 162 156 166 - - (mm) Date of deployment 18/10/07 17/10/07 16/10/07 16/10/07 20/6/08 30/6/08 22/6/08 22/6/08 22/6/08 30/6/08 30/6/08 1/7/08 21/6/08 30/6/08 - - End date 31/10/07 28/1/08 18/4/08 11/6/08 9/12/08 14/3/09 26/12/08 18/11/08 27/11/08 9/2/09 1/4/09 7/12/08 28/3/09 24/9/08 - - Transmission days1 13 101 182 235 169 254 184 146 155 219 271 156 277 84 175 75 No. of days with 8 41 54 106 55 94 99 76 82 87 125 82 154 35 78 38 location data2 Useable roost fixes3 9 75 45 324 50 122 219 120 202 128 255 161 322 59 149 102 Net overall 183 183 158 0 284 378 739 278 63 119 312 78 33 94 207 190 displacement km4 Max displacement 183/5 195/39 377/137 454/53 576/5 855/119 739/94 327/95 63/19 329/209 547/181 234/64 93/173 94/2 km/days5 Cumulative overall 195 241 702 1025 1121 1562 1102 840 172 763 1652 980 489 194 788 491 displacement km6 Max. step size km 125/2 110/5 190/5 193/5 576/5 349/17 335/5 165/5 42/2 199/3 166/2 126/3 49/2 94/2 in all data/days7 Median step size km 125/1 30/1 - 51/4 - 85/2 23/3 13/10 15/3 31/7 40/9 45/9 10/14 94/1 47 36 in 2 days/N 8 Min. step size km in 125/1 30/1 - 22/4 - 36/2 13/3 12*/10 15/3 18*/7 29/9 3*/9 4/14 94/1 33 38 2 days/N 9 Max. step size km 125/1 30/1 - 155/4 - 134/2 146/3 96/10 42/2 166/7 166/9 103/9 49/14 94/1 109 48 in 2 days/N 10 Longest day-night 125 44 230 205 500 259 336 175 42 166 166 123 49 79 179 126 step km in 2 days11 N for 1-week 2 14 25 34 19 29 26 21 22 29 39 22 40 11 periods Net displacement 98 21 26 32 60 53 37 31 5 24 39 27 12 17 34 23

Appendices 146 km/week12 No. roost sites used 2.0 1.0 1.3 1.4 1.0 1.4 1.4 1.8 1.4 1.4 1.5 1.8 2.0 1.4 1.5 0.3 in 1 week13 Cumulative km in 1 98 21 26 32 64 52 42 39 8 26 42 47 12 18 38 23 week14 N for 5-week - 2 5 6 4 6 5 4 4 6 8 4 8 2 periods Net displacement - 74 51 59 259 149 150 117 16 89 105 96 21 38 94 66 km in 5 weeks12 No. roost sites used - 2.5 2.2 2.7 2.5 2.7 3.0 4.0 2.3 2.8 3.3 3.5 2.9 3.0 2.9 0.5 in 5 weeks13 Cumulative km in 5 - 110 137 153 280 210 220 194 43 117 206.5 251 61 83 159 74 weeks14 N for 10-week - 1 2 3 2 3 2 2 2 3 4 2 4 1 periods Net displacement - 195 18 114 466 301 372 127 32 169 186 147 40 72 172 136 km in 10 weeks12 No. roost sites used - 4.0 2.5 4.3 3.5 4.0 5.0 6.5 3.0 4.7 5.0 6.0 4.3 5.0 4.4 1.1 in 10 weeks13 Max displacement - 195 35 454 576 679 627 208 63 199 300 232 54 94 286 226 km in 10 weeks15 Max. step size km - 110 35 193 576 349 335 165 42 199 166 126 46 94 187 154 in 10 weeks16 Cumulative km in - 216 125 306 561 419 537 388 86 234 413 503 122 165 313 167 10 weeks14 N for 20-week - - 1 1 1 1 1 1 1 1 2 1 2 - periods Net displacement - - 27 120 333 82 742 240 64 90 165 56 41 - 178 209 km in 20 weeks12 No. roost sites used - - 3.0 2.0 6.0 6.0 9.0 12.0 5.0 10.0 8.5 9.0 6.0 - 7.0 3.0 in 20 weeks13 Cumulative km in - - 135 120 1121 436 1074 776 172 618 826 1005 245 - 593 390 20 weeks14 N for 30-week - - - 1 - 1 - - - 1 1 - 1 - periods Net displacement - - - 107 - 576 - - - 158 357.00 - 36 - 247 219 km in 30 weeks12 No. roost sites used - - - 10.0 - 10.0 - - - 12.0 10.0 - 10.0 - 10.4 0.9 in 30 weeks13 Cumulative km in - - - 919 - 821 - - - 703 1059 - 489 - 798 217 30 weeks14 1 The total number of days from the date of deployment until the unit ceased functioning or until bat activity ceased (end date).

