Conservation of Australian Insectivorous Marsupials

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Conservation of Australian insectivorous marsupials:

biogeography, macroecology and life history

Rachael A. Collett

BSc Hons

A thesis submitted for the degree of Doctor of Philosophy at The University of Queensland in 2018 School of Biological Sciences ABSTRACT

The insectivorous marsupial Family Dasyuridae is endemic to Australia and Papua New Guinea. Dasyurids have a variety of life history strategies and are found in a wide range of habitats, latitudes and elevations. This makes them useful for exploring life history evolution, biogeographical patterns and macroecological theory. The life history and persistence of dasyurids are thought to be tightly linked to the distribution of their arthropod prey in space and time, but we currently have a limited understanding of the mechanisms. Arthropods are declining globally, and evidence suggests that climate change is already linked to changes in arthropod availability in the northern hemisphere. Understanding the relationship between insectivorous marsupials and their arthropod prey has become particularly important, as in 2018 two species from the dasyurid genus Antechinus were federally listed as endangered, and populations of other dasyurids appear to be declining across Australia.

The aim of this thesis was to combine biogeography, macroecology and life history to determine what is influencing the distribution and persistence of Australian insectivorous marsupials from the Family Dasyuridae, with a focus on antechinus species in Queensland. I addressed evolution, rarity patterns and phenological relationships between dasyurid marsupials and their arthropod prey.

Chapter 2 investigated how life history traits co-vary and are related to climatic variables, specifically how the evolution of dasyurid life history is related to productivity and predictability, and how environmental drivers are linked to patterns of life history variability. Based on analysis of data on life history characteristics of female dasyurids throughout Australia, there was evidence of two life history axes. The reproductive output axis including litter size and supernumerary young was related to annual rainfall and productivity, while position on the semelparity – iteroparity axis was associated with predictability of rainfall and arthropod availability. These results suggested how climate change might affect dasyurid marsupials and provide a broader understanding of their life history evolution that can be applied in a global context.

Previous global and Australian studies have found that population density in mammals is lower in the tropics than at temperate latitudes. Chapter 3 tested whether dasyurids show a latitudinal gradient in population density, focusing on antechinus population density across latitudes and elevations in Queensland. Data from the literature, combined with intensive trapping and arthropod sampling showed that dasyurids were rarest in the tropics

i and that antechinus population density was lowest at low latitudes and elevations. Population density was constrained by winter arthropod availability, which was associated with winter rainfall. High elevation sites maintained high arthropod availability throughout the year because they received orographic rainfall. These results help to explain rarity of antechinus species in the seasonal subtropics and tropics, including the Endangered silver-headed antechinus (A. argentus) in central Queensland, and the restricted Atherton antechinus (A. godmani) and rusty antechinus (A. adustus) in far north Queensland. The results also highlight the importance of Australian mountain-tops as refuge areas for insectivorous marsupials.

Chapter 4 focused on timing of breeding and distribution of antechinus species across mountains in Queensland. I used the same data collection approaches as in chapter 3 to determine timing of breeding, evolutionary age of antechinus and arthropod availability across elevations and latitudes. The results demonstrated that antechinus in Queensland do not rely solely on photoperiodic cues to trigger breeding. They are able to use local environmental conditions to time breeding so that lactation coincides with timing of peak arthropod availability. Timing of antechinus breeding and flushes in arthropod availability occurred progressively later as elevation increased. More ancient Antechinus species had small ranges on mountain-tops and less flexible breeding seasons. Taken together, these results suggest that in Queensland, ancient antechinus species restricted to high elevations are likely to be most at risk from climate change, if the timing of peak arthropod availability changes.

This thesis has contributed to life history, biogeography and macroecology theory at large and small spatial scales. It has enhanced our understanding of the relationship between dasyurid marsupials and their arthropod prey, and provided important information that can help us to deduce why certain dasyurids are rarer than others.

DECLARATION BY AUTHOR

This thesis is composed of my original work, and contains no material previously published or written by another person except where due reference has been made in the text. I have clearly stated the contribution by others to jointly-authored works that I have included in my thesis.

I have clearly stated the contribution of others to my thesis as a whole, including statistical assistance, survey design, data analysis, significant technical procedures, professional editorial advice, financial support and any other original research work used or reported in my thesis. The content of my thesis is the result of work I have carried out since the commencement of my higher degree by research candidature and does not include a substantial part of work that has been submitted to qualify for the award of any other degree or diploma in any university or other tertiary institution. I have clearly stated which parts of my thesis, if any, have been submitted to qualify for another award.

I acknowledge that an electronic copy of my thesis must be lodged with the University Library and, subject to the policy and procedures of The University of Queensland, the thesis be made available for research and study in accordance with the Copyright Act 1968 unless a period of embargo has been approved by the Dean of the Graduate School.

I acknowledge that copyright of all material contained in my thesis resides with the copyright holder(s) of that material. Where appropriate I have obtained copyright permission from the copyright holder to reproduce material in this thesis and have sought permission from co-authors for any jointly authored works included in the thesis.

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LIST OF PUBLICATIONS AND PRESENTATIONS DURING CANDIDATURE

Peer Reviewed Papers

Collett, R.A.; Baker, A.M. and Fisher, D.O. (2018) Prey productivity and predictability drive different axes of life history variation in carnivorous marsupials. Proceedings of the Royal Society of London B: Biological Sciences, 285(1890), 20181291.

Collett, R.A. and Fisher, D.O. (2017) Time-lapse camera trapping as an alternative to pitfall trapping for estimating activity of leaf litter arthropods. Ecology and Evolution, 7(18), 7527–7533.

Conference Abstracts

Collett, R.A. (2016) Antechinus and their prey on mountainsides. The Australian Mammal Society conference. Alice Springs, NT - September 2016.

Collett, R.A. and Fisher D.O. (2017) Camera trapping as an alternative to pitfall trapping to sample prey availability of insectivorous mammals. 12th International Mammological Congress. Perth, WA - July 2017.

Collett, R.A. and Fisher D.O. (2017) Rarity and resource availability for insectivorous mammals. Society of Conservation Biology conference. Cartagena, Colombia - August 2017.

Collett, RA. (2018) Life history variation and extinction risk of carnivorous marsupials. UQ School of Biological Sciences postgraduate conference. Stradbroke Island, QLD - February 2018.

Collett, R.A.; Baker, A.M. and Fisher, D.O. (2018) Prey productivity and predictability drive different axes of life history variation in carnivorous marsupials. The Australian Mammal Society conference. Brisbane, QLD – July 2018.

PUBLICATIONS INCLUDED IN THIS THESIS

No publications included.

MANUSCRIPTS INCLUDED IN THIS THESIS

Chapter 2:

Collett, R.A.; Baker, A.M. and Fisher, D.O. Prey productivity and predictability drive different axes of life history variation in carnivorous marsupials. Proceedings of the Royal Society of London B: Biological Sciences.

Contributor Statement of Contribution

Rachael Collett Conceived the idea for the study (85%)

Analysed the data (95%)

Wrote the paper (80%)

Diana Fisher Conceived the idea for the study (15%)

Wrote and edited the paper (15%)

Andrew Baker Wrote and edited the paper (5%)

Simon Blomberg Advised statistical analyses and statistical paper revisions (5%)

Chapter 3:

Collett, R.A.; Baker, A.M. and Fisher, D.O. Winter food availability explains rarity of tropical and lowland species.

Contributor Statement of Contribution

Rachael Collett Conceived the idea for the study (90%)

Analysed the data (100%)

Wrote the paper (85%)

Diana Fisher Conceived the idea for the study (10%)

Wrote and edited the paper (10%)

Andrew Baker Wrote and edited the paper (5%)

Eugene Mason Provided data for the study

Chapter 4:

Collett, R.A.; Baker, A.M. and Fisher, D.O. Do resource pulses drive latitudinal and elevational timing of breeding in the insectivorous marsupial genus Antechinus?

Contributor Statement of Contribution

Rachael Collett Conceived the idea for the study (90%)

Analysed the data (99%)

Wrote the paper (85%)

Diana Fisher Conceived the idea for the study (10%)

Wrote and edited the paper (10%)

Andrew Baker Wrote and edited the paper (5%)

Simon Blomberg Advised statistical analyses (1%)

Eugene Mason Provided data for the study

Emma Gray Provided data for the study

CONTRIBUTIONS BY OTHERS TO THE THESIS

The multidisciplinary nature of this thesis has warranted input from a broad spectrum of academics and fellow students. The most important contributions are listed below.

Eugene Mason and Emma Gray suggested study locations for field surveys at Kroombit Tops National Park and Springbrook National Park and provided additional data on litter size, population density and breeding timing of Antechinus argentus and Antechinus arktos. Emma Gray patiently trained me in Antechinus handling. Thomas Mutton provided data on the lineage age of Antechinus species.