Appendices 147

2 The number of days throughout the transmission period that bats were detected during daylight hours (between sunrise and sunset). 3 The total number of fixes used for analysis; this included only securitised records with accuracy <2 km and located at a feasible roost site. 4 The distance in km between the roost at which the individual was captured and its last recorded roost, during the lifespan of the transmitter. 5 The furthest distance between any two recorded roosts during the lifespan of the transmitter and the no. of days between those fixes. 6 The sum of all sequential distances between consecutive recorded roost sites throughout the study. 7 The maximum inter-roost distance across all consecutive pairs of different recorded roosts during the lifespan of the transmitter, and the no. of days between those fixes; (total N = 167 steps across all individuals). 8 The median inter-roost distance across all consecutive pairs of different recorded roosts that were separated by 2 days, and the no. of such steps for each individual. 9 The minimum inter-roost distance across all consecutive pairs of different recorded roosts that were separated by 2 days, and the no. of such steps for each individual; asterisked records show movements involving temporary roosts. 10 The maximum inter-roost distance across all consecutive pairs of recorded roosts that were separated by 2 days, and the no. of such steps for each individual. 11 The maximum distance between consecutive useable fixes, recorded as either night feeding locations or day roost sites, which were separated by 2 days. 12 The distance in km between the first and last roost sites during five time-periods; one week, five weeks, 10 weeks, 20 weeks and 30 weeks; for each time-period this measurement is the average across N (as shown) timed movements for each individual. 13 The average number of different recorded roost sites during five time-periods; one week, five weeks, 10 weeks, 20 weeks and 30 weeks; for each time-period this measurement is the average across N (as shown) timed movements for each individual. 14 The sum of all sequential distances between consecutive recorded roost sites during five time-periods; one week, five weeks, 10 weeks, 20 weeks and 30 weeks; for each time-period this measurement is the average across N (as shown) timed movements for each individual. 15 The furthest distance between any two recorded roosts during time-periods of 10 weeks; this measurement is the maximum across N (as shown) 10-week movements for each individual. 16 The maximum inter-roost distance across all consecutive pairs of different recorded roosts during time-periods of 10 weeks; this measurement is the maximum across N (as shown) 10-week movements for each individual.

Appendices 148

Appendix 7 Frequency distribution of the weekly net displacement of all 13 individuals that had 12 or more weeks of data.

10 20 25 A 78189 B 78190 C 78191

8 20 15

6 15 10

Frequency 4 10

5 2 5

0 0 0 15 20 15 D 78186B E 81073 F 81074

15 10 10

Frequency 5 5 5

0 0 0 30 20 H 80191 20 G 80187 I 81072 25

15 15 20

15 10 10

10 Frequency 5 5 5

0 0 0 20 25 15 K 80189 J 80188 L 80190 20 15 10 15 10 10 Frequency 5 5 5

0 0 0 10 0-5 5-50 51- 101- 201- 301- 401- 501- 0-5 5-50 51- 101- 201- 301- 401- 501- M 80192 100 200 300 400 500 600 100 200 300 400 500 600 Net displacement (km) Net displacement (km)

5 Frequency

0 0-5 5-50 51- 101- 201- 301- 401- 501- 100 200 300 400 500 600 Net displacement (km)

Appendices 149

Bat ID # 78188 78189 78190 78191 78186B 81072 81073 81074 80187 80188 80189 80190 80191 80192 Mean SD Feeding distance rank-order 1 6 7 5 13 12 11 9 2 8 10 14 4 3 Date of deployment 18/10/07 17/10/07 16/10/07 16/10/07 20/6/08 30/6/08 22/6/08 22/6/08 22/6/08 30/6/08 30/6/08 1/7/08 21/6/08 30/6/08 Transmission days1 13 101 182 235 169 254 184 146 155 219 271 156 277 84 175 75 Total feeding fixes2 10 56 29 139 105 140 192 147 169 150 228 169 308 71 128 66 Mean feeding visit duration (days)/ N3 1/1 5/9 2/6 13/12 17/7 15/5 17/8 7/6 36/4 8/12 11/14 6/10 15/14 17/2 12 9 N for all records4 1 9 6 24 10 14 15 7 14 17 21 12 22 1 12 7 Median feeding distance (km) 5 10 10 7 17 12 9 14 4 12 11 14 9 7 10 4 Mean feeding distance (km) 5 11 13 10 18 15 14 13 6 13 14 20 9 7 12 4 Standard error 1.4 2.3 2.6 2.1 1.9 2.0 2.2 5.4 0.9 Max. feeding distance (km) 5 17 32 30 36 32 28 21 24 31 50 56 15 7 27 14 Min. feeding distance (km) 5 4 3 5 8 3 5 6 2 2 5 2 2 7 4 2 Mean roost population size x103/ N 20/1 20/1 4/5 4/22 28/2 64/8 8/15 5/1 9/14 50/6 60/11 100/4 8/17 50/1 30 29 Mean feeding forest patch x103 (ha) 10.0 7.2 6.9 5.1 6.9 10.0 6.5 4.0 9.4 8.5 8.4 8.6 7.1 10.0 8 2 N for independent feeding records5 1 9 6 11 5 8 9 6 5 13 14 10 14 1 8 4 Median feeding distance (km) 5 10 10 12 14 11 9 14 8 12 11 14 9 7 10 3 Mean feeding distance (km) 5 11 13 13 18 14 13 13 12 13 15 21 9 7 13 4 Standard error 4.2 4.1 4.8 4.1 2.2 7.1 Max. feeding distance (km) 5 17 32 31 36 30 28 21 31 31 50 56 15 7 28 14 Min. feeding distance (km) 5 4 3 2 8 3 5 6 2 2 4.7 2 2 7 4 2 Mean roost population size x103/ N 20/1 20/1 4/5 6/9 28/2 62/5 10/9 5/1 15/5 50/6 56/8 100/3 9/11 50/1 29 27 Mean feeding forest patch x103 (ha) 10.0 7.2 6.9 5.3 9.5 10.0 6.0 4.6 9.8 8.7 7.7 8.5 6.9 10.0 8 2

1 The total number of days from the date of deployment until the unit ceased functioning or until bat activity ceased (end date). 2 The total number of feeding fixes throughout the transmission period that bats were detected during night time hours (between sunset and sunrise). 3 Average duration of visits by each individual to feeding sites, defined by the dates of the first and last fixes in consecutive duty cycles from a particular individual at a particular feeding site (includes time when flying-foxes used more than one feeding site per night); this measurement is the average across N (as shown) visits for each individual. Total N = 110 visits to different sites. 4 The number of feeding records per individual bat when all 173 records were included. 5 The number of feeding records per individual bat when only the 112 independent records included.

Appendices 150

Elevation % Forest % Built % Open All feeding records1 Roost sites Elevation 1.00 % Forest 0.41** 1.00 % Built -0.42** -0.66** 1.00 % Open -0.06 -0.55** -0.26* 1.00 Feeding sites Elevation 1.00 % Forest 0.21** 1.00 % Built -0.11 -0.16* 1.00 % Open -0.13 -0.90** -0.21** 1.00 Random points Elevation 1.00 % Forest 0.29** 1.00 % Built -0.28** -0.46** 1.00 % Open -0.12 -0.77** -0.21* 1.00 Independent feeding records2 Roost sites Elevation 1.00 % Forest 0.39** 1.00 % Built -0.43** -0.64** 1.00 % Open -0.12 -0.42** -0.34* 1.00 Feeding sites Elevation 1.00 % Forest 0.14 1.00 % Built -0.10 -0.23** 1.00 % Open -0.22* -0.88** -0.20* 1.00 * P < 0.05; **P < 0.01 1All records; Roost = 173, Feeding = 173, Landscape = 100 2Independent records; Roost = 112, Feeding = 112, Landscape = 100

Appendices 151

Appendix 10 Food for thought: Flying-foxes and bush regeneration

(Published in Big Scrub Landcare Newsletter, February 2011)

Authors: Dr Kristin den Exter, Billie Roberts, Angus Underwood, Dr Len Martin

Introduction

Flying-foxes are animals of extraordinary ecological and economic importance throughout forests of the tropics playing an essential role as forest pollinators and seed dispersers (Fujita and Tuttle 1991). Flying-foxes are considered a keystone species, that is a species “whose effect is large, and one that is disproportionately large relative to its abundance” (Power et al. 1996). Flying-foxes are the original bush regenerator with enviable characteristics such as a big wingspan, and the ability to fly and forage over large distances thereby pollinating and spreading the seed of numerous species, including rainforest species (e.g. Eby 1995).