Simon Blomberg advised the use of phylogenetic generalised least squares models for chapter 2 and the use of appropriate generalised linear models for chapter 4.

April Reside provided rainfall raster data and assisted with using Geographical Information Systems for chapter 2.

Ayeesha McComb created Antechinus stuartii and Antechinus arktos illustrations, and the infographic in chapter 4.

STATEMENT OF PARTS OF THE THESIS SUBMITTED TO QUALIFY FOR THE AWARD OF ANOTHER DEGREE

None

RESEARCH INVOLVING HUMAN OR ANIMAL SUBJECTS

The data collection protocols used in this thesis were assessed and approved by the Animal Ethics Committee at the University of Queensland (AEC approval number SBS/174/15/UQ/NESP). Data collection was approved by the Queensland Government under research permit numbers TWB/17/2015, WITK16151715 and WISP16146415. The certificate of ethics approval can be found in the appendices.

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ACKNOWLEDGMENTS

I sincerely thank my supervisors and advisors for their research mentoring and financial support during my candidature. Diana Fisher’s support allowed me to pursue my studies with academic freedom. Diana always advocated for me and worked tirelessly to correct my drafts. Andrew Baker shared his incredible antechinus knowledge and was meticulous with corrections. Robbie Wilson provided me with additional diverse expertise, advice and perspectives.

I owe a great deal of gratitude to Emma Gray, Eugene Mason and Thomas Mutton who assisted me in using their field sites, taught me how to handle antechinus and generously shared their data and knowledge. Thanks to Queensland Parks and Wildlife at Springbrook National Park, Kroombit Tops National Park and Danbulla National Park who provided lodging during field trips and access to their parks. This project would not have been possible without the help of numerous field volunteers, with special thanks to: Zoe Febicoski, Kate Garland, Pippa Kern, Natalie Freeman, Alexandra Ainscough, James Graham, Bianca op den Brouw, Jesse Rowland, Gabrielle Lebbink, Maddie Castles, Molly Gilmour and Aliesha Dodson. I particularly acknowledge volunteers who got leeches in their eyes, serious cases of scrub itch or caught no antechinus. Thanks to the Malone family, Alexandra Ainscough and Jesse Rowland for lending me vehicles and providing places to stay in north Queensland. Simon Blomberg, James McCarthy and Maddie Castles patiently assisted me with R scripting and graphing. Thanks to Renee Rossini for being a fellow biogeographer, providing input on my manuscripts and allowing me to rant about my ideas. Thanks to Ayeesha McComb for her beautiful natural history illustrations and infographics, and help with all things artistic throughout the PhD.

Lastly, I would like to thank my close friends Gabby Lebbink, Maddie Castles, Alex Ainscough and many others who made my PhD a fun, laugh filled experience, and my family for always encouraging me to pursue my interests.

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FINANCIAL SUPPORT

This research was supported by an Australian Government Research Training Program Scholarship.

Fieldwork was supported by the Australian Research Council (Grant/Award Numbers: FTll010019 and DP150100198), the Australian Government’s National Environmental Science Program through the Threatened Species Recovery Hub.

KEYWORDS

Biogeography, dasyurid, antechinus, rarity, life history, mammal, Australia, arthropod, climate change, insectivorous.

AUSTRALIAN AND NEW ZEALAND STANDARD RESEARCH CLASSIFICATIONS (ANZSRC)

ANZSRC code: 060208 Terrestrial Ecology 40%

ANZSRC code: 060302 Biogeography and Phylogeography 20%

ANZSRC code: 060311 Speciation and Extinction 40%

FIELDS OF RESEARCH (FOR) CLASSIFICATION

FoR Code: 0602 Ecology 40%

FoR Code: 0603 Evolutionary Biology 60%

TABLE OF CONTENTS

ABSTRACT ...... i DECLARATION BY AUTHOR ...... iii LIST OF PUBLICATIONS AND PRESENTATIONS DURING CANDIDATURE ...... iv PUBLICATIONS INCLUDED IN THIS THESIS ...... v CONTRIBUTIONS BY OTHERS TO THE THESIS ...... vii STATEMENT OF PARTS OF THE THESIS SUBMITTED TO QUALIFY FOR THE AWARD OF ANOTHER DEGREE ...... vii RESEARCH INVOLVING HUMAN OR ANIMAL SUBJECTS ...... vii ACKNOWLEDGMENTS ...... viii FINANCIAL SUPPORT ...... ix KEYWORDS ...... x AUSTRALIAN AND NEW ZEALAND STANDARD RESEARCH CLASSIFICATIONS (ANZSRC) ...... x FIELDS OF RESEARCH (FOR) CLASSIFICATION ...... x LIST OF FIGURES ...... xiv LIST OF APPENDICES ...... xv LIST OF ABBREVIATIONS USED IN THE THESIS ...... xvi CHAPTER 1: General Introduction ...... 1 Thesis aims ...... 2

Biogeography and macroecology ...... 2

Life history ...... 3

Latitudinal gradients ...... 5

Mountains and elevational gradients ...... 6

Speciation and distributions ...... 7

Extinction risk, life history, ecology and climate change ...... 8

Dasyuridae and the genus Antechinus ...... 9

Study scope ...... 12

Study sites ...... 13

Thesis outline ...... 14

CHAPTER 2: Prey productivity and predictability drive different axes of life history variation in carnivorous marsupials ...... 16 Abstract ...... 17

Introduction ...... 18

Methods ...... 20

Results ...... 22

Discussion ...... 27

CHAPTER 3: Winter food availability explains rarity of tropical and lowland species ...... 30 Abstract ...... 31

Introduction ...... 32

Methods ...... 35

Results ...... 38

Discussion ...... 44

Conclusions ...... 48

CHAPTER 4: Do resource pulses drive latitudinal and elevational timing of breeding in the insectivorous marsupial genus Antechinus? ...... 49 Abstract ...... 50

Introduction ...... 51

Methods ...... 54

Results ...... 56

Discussion ...... 62

CHAPTER 5: Discussion and final remarks ...... 66 General discussion ...... 67

Climate change and life history ...... 68

Distribution of food in time and space ...... 71

Rarity and food availability ...... 71

Dasyurid species at risk ...... 72

Concluding remarks ...... 73

REFERENCES ...... 76 APPENDICES ...... 105 xii

Appendix A ...... 106

Appendix B ...... 113

Appendix C ...... 115

Appendix D ...... 116

Appendix E ...... 135

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LIST OF FIGURES

Figure 1.1. Distribution of antechinus species in Queensland...... 12

Figure 2.1. The association between litter size and partial residuals of mean annual rainfall for Australian insectivorous dasyurid species...... 23

Figure 2.2. The association between log female maximum lifespan and partial residuals of sin Colwell's predictability index of rainfall for Australian insectivorous dasyurid species...... 24

Figure 2.3. The association between log10 length of the breeding season and partial residuals of sin Colwell's predictability index of rainfall for Australian insectivorous dasyurid species...... 25

Figure 2.4. The centroid point of the geographic range of dasyurid species included in this study and mean annual rainfall throughout Australia...... 26

Figure 3.1. Antechinus trapping and arthropod monitoring locations in Queensland..... 41

Figure 3.2. Popuation density of insectivorous dasyurids in forests on Australia's east coast...... 42

Figure 3.3. Population density of antechinus including 95% confidence intervals at low, medium and high elevations at four locations from 17°S to 28°S...... 43

Figure 3.4. Total winter rainfall (mm) and winter arthropod availability (total counted on cameras) in the lowest month including standard errors at four locations from 17°S to 28°S...... 44

Figure 4.1. Number of arthropods and Julian week when antechinus species have their young in the nest from low latitude (top) to high latitude (bottom) 1. Danbulla National Park 2. Kroombit Tops National Park 3. Conondale National Park 4. Springbrook National Park...... 58

Figure 4.2 Antechinus distribution across mountains and lineage age of species (my = million years) captured in this study at Springbrook National Park (28°S), Conondale National Park (26°S), Kroombit Tops National Park (24°S) and Danbulla National Park (17°S)...... 62

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LIST OF TABLES

Table 3.1. Lowest elevation detected (m) and elevations sampled for antechinus species at four locations...... 40

Table 4.1. Mixed linear models showing the association between altitude and latitude on Julian week antechinus commence breeding, Julian week arthropod availability is highest, and antechinus evolutionary age (BEAST)...... 57

LIST OF APPENDICES

Appendix A Dasyurid life history data and the literature data was taken from for Chapter one.

Appendix B Site locations, survey periods and effort (total trap nights) for one live and two camera trap captures of Sminthopsis Leucopus in north Queensland.