Three species of mega bats (Family: Pteropodidae) otherwise known as ‘flying-foxes’ occur in the Big Scrub; the Grey-headed flying-fox (Pteropus poliocephalus), the Black flying-fox (Pteropus alecto); and the Little Red flying-fox (Pteropus scapulatus) (Figure A10.1). Whilst the Black flying-fox has expanded its range poleward (DECCW 2009) and the Little Red is highly nomadic often occurring in great numbers, the Grey-headed flying-foxes numbers are in decline and this species is listed as vulnerable under the NSW Threatened Species Act 1995 and the Commonwealth Environment Protection and Biodiversity Conservation Act 1999. The principle reason for this population decline is habitat loss. Habitat loss leading to restricted food supplies and a lack of suitable roosting sites (DECCW 2009). Clearly there is a role for human-assisted bush regeneration to help address this problem; however this may not always be a simple task.

Appendices 152

Figure A10.3 Distribution of the flying-foxes in Australia (Source: Roberts and Hall pers comm. 2010)

The camps of flying-foxes play a number of roles in the life histories of the animals and there is a growing awareness of the need to actively manage these sites to ensure the longevity of the vegetation and its suitability as roosting habitat, and to reduce conflict between flying- foxes and humans. Although there are a number of sites that have a history of active management, these experiences have not been compiled and little information is available to guide others. A recent forum held in July 2010 in Brisbane was convened to discuss the management and restoration of flying-fox camps. The forum brought together over 80 people with an interested in camp management, focusing on maintenance and regeneration of camp vegetation. To build upon this recent forum, a panel was convened at this year’s Big Scrub Rainforest Day to discuss bush regeneration in flying-fox camps within the Big Scrub region. The aim of this paper is to take these discussions even further. Specifically we examine how to conduct bush regeneration underneath flying-foxes, particularly camps in small rainforest remnants, to reduce disturbance to the species and aid restoration of the vegetation communities.

Flying-fox feeding and roosting habitat

Flying-foxes commonly use forests and woodlands east of the escarpment in NSW and Qld as feeding habitat (Hall and Richards 2000). Current diet lists for the flying-foxes contains over

Appendices 153

100 species of trees and vines (e.g. Eby 1995). Approximately half of the plants in their diet are fleshy fruits from sub-tropical and warm temperate rainforest. The balance consists of blossoms from a range of vegetation communities dominated by Eucalypts, Melaleucas and Banksias. Flying-foxes also use a range of introduced plants – most notably commercially grown fruits. Flying-foxes travel up to 50 km per night to search for food, although typically this distance is less than 20 km (Eby 1991a; Tidemann 1999). Flying-foxes accommodate shifts in the volume and locations of food by migrating, often over large distances (Tidemann and Nelson 2004).

Flying-foxes roost during the day in large communal roosts or camps. Numbers can range from a few hundred to over 50,000 (Ratcliffe 1931; Eby et al. 1999), and are driven by the amount of food resources in the surrounding area (Ratcliffe 1931; Parry-Jones and Augee 2001). Flying-foxes exhibit strong fidelity to ‘traditional’ campsites, with some roosts being occupied for >100 years.

Although flying-foxes display a degree of flexibility in habitat choice, there are some key camp elements that are required (Ratcliffe 1931; Nelson 1965; Hall & Richards 2000; Parry- Jones and Augee 2001; Eby 2002b; Peacock 2004; Roberts 2005; Snoyman 2008) for example:

• Camps need to be positioned within nightly commuting distance (generally, <20 km) of sufficient food resources. • Camps are situated in the coastal lowlands. • Camps are commonly located in closed forest, Melaleuca swamps or stands of Casuarina and are generally found near rivers or creeks. • Camps occur in vegetation ranging from continuous forest to remnants as small as 1 ha • Typically canopy height of at least 5 m. • The microclimate characteristics of camps, such as temperature and humidity of sites, appears to be important.