Appendix C 2016 captures of Antechinus godmani and Antechinus adustus at sites within their historical distribution in north Queensland.

Appendix D Time-lapse camera trapping as an alternative to pitfall trapping for estimating activity of leaf litter arthropods.

Appendix E Animal ethics approval certficiate.

LIST OF ABBREVIATIONS USED IN THE THESIS

BEAST Bayesian evolutionary analysis sampling trees

EPBC Environment Protection and Biodiversity Conservation Act 1999

ID Identification

MY Million years

Nha Number per hectare

N.P National Park

PC Personal communication

PGLS Phylogenetic generalised least squares

PTR Personal trapping records

UK United Kingdom

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CHAPTER 1: General Introduction

Image: Natural history illustration of the Endangered Antechinus arktos by Ayeesha McComb.

Thesis aims

The overall aim of this project is to combine biogeography, macroecology and life history to determine what is influencing the distribution and persistence of Australian insectivorous marsupials from the Family Dasyuridae, with a focus on antechinus species in Queensland. The results will help us understand why there are three threatened antechinus species restricted to mountain tops, why some insectivorous marsupial species are rare and others common, and which species will be most threatened by climate change. This will be achieved by addressing life history evolution, rarity patterns, and phenological relationships between insectivorous marsupials and their arthropod prey.

The thesis has four main aims:

1. Identify environmental correlates of life history evolution in Australian dasyurids. 2. Determine factors that limit dasyurid population density across latitude and elevation. 3. Understand factors influencing antechinus distribution across elevation. 4. Combine this knowledge to determine what influences dasyurid and antechinus rarity, and identify species that may be particularly threatened by climate change.

Biogeography, macroecology and life history approaches can be combined to understand patterns and processes of species distribution, abundance and biological cycles over a variety of spatial scales (Wiens & Donoghue, 2004). These fields have high potential for application to conservation, because they can help us understand rarity and identify geographic areas that are important to preserve (Isaac, 2009; Whittaker et al., 2005).

Biogeography and macroecology

Biogeography includes aspects of evolution, taxonomy, ecology, geology, palaeontology, and climatology. This field involves investigating current and historical species distributions, and the processes that have led to these distributions. Biogeography can be divided into two categories: ecological and historical. Ecological biogeography is concerned with shorter time periods and smaller scales, and asks questions such as why a species is confined to its present range, and what enables the species to persist in an area. Historical biogeography involves evolutionary time periods and larger areas. It aims to answer questions such as how a species came to be confined to its current range, and clarify the evolutionary relationships between species (Cox et al., 2000). Recent advances

2 in molecular methods and cladistic techniques have enhanced our understanding of species relationships, including dates of divergence from known common ancestors (Cox et al., 2000; Hufnagel, 2018). Current trends and topics of importance in biogeography include understanding where biodiversity is greatest (Fine, 2015; Willig et al., 2003), where it is under threat (Jenkins et al., 2013; Venter et al., 2016) and how climate change might affect biodiversity and species distributions (Ackerly et al., 2010; Urban, 2015).

Macroecology investigates large scale patterns of species abundance and distribution (Gaston & Blackburn, 2008; Maurer, 1999), to identify factors that influence the structure and function of ecological systems (Blackburn & Gaston, 2002). Macroecology takes a broader view of ecosystems to understand questions that intersect ecology, biogeography and macroevolution (Brown, 1995). Some of the predominant patterns that macroecologists aim to explain are: altitudinal gradients in species richness, range size– niche breadth relationships, extinction–range size relationships, latitudinal gradients in geographical range size (Rapoport’s rule) and abundance–range size relationships (Gaston & Blackburn, 2008). There is a current focus and recent progress in understanding patterns of abundance (Novosolov et al., 2016; Santini et al., 2018) and distribution–abundance relationships (Slatyer et al., 2013; Steenweg et al., 2018).

Life history

Life history theory seeks to understand the evolution of species schedules of growth, reproduction and survival (Stearns, 1992). Life history characteristics include traits such as size at birth, age of first reproduction, reproductive seasonality, gestation length, fecundity and lifespan. These traits often co-vary. Life history characteristics are related to fitness because they dictate how many reproducing descendents an individual may leave (Roff, 2002).

Selection does not produce species that begin reproducing at birth, have infinite reproductive rates and live forever, because of constraints (Law, 1979). Limitations on the evolution of traits can include laws of physics, phylogenetic history and development, physiological function, limited energy and nutrient budgets, ability to repair oxidative damage and mutations, and genetic associations such as antagonistic pleiotropy in which a gene has multiple opposing effects on fitness (Brown & Sibly, 2006; Roff & Fairbairn, 2007; Stearns, 1983). Constraints on life history traits cause trade-offs, where a change in one life history trait resulting in an increase in fitness will lead to other life history traits changing in a way that reduces fitness (Van Noordwijk & de Jong, 1986). Life history 3 theory focuses on understanding the most important constraints and tradeoffs, their genetic and physiological mechanisms, and ecological drivers (Flatt & Heyland, 2011; Read & Harvey, 1989).

A crucial trade-off in life history theory is between current and future reproduction, and survival. If an organism invests in current reproduction, it will reduce future reproductive potential and /or shorten its lifespan. The major physiological model to explain why this occurs has been the disposable soma theory, or Y-model of resource allocation. This theory states that an organism has limited resources to allocate either to reproduction or somatic maintenance, so that increased investment in reproduction decreases investment in somatic repair, reducing survival (Kirkwood, 1992; Kirkwood & Holliday, 1979). At the physiological level, important resources for physiological function are often considered to be energy or nutrients (Johnson et al., 2001; Speakman, 2008), but may also be related to repair or immunity (Gems & Doonan, 2009; Zhang et al., 2009). Many aspects of life history remain unresolved. For example, recent physiological research disputes the Disposable Soma Theory and proposes that energy supplies in the environment are often unlimited, and animals are constrained by their capacity to dissipate body heat (Król et al., 2003; Speakman & Król, 2010).

Major life history trade-offs that have been intensively studied are: 1) current reproduction versus survival, future reproduction and growth; and 2) number of young versus their size. Consistent trade-offs between these life history traits means that species typically occur on single continuum from fast - slow (Gaillard et al., 1989). For example, the African elephant (Elephas maximus) is defined as a slow species because it is long lived, has a lengthy gestation period and only produces a single offspring during each reproductive attempt (Brown et al., 2000; Gaillard et al., 2016; Schmidt-Nielsen, 1984). Ecology and the environment are often related to species life history strategies. For example, food (Fisher et al., 2001), predators (Virgos et al., 2006; Wilkinson & South, 2002) and other drivers of extrinsic age-specific mortality (Ghalambor & Martin, 2001; Martin, 1995; Reznick et al., 2004) are important factors in the evolution of life histories. Evidence suggests that there might be more than one axis of life history variation (Bielby et al., 2007), and this is a promising research area for advancing life history theory.

One area of life history research that has received much attention is predicting litter or clutch size. Lack (1947) proposed the first theory of clutch size, which states that a birds’ clutch size should maximise the number of surviving offspring. Parents will be unable to

4 rear their offspring if they produce a large clutch and cannot provide enough food, and individuals will lower their fitness if their clutch is too small. Trade-offs between current reproduction and parental survival, current and future reproduction, and the number and size of offspring mean that clutch size is usually smaller than the ideal clutch (Lack 1947). For example, across mountains birds at high elevation have smaller clutches than birds at low elevation but invest in offspring quality by providing more parental care (Badyaev & Ghalambor, 2001). This may be related to low food availability or increased predation at high elevation, where having a small clutch and enhanced parental care increases the likelihood of offspring surviving in a harsh environment (Badyaev & Ghalambor, 2001; Ghalambor & Martin, 2001).

A second fundamental topic of life history research is predicting how many times an individual should reproduce. Natural selection should lead to iteroparity (multiple reproductive cycles over the course of a lifetime) and a long reproductive lifespan if adult survival is high and juvenile survival is low (Reznick et al., 2004). High mean adult survival increases the number of reproductive events possible per lifetime and low juvenile survival selects for more reproductive attempts (Virgos et al., 2006; Wilkinson & South, 2002). In females, semelparity or short reproductive lifespan is selected by low mean adult survival and high juvenile survival. For example, high adult mortality of Tasmanian devils (Sarcophilus harrisii) caused by devil facial tumour disease has resulted in earlier age of maturity and most females only reproducing once in their lifetime (Jones et al., 2008).

Latitudinal gradients

One of the main themes in biogeography and macroecology is understanding why there are patterns in the distribution, diversity and abundance of species over latitudinal gradients (Lomolino & Brown, 2004). Terrestrial biodiversity generally increases from temperate zones to the tropics, and tropical species often have smaller ranges and lower population densities than their temperate counterparts (Stevens, 1989). The increase in diversity at low latitudes has been attributed to increasing plant productivity (Hillebrand, 2004; Saugier, 2001; Willig et al., 2003), as net primary productivity (NPP) is directly affected by temperature and precipitation which tend to increase towards the equator (Ciais et al., 2001; Holdridge, 1947). However, recent evidence suggests that primary productivity may actually peak between 30° and 50, because length of the growing season has more influence on NPP than climate variables (Huston & Wolverton, 2009; Michaletz et al., 2018).

Tropical species are thought to have smaller ranges than temperate species because the high diversity of the tropics reduces niche size and increases ecological specialisation (Hubbell, 2001; Slatyer et al., 2013; Vázquez & Stevens, 2004). Species with smaller ranges have lower population densities (Brown, 1984; Gaston, 1996). The predominant theories to explain this pattern are: 1) range position – both abundance and occupancy often decline towards the edge of a species’ range (Lawton, 1993; Safriel et al., 1994); 2) resources - variation in food supply causes the distribution and abundance of species to change in synchrony (Gaston et al., 1997; Hanski, 1993); and 3) population dynamics - rate of immigration has been shown to increase with greater patch occupancy (Gaston et al., 2000; Hanski & Gyllenberg, 1993). Small ranges and low abundances may put tropical species at greater risk of extinction (Brown, 1995; Fisher & Owens, 2004), making it particularly important to continue researching why these biogeographical patterns occur.

Mountains and elevational gradients

Biogeographers and macroecologists also investigate ecological effects of mountains, as they provide habitat for a large number of species, and have great variation in environmental variables such as temperature and rainfall over small geographic areas. This makes them an ideal landscape for deducing how the environment is associated with species distribution and abundance (Currie & Kerr, 2008; Körner, 2007; McCain, 2004). Elevational gradients often show similar biogeographical patterns to latitudinal gradients (MacArthur, 1984), so studying ecological processes on mountains can help us understand the mechanisms that influence latitudinal trends.

Explanations for species distributions over elevational gradients have largely focused on vegetation, climate or physical boundaries (Bateman et al., 2010; Sánchez-Cordero, 2001; van Ingen et al., 2008), and modelling of species physiological niches (Chen, 2008; Hernandez et al., 2008; Parra & Monahan, 2008). However, food availability (Rickart et al., 1991), competition between species (Dickman, 1986; Pigot & Tobias, 2013), and ability to adapt to new abiotic and biotic conditions (Galbreath et al., 2009; Gür et al., 2018; Waltari & Guralnick, 2009) also affect species distributions and how successfully they may persist in an area. For example, Rickart et al. (1991) found that the distribution of insectivorous mammals on a Philippine mountain was dependant on food availability. High elevation, detritus rich forests were favoured by insectivorous species because of the abundance of earth worms. For small mammals living in cold high elevation sites, a large energy intake is necessary for successful thermoregulation, suggesting that food availability may be

6 particularly important for persistence (Geiser, 1988). Most studies of elevational gradients have focused on the diversity and distribution of species, rather than abundance. Studies of species abundance across mountains are likely to reveal important information about factors that limit population density.

Mountains are important for conservation, as they are highly biodiverse and support many species with small geographic ranges, due to speciation promoted by isolation between valleys and mountain-tops. Mountain-tops can act as climate refugia (Reside et al., 2013). Climate refugia are stable habitats where species are able to persist with changing climatic conditions (Keppel et al., 2012; Keppel & Wardell‐Johnson, 2012) and are often areas that have allowed species to survive past climatic changes (Tzedakis et al., 2002). As the earth warms, cool adapted forests are retreating up mountains, and species that use these habitats are also being pushed higher in elevation. Persistent, cool adapted forests are important as refugia, as they can host mountain top specialists and mid elevation species experiencing range shifts (Parmesan & Yohe, 2003).

Speciation and distributions

Allopatric (or vicariant) speciation occurs when populations become separated, leading to reproductive isolation and genetic divergence (McCormack et al., 2010; White, 1978; Wiens, 2004). Vicariance can be caused by geological change, such as the building of a mountain range, or by large climatic oscillations which influence the distribution of flora and fauna. If climatic change alters vegetation this can lead to species range contractions, speciation and sometimes subsequent expansion (Wiens & Donoghue, 2004). Species distributions are thus influenced by evolution in changing environments, so they can reflect species age and the climatic history of a region (Byrne et al., 2011; Fjeldsaå & Lovett, 1997; Roelants et al., 2004), as well as biotic interactions and niche limitations (Bateman et al., 2012b; Gaston & Blackburn, 1996; White, 1978). Sympatric speciation is an alternative mode of speciation, where two populations become reproductively isolated and speciate without physical divergence. Allopatric speciation appears to be more common, but the existence of sympatric speciation has become increasingly accepted (Via, 2001). The most likely examples of species that have undergone sympatric speciation are cichlid fishes in crater lakes (Poelstra et al., 2018; Schiaffino et al., 2017) and herbivorous insects (Abrahamson & Weis, 1997; Filchak et al., 2000). Evidence for sympatric speciation in tetrapods is extremely rare (Rolshausen et al., 2010). The first compelling evidence has come from studies of storm petrels (Oceanodroma castro) on subtropical and tropical

7 islands, where individuals occupying the same islands breed in different seasons and have ceased to exchange genes (Friesen et al., 2007).

Extinction risk, life history, ecology and climate change

There have been recent advances in understanding how life history traits affect extinction risk (Öckinger et al., 2010), particularly with forecasted climate change (Angert et al., 2011; Pacifici et al., 2015). These studies found that species with low reproductive rates and long lifespans are most strongly affected by habitat loss and may be least able to shift their ranges to colonise new habitats. They also highlight the need for more studies identifying species that are likely to be most vulnerable to climate change.

It is important to understand species life histories from a conservation perspective, because life history dictates how quickly populations are able to recover, evolve and respond to threats including environmental changes. Understanding the evolution of life history and trends across landscapes can help us identify species with high extinction risk and factors influencing their persistence (Isaac, 2009; McKinney, 1997). For example, long-lived species with low reproductive rates are unable to recover rapidly from threats such as hunting, and short-lived species that rely on seasonal survival of young may be severely threatened by climate change (Fritz et al., 2009; Purvis et al., 2000). Most research on life history evolution has been conducted in the northern hemisphere. Life history of species in the southern hemisphere may show different patterns because the species, climate and biological systems are distinct (Fisher et al., 2001). For example, litter and clutch size evolution in mammals and birds is strongly influenced by seasonality in parts of the northern hemisphere where harsh cold winters are followed by periods of high food availability (Ashmole, 1963; Badyaev & Ghalambor, 2001; Bywater et al., 2010; Whorley & Kenagy, 2007). This pattern is unlikely to be replicated in regions such as the Australian desert.

In addition to particular life history characteristics, traits that are associated with extinction risk in mammals include: small geographic range and low population density, habitat specialisation and endemism, and lineage age. If a species has a small geographic range and low population density the likelihood of chance extinction is increased (Brown, 1995). Specialised or endemic species often have small ranges because of limited habitat and conservative niches. For example, species living in mountain-top refugia with a long history of evolution in isolated high elevation patches may be unable to disperse into adjacent habitats or persist with environmental change (Fisher & Owens, 2004; Wiens & 8

Donoghue, 2004). Species from ancient lineages have often become more specialised over time with decreasing range size and population density, and may be nearing the end of their evolutionary lives in terms of natural extinction trajectories (Johnson et al., 2002).

Climate change throughout the 21st century will differ between regions but predictions include increased temperatures and changes in rainfall, which may lead to droughts, intense wildfires and altered seasonality patterns in some areas (IPCC, 2014). These changes are predicted to influence animal distributions and densities, as available niches, habitat and community composition change (Isaac & Williams, 2007; Thomas et al., 2004; Walther et al., 2002). In temperate regions, there is already evidence that species have expanded their ranges northwards with increased temperatures (Hickling et al., 2006; Thomas & Lennon, 1999). Similarly, on mountains there have been documented range shifts to higher elevations, or retractions of lower elevation margins (Thomas et al., 2006; Wilson et al., 2005). In the arid zone, many species have boom-bust systems that rely on rainfall, and climate change may alter the amplitude of population cycles and increase risks associated with extreme population fluctuations (Pavey et al., 2017). For predators, climate change may lead to differences in the abundance and timing of prey availability. This can alter predator-prey interactions with biological consequences across ecosystems, and cause phenological mismatch and population declines (Visser & Both, 2005).