There are eight known camps used by flying-foxes within the Big Scrub region. When examining the characteristics of these camps (Table A10.1) it is notable that most occur in small remnant rainforest patches. The largest continuously occupied camp is Rotary Park at 12.8 ha and the smallest is Lumley Park at 2.2 ha. These small patches present challenges to bush regenerators, managers and flying-foxes alike.

Appendices 154

Table A10.1: Attributes of known flying-fox camps in the Big Scrub, Northern NSW (Source: Roberts 2007)

Boat Harbour Wilson Nature Maguires Rotary Park Currie Park Booyong Lumley Davis Scrub Nature Reserve Reserve Creek Type 1 N H H N T H unk H Year established c. 2005 at least 1960s 1940 2003 >100 years at least 1950s c. 1990 1970s Recent usage 2 Con Con R R (twice) Ann Con R R Season occupied all year all year summer summer (Jan) not mid-winter all year unk spring/ summer Year last occupied current Sept 2005 2006 2004 2005 current mid 1990s 1992 Species 3 bks, gh bks, gh, lr bk, gh bk, gh bk, gh bk, gh bk, gh bk, gh Minimum number 2,000 0 0 0 0 0 unk 0 Maximum number 30,000 80,000 10,500 20,000 14,000 32,000 unk unk Typical number 5,000–10,000 40,000–50,000 2,000 na 6,000–7,000 6,000–7,000 2,000–3,000 unk Known maternity site yes yes no no yes yes no no Patch size (ha) 12.8 6.2 16.7 25.9 11.3 2.2 4.1 13.5 Elevation (m) 10 3 12 10 15 120 100 172 Distance to nearest adj 25 100 30 60 20 60 1,000 drainage (m) Drainage type small creek river river small creek river creek creek small creek urban (high urban (low urban (medium urban (high residential (low Surrounding area rural rural rural density) density) density) density) density) Aspect 4 SW W SE SSW F F F F 10–20, with Typical tree height (m) 20–30 12 10–20 20–25 17 10–20 20–30 emergents to 25 m Dominant tree type rainforest spp privet rainforest spp rainforest spp rainforest spp rainforest spp rainforest spp rainforest spp Dominant roost tree rainforest spp blackbean eucalyptus spp na rainforest spp rainforest spp rainforest spp rainforest spp Understorey type na weedy mixed rainforest spp na rainforest spp rainforest spp rainforest spp % canopy cover 60–70 20–30 70–80 60–70 70–80 30–40 70–80 80–90 Height roosting bks (m) 8–15 na na na 15+ 10–15 na na Height roosting gh (m) 15–25 na na na 10–15 8–12 na na

Appendices 155

1 Type N = New site established in the last decade; T = Traditional camp site. Camp used regularly for as long as we have records >100 years. Also often used as a maternity site; H = Historical site (c. 50 yr history). 2 Usage Con = Continuously occupied (year-round occupancy), Ann = Annual (the site had been occupied in 80% of years, but not continuously), Ir = Irregular (occupancy in 20–80% of years), R = Rare (occupancy has been recorder in less than 20% of years 3 Species bks = Black Flying-fox (Pteropus alecto); gh = Grey-headed Flying-fox (P. poliocephalus); lr = Little Red Flying-fox (P. scapulatus) 4 Aspect F = flat land (no aspect)

Appendices 156

Bush regeneration in Big Scrub Flying-fox Roosts

A number of issues require consideration when undertaking bush regeneration in flying-fox roost sites, for example the timing of works, the paradox of weeds as habitat and weeds as threats to vegetation community structure and health. Patch size is a major consideration when determining the appropriate course of action. Many bush regenerators are of the view that bush regeneration needs to occur in continuously occupied camps because of the increased weed infestation that invariably occurs with flying-fox occupation. The effects of continuous occupation of flying-foxes in very small patches are well known. For instance roosting in small patches causes damage to the canopy, letting in extra light, and there is also thought to be an increase in available nutrients. This disturbance leads to favourable conditions for the invasion by many weeds species, some of which are introduced by flying- foxes.