Dasyuridae and the genus Antechinus

Dasyuridae is a family of predominantly insectivorous marsupials that occur in Australia and Papua New Guinea / West Papua, in a wide variety of habitats including the arid zone and tropical rainforests. The Family Dasyuridae includes 17 genera and 75 species, with large variation in life history. Dasyurid species range in size from less than five grams (the long-tailed planigale, Planigale ingrami) to fourteen kilograms (the Tasmanian devil, Sarcophilus harrisii), and have a maximum lifespan of one to six years (Baker & Dickman, 2018). Litter sizes vary from two to 14 and some species produce supernumerary young, which die soon after birth (Ward, 1998). Dasyurids are unique for a mammal family as they include the entire spectrum from obligate semelparity to iteroparity (Fisher et al., 2001). Some species are monoestrous and only breed once a year, while others are polyoestrous and can produce multiple litters. For seasonal breeders, the reproductive season lasts from two weeks to six months, depending on the species (Van Dyck et al., 2013).

Antechinus is a genus within the family Dasyuridae found mainly on Australia’s east coast. The ranges of eastern Queensland are the centre of antechinus diversity. There are nine 9 species distributed from the New South Wales border to Cape York (Baker & Dickman, 2018) (Figure 1.1). Antechinus in Queensland have received less study than species in south-east Australia (e.g., Dickman et al., 1983; Kraaijeveld-Smit et al., 2002; Sale et al., 2008), particularly with the recent discovery of three new species in Queensland. Antechinus species in Queensland range in mass from an average of 15g to 75g (Baker et al., 2012). The antechinus diet is generalist and is predominantly composed of arthropods, although some species will supplement with small vertebrates (Fisher & Dickman, 1993a; Gray et al., 2017b; Mason et al., 2015). Some species are purely terrestrial and forage in the leaf litter, while others are semi-arboreal and also forage on trees (Lazenby-Cohen & Cockburn, 1988).

Antechinus have a short mating season (rut), which lasts for approximately one to three weeks during winter or early spring. The exact timing differs between species and sites (McAllan et al., 2006; Watt, 1997; Woolley, 1966). Evidence suggests that breeding timing is triggered by rate of change of photoperiod, and species in Queensland appear to have longer breeding seasons than species in southern Australia (McAllan et al., 2006). Male antechinus are considered to be semelparous, as they only reproduce once in their life time (Braithwaite & Lee, 1979). Before the breeding season males experience spermatogenic failure, and during the rut males use stored sperm to reproduce with as many females as possible. During this time males become active day and night, and use large amounts of energy travelling or searching for females and mating for long periods. High levels of testosterone caused by intense mating prevent the production of corticosteroid binding globulins, which means that circulating cortisol is unbound and biologically active. Antechinus target tissues are extremely sensitive to increases in circulating hormones, resulting in an immune system collapse which leads to male die-off soon after the end of the mating period (Bradley, 2003; Naylor et al., 2008).

Antechinus speciation may have been promoted by varied mountain landscapes and barriers preventing dispersal during the Pleistocene (Crowther et al., 2004). Competition between species also influences Antechinus distribution (Dickman, 1986). Multiple species occur across mountain ranges and threatened, small-range endemics are often restricted to mountain tops and face imminent threats from climate change (Van Dyck et al., 2013). Since 2012, three new species of antechinus have been discovered in Queensland (Baker, 2014). In 2018, two of these new species, the silver-headed antechinus (Antechinus argentus) and the black – tailed dusky antechinus (Antechinus arktos), were federally listed as endangered (EPBC, 1999). Both of these species occur on isolated mountain 10 tops and are among the most geographically limited mammals in Australia (Baker et al., 2014a; Baker et al., 2014b). Based on historical records from the 1970s and 80s and survey efforts in more recent times, A. arktos (a large, 40-120 g antechinus) may have retreated to high elevations on the Tweed Volcano caldera. A third new species, the buff- footed antechinus (Antechinus mysticus), appears to occur patchily between Brisbane and Mackay in eastern Queensland and may need consideration for threatened species listing. The poorly known Atherton antechinus (A. godmani) from Queensland’s wet tropics was listed by the IUCN as near-threatened ten years ago (IUCN, 2015). This species occurs in a 30 km–wide band of rainforest above 650m elevation in the Atherton uplands (Burnett, 2008). The distribution and habitat of A.godmani is highly fragmented, and it is expected to lose much of its current range to climate change over the next 30 years (IUCN, 2015).

Figure 1.1. Distribution of Queensland antechinus species included in this study. All Queensland species were included, except for the cinnamon antechinus (Antechinus leo) from the remote Cape York Peninsula.

Study scope

We do not currently have a thorough understanding of what influences variation in life history strategy, population density and distribution of dasyurid marsupials. This thesis investigates correlates of life history evolution and population density for dasyurids across Australia, to understand patterns of rarity and identify which species are most likely to be threatened by climate change. The thesis then focuses on antechinus distributed throughout mountains in the Queensland Great Dividing Range and associated uplands. Antechinus species have similar ecology and are likely to all be threatened by anthropogenic causes, yet some species are rare with high extinction risk and others are

12 common. This suggests that environmental requirements, biotic interactions or intrinsic factors are influencing antechinus distribution and abundance, leading to rarity in some species.

This thesis incorporates data on dasyurid life history traits, population densities, distributions and lineage ages taken from the literature. It also includes data collected on eight antechinus species and their arthropod prey, on four separate mountains at different latitudes in the ranges of eastern Queensland. At some locations, antechinus species are sympatric, and at other locations there is an elevation gradient of antechinus species replacement.

Study sites

Danbulla National Park is located in tropical north Queensland at approximately 17°S and 146°E. The main habitat types are vine forest, tall open forest and woodland. The elevation at our study location ranges from 600m to 1100m. There are three antechinus species found in this region: the rusty antechinus (A. adustus), the Atherton antechinus (A. godmani) and the yellow footed antechinus (A. flavipes). A. adustus and A.godmani are generally only found at high elevation and A. flavipes may occur across the entire elevation range (Watt, 1997).

Kroombit Tops National park is in central-east Queensland at approximately 24°S and 151°E. The maximum elevation at our study location is 900m and the predominant vegetation type is eucalyptus woodland. Two antechinus species occur at Kroombit Tops: the endangered A. argentus at high elevation and A. flavipes at lower elevation (Baker et al., 2014a).

Conondale National Park is located in south-east Queensland at approximately 27°S and 153°E. The main vegetation types are vine forest and Eucalyptus woodland. Three antechinus species are known to occur at Conondale National Park: A. flavipes, the buff- footed antechinus (A. mysticus) and the subtropical antechinus (A. subtropicus) (Baker et al., 2012).

Springbrook National Park is in far south-east Queensland at approximately 28°S and 153°E. Vegetation types at Springbrook include subtropical, warm temperate and cool temperate rainforests, and open eucalypt forest. Two antechinus species are found at Springbrook: the brown antechinus (A. stuartii) occurs at mid elevation and in sympatry

13 with the endangered black-tailed dusky antechinus (A. arktos) at high elevation (Baker et al., 2014b).

Thesis outline

Chapter 2. investigates the association between life history traits of Australian dasyurid species, prey productivity and seasonal predictability. My results suggest that there are two separate life history axes, rather than a single fast-slow continuum. I found that prey availability is associated with reproductive output, and prey predictability is correlated with position on a semelparity-iteroparity gradient. The results differ from studies in the northern hemisphere that have found a relationship between seasonality and reproductive output, most likely because Australia has different patterns of rainfall and food availability.

Chapter 3. investigates population density of dasyurid species across latitude, and population density of antechinus across elevation, in relation to species diversity and food availability. Appendix B. includes trapping effort to catch a rare subspecies of the white- footed dunnart (Sminthopsis leucopus) in north Queensland. Over latitudes, tropical systems are generally considered to be the most diverse and productive, with abundant food resources. Similarly, across mountain ranges lower elevations are often thought to be relatively benign habitats, with increasing harshness and seasonality towards mountain- tops. My results show that dasyurid and antechinus population density is lowest at tropical and low elevation sites, and this is related to low winter food availability. This goes against the premise that tropical, low elevation habitats have abundant food. My results suggest that winter food availability is limited in these locations because of highly seasonal yearly rainfall. I found that Australian mountain-tops receive orographic rainfall (where mountains cause moist air to rise) and maintain high prey availability throughout the year. This means that high elevation sites are suitable refuge locations for mountain dwelling dasyurids.

Chapter 4. examines the distribution of antechinus species and timing of breeding across latitude and elevation, in relation to evolutionary age and prey availability. It has been suggested that differences in timing of breeding may have lead to allopatric speciation in antechinus (Dickman, 1988). Photoperiod is thought to be the main environmental trigger that cues antechinus breeding (McAllan, 2006) and this implies that if timing of peak food availability changes antechinus will be unable to adapt, resulting in phenological mismatch. My results show that ancient antechinus occur at higher elevations than more recently evolved species on the same mountains, and suggest that habitat retractions with climate change may have caused antechinus speciation. Appendix C. includes data on potential 14 range contractions of the Atherton antechinus (A. godmani) and the rusty antechinus (A. adustus) in north Queensland. I found that antechinus are timing their breeding so that peak prey availability aligns with late stages of lactation. This varies between populations experiencing the same photoperiod and appears to depend partly on a local environmental cue, indicating that antechinus may have some ability to adapt to changes in timing of food availability.