In Rotary Park (a newly established camp) regenerators have documented the invasion of a new suite of weeds possibly brought in flying-foxes including Giant Devil’s Fig, seedling of seeded bananas, Cockspur, Guava, Cocos Palm, Alexandra Palms etc (Rosemary Josephs pers comm. 2010). At Lumley Park, flying-foxes are estimated to have had a significant impact on canopy health in approximately half the site. The extra light, nutrient and weeds make restoration of this already small patch, more difficult. However, the lower and mid layers of the forest have recovered well despite continuous use by flying-foxes with a substantial revegetation effort (Darren Bailey, pers comm. 2010). Addressing the influx of new weeds may mean that greater resources are required for weed control than just at maintenance level (Heidi Lunn, pers comm. 2010).

In terms of flying-fox habitat, weeds may prove allies where core vegetation is already under pressure from roosting flying-foxes. Flying-foxes will roost in weed species, as they show no selection preferences for tree species (Roberts 2005). For example in Rotary Park, flying- foxes have been observed roosting in mature Large Leaved Privets (Rosemary Josephs pers comm. 2010). Lower stratum weeds even morning glory, are known to be used during heat events. There are numerous examples of places where understory weeds have been removed and the habitat made unsuitable for Flying-foxes.

Appendices 157

If weeds are left in core remnant vegetation then the viability and ongoing succession of the community is likely to be affected. From the bush regeneration perspective, the long-term sustainability of the vegetation patch can only be achieved through weed control of the understory weeds. So how do we accommodate dual goals of restoring Big Scrub remnants with sustainable flying-fox roosts? Can we maintain and create flying-fox habitat without the help of weeds? Is it a matter of allowing (some) weeds to stay in some places but not others? The questions are complex and often hotly contested, with or without the added complexity of flying-foxes.

When discussing this amongst practitioners it is clear that many now consider it unwise to be advocating a sudden and total removal of all weed species unless the site warrants it. There are many reasons for the staged, gradual and strategic removal of weed species, flying-fox habitat requirements are just another consideration to take into account for some sites. Opportunities arise over the longer time frame when continuously occupied camps are ‘abandoned’ for a short period of time. It is at these times that bush regeneration work that could not be done under occupation can be acted on. The key is to have the resources to be able to act at that time. This may currently be the case for Lismore’s Currie Park.

In larger patches it appears that neither the weed nor canopy health issues are quite as critical. For example, at Booyong flying-foxes impact on the site is considered to be minimal, due to the large remnant size, small flying-fox population and the fact the core roosting area shifts through time. Flying-foxes are thought to still bring in Cocos Palm, Devils Fig and White Passionflower to this site but according to bush regenerators the level is manageable (Darren Bailey pers comm. 2010). So it seems logical that if the issues are lessened in the larger remnants that we look to increase the patch size of our smaller sites, but the question is how, especially when many of these remnants have confined boundaries.

The topic of how to increase the size of the smaller remnants provided for an interesting discussion between the panel and the audience at Big Scrub Day including actively planting non-rainforest species, for example fast growing Eucalypts, in areas within existing reserve boundaries but away from core remnant vegetation, and even allowing the weeds to take their course, thereby providing the kind of vegetation structure required for flying-fox roosts (i.e. emergent trees about a dense understorey). This issue becomes more complex when considering most of the Big Scrub remnants are Endangered Ecological Communities and

Appendices 158

contain a range of threatened plant species. Whatever the management approach is it must consideration the conservation of the range of species that are threatened in the area.

Whether the goal is to manage human flying-fox conflicts or to increase vegetation resilience to flying-fox roosting, there is consensus that we need to look at expanding the current sites. Some bush regenerators estimate that, whether the goal is to manage human flying-fox conflicts or to increase vegetation resilience to flying-fox roosting, there is consensus that we need to look at expanding the current sites. Some bush regenerators estimate that in the Big Scrub region it may only take between 10–20 years, depending on the site, maintenance regimes, and species selection, for plantings to be utilised by flying-foxes. Large scale planting of rainforest trees has already been shown to provide habitat for flying-foxes at Fernleigh. Planting of mixed species rainforest trees along a riparian strip has been ongoing at a site managed by Mark Dunphy since 1991, which has created an area that has been used as a roost site for up to 500 Black flying-foxes (Angus Underwood, pers. obs. 2009). The flying- foxes are regularly present at the site, which is around 100 m wide, roosting in both remnant trees at the top of a gully, as well as the surrounding emergent planted trees including Cudgerie, Hoop Pine and Blue Quandong.