CHAPTER 2: Prey productivity and predictability drive different axes of life history variation in carnivorous marsupials

This chapter has been accepted for publication in Proceedings of the Royal Society of London B: Biological Sciences

Image: A kultarr (Antechinomys laniger); B wongai ningaui (Ningaui ridei); C stripe-faced dunnart (Sminthopsis macroura); D Giles’ planigale (Planigale gilesi); E red-tailed phascogale (Phascogale calura); F northern quoll (Dasyurus hallucatus).

Abstract

Variation in life history strategies has usually been characterized as a single fast–slow continuum of life history variation, in which mean lifespan increases with age at maturity as reproductive output at each breeding event declines. Analyses of plants and animals suggest that strategies of reproductive timing can vary on an independent axis, with iteroparous species at one extreme, and semelparous species at the other. Insectivorous marsupials in the Family Dasyuridae have an unusually wide range of life history strategies on both purported axes. We test and confirm that reproductive output and degree of iteroparity are independent in females across species. Variation in reproductive output per episode is associated with mean annual rainfall, which predicts food availability. Position on the iteroparity-semelparity axis is not associated with annual rainfall, but species in regions of unpredictable rainfall have longer maximum lifespans, more potential reproductive events per year and longer breeding seasons. We suggest that these two axes of life history variation arise because reproductive output is limited by overall food availability, and selection for high offspring survival favours concentrated breeding in seasonal environments. Longer lifespans are favoured when reproductive opportunities are dispersed over longer periods in environments with less predictable food schedules.

Introduction

Variation between species in schedules of survival, growth and reproduction is usually considered on one axis of life history variation from fast to slow (Brown & Sibly, 2006; Gaillard et al., 2016; Harvey, 1989), assuming that trade-offs between age at maturity, fertility and lifespan constrain life history strategies, so that species invest most in either reproduction (faster species) or survival (slower species) (Bielby et al., 2007; Oli, 2004). However, several analyses have suggested that the degree of iteroparity (i.e., breeding repeatedly in a dispersed time period at one end of the spectrum and breeding once in a concentrated time period at the other) is independent of the fast-slow continuum. That is, the degree of iteroparity (number and spacing of reproductive events) is not necessarily traded off with life history speed (investment in reproduction versus longevity). Stearns (1983) found a secondary precociality–altriciality continuum in mammals after accounting for the slow–fast continuum, and Gaillard et al. (1989) identified this as part of a semelparity- iteroparity axis that accounts for up to 15% of variation in birds and mammals. In a more recent factor analysis of mammals, Bielby et al. (2007) identified a factor that explained up to half of the variance between species, and included maturity, weaning time and time between reproductive bouts. A second factor explained a further quarter of the variance and described output per reproductive episode. Species at one end produced large litters of small young, and species at the other end invested more in large but few young. Bielby et al. (2007) interpreted species position on this output axis in terms of the well-known offspring number versus quality trade-off, which is grounded in physiological constraints (Rollinson & Hutchings, 2013; Smith & Fretwell, 1974). Salguero-Gomez et al. (2016) have recently also demonstrated that the fast–slow continuum in plants includes traits of growth rate and lifespan on one axis and degree of iteroparity on another. Iteroparity is a risk-spreading reproductive tactic and is likely to be an advantage in variable environments. When conditions favouring offspring survival are unpredictable, bet-hedging by repeated breeding increases fitness, given a trade-off between reproduction and survival (Dewar & Richard, 2007; Stearns, 1992; Venable, 2007). Bielby et al. (2007) called for research to test how the iteroparity and reproductive output axes in mammal life history variation are associated with environmental variability.

Reproductive output, which includes number and size of offspring, is expected to be constrained by food availability and a female’s ability to use energy and nutrients for reproduction (Brown & Sibly, 2006; Król et al., 2003; Sibly & Brown, 2009). In marsupial taxa, adoption of higher energy diets has been associated with evolutionary switches to 18 higher reproductive rates. Corresponding trade-offs between reproductive output and other life history traits have led to the evolution of fast life history strategies in carnivorous species (Fisher et al., 2001). Rainfall and temperature seasonality might also influence age-specific survival (Ellis et al., 2009), which determines how species should trade off reproduction and survival (Ricklefs, 2010). We therefore predict that in carnivorous marsupials from the Family Dasyuridae, which are distributed widely across climate zones, features of climate that increase overall arthropod availability will be correlated with higher reproductive output in terms of litter size per reproductive bout and a faster life history.

Adaptive reproductive timing coincides with events that maximise offspring survival, such as seasonal rainfall and peaks in prey abundance (Dewar & Richard, 2007; Virgos et al., 2006; Whorley & Kenagy, 2007). For example, the desert chameleon (Furcifer labordi) from Madagascar has evolved semelparity and extended incubation time in an arid, seasonal environment (Karsten et al., 2008). Similarly, Australian dasyurids with late maturity, monoestry and semelparity occur where there are predictable annual peaks in arthropod abundance, because only one favourable time to wean young per year is possible, given that the marsupial trait of long lactation precludes breeding in the season of an individual’s birth (Fisher et al., 2013). We therefore predict that features of climate that increase food seasonality and the predictability of peaks in prey abundance will be correlated with semelparity in female dasyurids.

Using databases of life history traits and location records in the Australian marsupial Family Dasyuridae and long-term climate data, we test how female reproductive output, degree of iteroparity and lifespan co-vary with food abundance and seasonal predictability of food.

Specific predictions

We hypothesise that reproductive output and degree of iteroparity in females are independent: output will depend on food availability and not food predictability, whereas degree of iteroparity will depend on food predictability and not food availability. We therefore predict that litter size and the number of neonates at birth will co-vary with the amount of rainfall, and lifespan, length of the annual reproductive season, and the number of reproductive attempts will co-vary with rainfall predictability.

Methods

Study taxa

Dasyurids are predominantly insectivorous, range in size from < 5 g to 9 kg, and have a maximum lifespan of 1-6 years (Van Dyck et al., 2013). The maximum number of young that can be reared is determined by the number of teats, which vary from two to 14. Some groups such as antechinus produce supernumerary young: they give birth to more young than the number of teats, so some inevitably die at birth. Other species produce fewer young than the number of teats (Ward, 1998). In seasonal breeders, the reproductive season lasts for two weeks to six months, depending on the species. Uniquely in mammals, dasyurid males include the entire spectrum from obligate semelparity to iteroparity. Females can breed multiple times and vary from virtually semelparous to continuous breeding (Charnov & Schaffer, 1973; Fisher et al., 2001; Ricklefs, 2010). Complete male die off occurs in 20% of dasyurid species (Fisher et al. 2013), including: all in the genera Antechinus, Phascogale and Dasykaluta (Krajewski et al., 2000); Dasyurus and Parantechinus each contain a single species with facultatively semelparous males (Dickman & Braithwaite, 1992; Oakwood et al., 2001). Females from some species are monoestrous (i.e., breed once a year), while others are polyoestrous (i.e., can produce multiple litters per season) (Jones et al., 2003).

Data

We collated published female life history data on 34 Australian dasyurids taken from 82 studies (Appendix A). We only included species that are predominantly insectivorous (arthropods are >75% of their diet), because associations between rainfall and arthropod availability have been quantified (Fisher et al., 2013), allowing us to use rainfall as a proxy for food availability (Fisher & Blomberg, 2011). Traits analysed included: body mass at adulthood, maximum lifespan, polyestry vs monoestry, duration of reproductive season (indicating number of possible reproductive attempts), litter size and number of supernumerary young. Where possible, we used published field studies. Because potential within-breeding episode trade-offs with short-term food supply are likely to be important in dasyurids (Fisher & Blomberg, 2011), we used offspring number per reproductive bout rather than a ratio of long-term output over time such as reproductive rate. We used litter sizes recorded within a week of birth, because mothers may progressively lose pouch young during lactation. We calculated mean values for traits

20 when there were multiple studies of the same species. We defined the duration of the reproductive season as the number of weeks with births (Fisher et al., 2011).