Past Recommendations

When considering expanding roost habitat it would also be useful to know more about which tree species are more resilient to flying-fox roosting, or indeed may respond to flying-fox presence. It is critical to any such endeavours that the resources currently allocated for core vegetation work must not be re-directed, as this work is essential to the long term sustainability of the vegetation community. More resources are required to assist in the expansion of the vegetation structure required for flying-fox roosts, and we argue here that continuously occupied, maternity roosts in small remnants should be the priority.

In our view the best practice management approach for bush regeneration under continuously occupied flying-fox roosts would be: 1) make an assessment of the impacts to flying-foxes of vegetation structure change that may occur as a result of bush regeneration before undertaking any works; and 2) taking a staged approach to any weed removal. As well as the staged removal of weeds, a number of other strategies can be employed to minimise the impact of bush regeneration on roosting flying-foxes, including the timing of works (preferably between

Appendices 159

May–July), eliminating the use of machinery and camp monitoring. Firstly, let’s look at the timing of works.

Working in the breeding season is an obvious issue that needs to be considered. Other than hoping and waiting for the site to be “abandoned” (discussed above) there are some other options: 1) Not to carry out works under active flying-fox maternity roosts during the breeding season; 2) Not to carry out works within a reasonable distance of active flying-fox maternity roosts during the breeding season; and 3) To continue only necessary works and to do this as quietly as possible with continual monitoring for signs of disturbance/distress.

Whilst it might seem an obvious course of action to go with options 1 or 2 this may present problems for some practitioners working on core vegetation weed control within continuously occupied maternity roosts. As with many protocols it may not be that a one size fits all approach will work, so any guidelines need to allow for some flexibility and feedback with regards to site context. Critical breeding and maternity season (Sept–March) is also prime weed control season. Canopy and roost height can also be variable, for example Booyong has a high canopy compared with many camps in coastal swamp forests, and disturbance levels can be lower under some higher roosting camps. So in some cases perhaps option three is the practical way to go? In any case, if work is required directly under a camp this should be carried out in a way to minimise the impacts on the camp. Work team should be small in size, noise level and time within camp should be kept to a minimum.

Using powered or noisy machinery is not such a complex issue. Machinery, such as chainsaws, brushcutters and generators that are likely to disturb flying-foxes should not be used in and around occupied camps, particularly during the breeding times. Hand tools are preferred, but we re-iterate that an assessment be made of the impacts to flying-foxes of vegetation structure change before undertaking such activities, that a staged approach be taken to any weed removal and that no disturbance should be made to trees in which flying-foxes roost.

Whatever the course of action taken, it is important to be able to monitor what is happening in the flying-foxes camp in terms of behaviour etc as well as what is happening with respect to canopy and weeds. It is important that bush regenerators working in flying-fox camps know what to look for, for example to know what constitutes normal behaviour and what constitutes ‘disturbance’ or ‘distress’. This may involve bringing in ecologists to talk with bush

Appendices 160 regeneration teams. The recent initiative by Byron Shire Council is one example which involved flying-fox ecologist Billie Roberts presenting two free seminars on flying-fox ecology to both council staff and members of the public. In addition to this a set of guidelines have been developed for bush regenerators working in and around flying-fox camps which aims to minimise the impacts on both flying-fox camps and the OH&S risks on workers.

Finally let’s turn to what bush regenerators can do to minimise the OH&S risks. A site OH&S risk assessment should be undertaken to determine the appropriate level of personal protective equipment required. It is currently the practice of some to wear an outer layer of clothes (at least an overshirt) while working under flying-foxes. If workers find injured or sick flying- foxes local wildlife carers should be contacted immediately. Workers should not touch or handle flying-foxes. If a worker is bitten or scratched wash the wound thoroughly with soap and water for at least five minutes and inform a doctor immediately.

The authors welcome feedback and response to this article, as we see it, the conversation has just begun.

References

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Acknowledgements

Thanks to Rosemary Josephs, Darren Bailey, Heidi Lunn for providing comments on those tricky questions of bush regeneration in flying-fox colonies, thanks to Peggy Eby, Billie Roberts and Liz Gould for the Flying-fox Forum and to Lib Ruytenberg (WIRES Northern Rivers) for her comments on flying-fox behaviour.

Appendices