We used rainfall as a proxy for arthropod availability (abundance and activity) (Collett & Fisher, 2017). For each species, we used mean annual rainfall at the centroid of geographic range based on all recorded locations (Fisher et al., 2013). We calculated seasonal predictability of rainfall by collating monthly rainfall from the Bureau of Meteorology (2016) at the study sites where life history information was collected. We gathered these data for the ten years preceding the end of the study, as Fisher et al. (2013) found that 3-8 years of insect and climate data gave repeatable results and clear outcomes in tests of hypotheses at these sites. For each site, we categorised monthly rainfall as ‘high’ if it was in the top 25% of abundances, or ‘low’ if it was in the lower 75% of abundances. We used these categorical data to calculate a Colwell index for rainfall at each site where marsupial life history data was collected (Fisher et al., 2013). Colwell’s index (P) uses categorical data to measure how tightly an event is linked to a season. P is composed of C (constancy) and M (contingency). Constancy describes how uniform the event is across seasons. Contingency measures the repeatability of seasonal patterns between years. P is maximized when the event occurs constantly throughout the year or if the pattern of occurrence is repeated across years (Colwell, 1974).

Statistical analyses

We log-transformed body mass, lifespan and length of the reproductive season and arcsin-transformed rainfall predictability (P) to normalise the distributions. We used phylogenetic generalised least squares (PGLS) models in R, using the packages ape (Paradis et al., 2004) and nlme (Pinheiro et al., 2018) to test the relationships between predictor variables: annual rainfall, rainfall predictability (P), lifespan, length of the reproductive season, polyestry and response variables: lifespan, length of the reproductive season, litter size and supernumerary young, incorporating phylogenetic information and body mass into models. We used a recent marsupial phylogeny (May-Collado et al., 2015) to account for interspecific autocorrelation due to phylogeny (Symonds & Blomberg, 2014). We used a multivariate normal prior for the phylogenetic random effects, with unit variances and correlation structure derived from the phylogenetic tree using Grafen’s branch lengths (Grafen, 1989). We calculated a pseudo r-squared for each PGLS model (Nagelkerke, 1991).

Results

Trade-offs and climate predictors of reproductive output

In agreement with our hypothesis that food availability limits reproductive output, species in more arid climates produced fewer young per reproductive bout (litter size versus mean annual rainfall: t = 2.72, p = 0.01, df = 34, slope = 0.001, se = 0.0005; Figure 2.1). Litter size was negatively associated with mass (t = -2.89, p = 0.007, df = 34, slope = -0.68, se = 0.24). Species with larger litters were more likely to have supernumerary young (t = 3.47, p = 0.002, df = 34, slope = 1.64, se = 0.47), and the number of supernumerary young was correlated with annual rainfall (t = 2.14, p = 0.04, df = 34, slope = 358, se = 167), further supporting our prediction that there would be a positive relationship between food availability and reproductive output. Species occurring in Australia’s arid and semi-arid zones (< 350mm annual rainfall) never had more than seven young, and only one desert species, the kowari (Dasyuroides byrnei), produced any supernumerary young. In agreement with our prediction that reproductive output would not vary with food predictability, litter size was not significantly related to P (rainfall predictability) (t = -0.4, p = 0.69, df = 34, slope = -0.79, se = 2) (pseudo r-squared for model one = 0.32). Litter size was also not associated with traits that indicate the degree of iteroparity in females (litter size versus length of reproductive season: t = -1.85, p = 0.07, df = 34, slope = -0.08, se = 0.04; litter size versus polyestry: t = 1.19, p = 0.24, df = 34, slope = 1.1, se = 0.92) and dasyurids do not trade off litter size against lifespan (litter size versus lifespan: t = -0.04, p = 0.97, df = 34, slope = -0.04, se = 1.03) (pseudo r-squared for model two = 0.25). Litter size of species in our study ranged from four to ten.

Trade-offs and climate predictors of the degree of iteroparity

Female maximum lifespan of species in our study ranged from one to six years and were positively associated with mass (t = 2.27, p = 0.03, slope = 0.11, se = 0.05). As predicted, lifespan was longer in areas with more unpredictable food supplies (lifespan versus rainfall predictability index P: t = -3.23, p = 0.003, d.f = 34, slope = 1.24, se = 0.38, Figure 2.2) (pseudo r-squared for model three=0.32). Species with long lifespans are more likely to have long reproductive seasons (lifespan versus reproductive season length: t = 4.29, p = 0.0002, df = 34, slope = 0.02, se = 0.005) (pseudo r-squared for model four = 0.38) and to have multiple litters per season (lifespan versus polyoestry: t = 2.51, p = 0.02, df = 34, slope = 0.25, se = 0.1) (pseudo r-squared for model five = 0.19). Reproductive season length alone was also strongly associated with rainfall predictability (reproductive season 22 length versus rainfall predictability index P: t = -4.73, p = 0.0001, df = 34, slope = -0.89, se = 0.26, Figure 2.3) (pseudo r-squared for model six = 0.14). This supports our hypothesis that adaptation to a seasonal climate, and therefore predictability of food schedules, favours a short reproductive period in seasonal environments, and a long lifespan with repeat breeding over a long period is more likely to evolve where there is less predictable rainfall. Annual rainfall did not significantly predict rainfall predictability (t = 1.14, p = 0.26, df = 32, slope = 731, se = 643.1), as some regions of arid Australia where dasyurids were sampled have highly predictable rainfall, and some more mesic areas have unpredictable rainfall (Figure 2.4). For example, Ningaui timealeyi (body weight 5.8g) has a maximum lifespan of one year, and although its Western Australia Pilbara location is a dry environment, summer cyclones are common and most annual rain falls predictably in February (Dunlop & Saule, 1982). Planigale gilesi (body weight 6.9g) in arid western New South Wales is similar in size and ecology but lives for a maximum of five years in a region where low, annual rainfall falls unpredictably across the year (Read, 1995).

Figures

Figure 2.1. The association between litter size and partial residuals of mean annual rainfall for Australian insectivorous dasyurid species. The line indicates the fitted regression from model one, including 95% confidence intervals. 23

Figure 2.2. The association between log female maximum lifespan and partial residuals of sin Colwell's predictability index of rainfall for Australian insectivorous dasyurid species. The line indicates the fitted regression from model three, including 95% confidence intervals.

Figure 2.3. The association between log10 length of the breeding season and partial residuals of sin Colwell's predictability index of rainfall for Australian insectivorous dasyurid species. The line indicates the fitted regression from model six, including 95% confidence intervals.

Figure 2.4. The centroid point of the geographic range of dasyurid species included in this study and mean annual rainfall throughout Australia. Species are marked with a ∆ if Colwell’s P is less than 0.7 (less seasonally predictable) and a ○ if Colwell’s P is equal to or more than 0.7 (more seasonally predictable). For full species names see Appendix A. Rainfall raster data was taken from Reside et al. (2012).

Discussion

Our results agree with several previous analyses, which concluded that aspects of the fast-slow continuum are independent of the semelparity-iteroparity axis in mammals. We focused on offspring number, because previous studies revealing multiple axes of life history variation in mammals identified reproductive output as a key variable (Bielby et al., 2007; Gaillard et al., 1989). The theory basis of within-bout trade-offs with litter size is well established (Król et al., 2003; Speakman & Król, 2010). Experiments and descriptive tests in small eutherian mammals have shown that the trade-off between the number and pre- natal growth rate of offspring in a litter is strongly affected by physiological constraints of energy, nutrients, temperature and tissue capacity. Total investment in reproduction is expected to reduce long-term survival under the disposable soma theory, which states that investment in reproduction reduces individual somatic maintenance (Kirkwood & Holliday, 1979; Selman et al., 2012). In an environment with high extrinsic mortality in adults, organisms should invest in early and high reproductive output rather than long-term maintenance and survival. Position of a species on the fast-slow continuum is therefore expected to depend on aspects of its ecology and environment that affect age-specific mortality risk (Healy et al., 2014). Litter size and growth is traded off within each reproductive episode based on maternal investment capacity at the time (Król et al., 2003; Rollinson & Hutchings, 2013). However, distributing this investment over a longer breeding period does not necessarily change the upper limit on the number of offspring per litter. For example, rate of milk transfer and heat production are mechanisms limiting investment within a reproductive bout (Król et al., 2003; Speakman & Król, 2010). Habitats and ecology that cause higher extrinsic mortality risk do not necessarily have higher or lower seasonal predictability of food. If they do, the direction of selection can be reversed. For example, Reznick et al. (2004) found that guppies in high predation sites evolved faster reproduction when high predation environments had scarcer food, perhaps because predators indirectly reduced net mortality by reducing density and thus competition for food. In variable environments, organisms that hedge their bets by dispersing reproductive effort over a longer breeding season and have a longer reproductive lifespan have a lower risk of failure (Dewar & Richard, 2007; Speakman & Król, 2010). Orzack and Tuljapurkar (2001) showed that unpredictable environments could favour either high or low reproductive output through their effect on reproductive costs.

In our study, rainfall seasonality was unrelated to annual rainfall. Therefore, aspects of the environment that affect whether iteroparity or semelparity is likely to lead to greater fitness 27 in females are at least partly disconnected from aspects of the environment that affect whether females can invest in large litters and whether mortality risk and reproductive costs are likely to lead to higher fitness in females that increase reproductive effort.

As predicted, a climate variable related to the predictability of peaks in prey abundance (rainfall predictability) was correlated with species position on the semelparity-iteroparity axis, and a variable that alters food availability and reflects energy limitation (annual rainfall) was associated with variation in reproductive output. These findings concord with some previous predictions in mammals and other vertebrates. For example, in the mammal family Leporidae (rabbits and hares) temperature seasonality predicted 71% of the global variation in litter size and body size, and the authors interpreted this in terms of food limitation caused by seasonality. Unpredictable timing of stressful environmental conditions was associated with increased iteroparity, whereas nest predation rate predicted 55% of variation in the timing trait of gestation duration (Virgos et al., 2006). In endemic mammal families in Madagascar, iteroparity involving short intervals between breeding episodes, a long breeding season and high adult survival is common, and this has been attributed to the particularly unpredictable timing of rainfall on this island (Dewar & Richard, 2007). Comparing desert populations of a ground squirrel on a gradient of increasing seasonal predictability, Whorley and Kenagy (2007) also found that more unpredictable rainfall was associated with longer breeding seasons, lower synchrony and smaller litter size. In Rose’s mountain toadlet (Capensibufo rosei), 94% of variation in toad lifespan between years is explained by variation in breeding season rainfall. In dry years, survival is increased and reproductive output is low, and in wet years, toads increase reproduction at the expense of survival (Becker et al., 2018).

In dasyurids, we found that species with large litters were more likely to occur in high rainfall habitats and to have supernumerary births. Arid zone species rarely had supernumerary young and often failed to have all teats occupied by neonates, suggesting they cannot reliably obtain enough food to produce excess young. We conclude that energy or nutrient availability constrains female reproductive output, consistent with many studies of limitations to reproductive output in small mammals (e.g., (Clutton-Brock, 1984; Clutton-Brock et al., 1982; Cody, 1966; Descamps et al., 2009; Fisher et al., 2001; Nilsen et al., 2009; Sibly & Brown, 2007; Williams, 1966). For example, Sibly and Brown (2007) found that mass of mammal neonate tissue was associated with reliable and abundant food. However, seasonality is often also associated with reproductive output, because seasonal environments have a reliable annual pulse of abundant food, especially at high 28 latitudes. For example, offspring number often increases with environmental seasonality in birds (Ashmole, 1963; Badyaev & Ghalambor, 2001) and mammals, including European lagomorphs (Virgos et al., 2006), boars (Sus scrofa) (Bywater et al., 2010) and ground squirrels (Ammospermophilus leucurus) (Whorley & Kenagy, 2007). Similar trends have not been obvious in carnivorous and southern hemisphere mammals at lower latitudes (Bunnell & Tait, 1981; Lord Jr, 1960), with the exception of Antechinus agilis in the relatively low latitude of southern Australia (Beckman et al., 2007). Unlike seasonal Australian environments, northern hemisphere habitats with severe winters have large seasonal peaks in food availability relative to the scarcest season (Ashmole, 1963).

We found that degree of iteroparity in female dasyurids across the continent was correlated with predictability of rainfall and thus schedules of reliable food availability. Species in environments with seasonally predictable rainfall were more likely to be monoestrous, have shorter lifespans and shorter reproductive seasons. These species time reproduction so that late lactation, which is energetically costly, coincides with the peak in arthropod availability (Fisher et al., 2013). Female dasyurids in regions of unpredictable rainfall live longer, are more likely to be polyestrous and have longer reproductive seasons. The opportunity for multiple breeding attempts over several years is likely to be adaptive if survival of young is highly variable (Congdon et al., 1982; Stearns, 1992), as a long reproductive period enables bet-hedging, which increases the likelihood of some births during times of high food availability (Jones, 2011). Bet-hedging strategies occur in plants (desert annuals) (Venable, 2007), bees (Perdita portalis) (Danforth, 1999), tortoises (Gopherus agassizii) (Lovich et al., 2015), primates (Jones, 2011) and many other taxa, which spread their reproductive effort over multiple episodes in unpredictable environments (Congdon et al., 1982; Stearns, 1976).

Patterns of rainfall explained significant variation in production of young, lifespan and length of the reproductive season. However, there was still a large proportion of variance unexplained by our models. These effects might be mediated by competition and population density (Gaillard et al., 1998), temperature (Speakman & Król, 2010), rates of age-specific predation (Ghalambor & Martin, 2001; Reznick et al., 1990; Reznick et al., 2004; Wilkinson & South, 2002), and torpor (Turbill et al., 2011), which would be promising future avenues for further understanding of the mechanisms.

CHAPTER 3: Winter food availability explains rarity of tropical and lowland species

This chapter has been submitted for publication in Ecography

Image: Kroombit tops National Park and the Endangered Antechinus argentus (Gary Cranitch).

Abstract

Species in the tropics often have lower population densities than temperate species, putting them at greater risk of extinction. Possible explanations for rarity in the tropics include low food availability, increased biodiversity and reduced niche breadth, or greater lineage age of tropical species. Mountains often replicate patterns seen across latitudes, which may help us to understand large scale macro-ecological patterns. We use Australian insectivorous marsupials (Family Dasyuridae) to investigate how population density is related to latitudinal and elevational gradients, and to test how this is associated with food availability, species diversity and evolutionary age. We particularly focus on the genus Antechinus and their arthropod prey in four mountain regions along a latitudinal gradient from the subtropics to the tropics in Queensland. Our results show that dasyurid population densities increase from low to high latitude, and antechinus species have the lowest population densities in the tropics and at low elevations. This is associated with rainfall and arthropod availability, which are low throughout winter at tropical and low elevation sites. Population density of antechinus is limited by winter food availability, which is tightly linked to rainfall. This suggests that climatic change leading to reduced food availability may threaten insectivorous species.

Introduction

Tropical systems tend to be the most biodiverse, but tropical species often rare and have low population densities, and therefore an increased risk of extinction (Johnson, 1998a; Symonds et al., 2006). This macroecological pattern has been documented for groups of animals around the world including birds (Blackburn et al., 1996; Currie & Kerr, 2008; Jenkins & Hockey, 2001), mammals (Johnson, 1998a) and invertebrates (Currie & Fritz, 1993), but it is unclear what causes the latitudinal trend in population density.

One theory proposed to explain the low population densities of Australian marsupials closer to the equator is that food is scarce in the tropics (Johnson, 1998a). Huston and Wolverton (2009) studied net primary productivity across latitudes and found that terrestrial productivity peaks between 30° and 50°, in contrast to some previous assumptions that tropical habitats are the most productive. A species’ trophic level constrains population density, because energy is lost as it transfers between trophic groups (Huston & Wolverton, 2011). Therefore, primary producers are more abundant than herbivores, and herbivores are generally more abundant than carnivores (Barneche et al., 2016; Trebilco et al., 2013). While there have been many recent studies on primary productivity gradients, we do not know whether these gradients also occur in taxa that occupy higher trophic levels, such as the prey base for insectivorous vertebrates (Huston, 1994; Huston & Wolverton, 2009; Wolverton et al., 2009). Across latitudes, the highest population densities should occur where food availability is highest (McNab, 2010). To date, food availability for species other than those that eat vegetation, fruit and nectar has not been empirically measured across latitudinal gradients and related to population density.

A second theory that has been used to explain tropical rarity in Australia is that species found closer to the equator may be from ancient lineages and nearing the end of their evolutionary lives. Ancient species may have become more specialised over time resulting in decreased range size and low population densities (Johnson et al., 2002). Species around the world show different patterns of evolutionary age depending on past climate change and diversification (Hewitt, 2004). For example, frogs in the southern hemisphere are older than frogs in the northern hemisphere (Dubey & Shine, 2011) and climate refuges such as tropical mountains support particularly ancient species (Hewitt, 2004). The current climate of the Australian wet tropics is similar to the Cretaceous and early Tertiary periods (White 1994) and species in drier areas are more likely to be recently evolved (Hawkins et al. 2005). Symonds et al. (2006) studied 54 species of honeyeater

(Meliphagidae) that feed on insects and nectar in Australian woodlands and found that mean abundance was positively correlated with latitude. While this pattern was clear between species, intraspecific population density was unaffected by latitude. This suggests that rarity is not related to an environmental variable or biological interaction that changes across latitude, but may instead be correlated with evolutionary age (Johnson, 1998b).

One of the most prevalent global biogeographical patterns is increasing biodiversity from the poles to the equator (Brown, 2014). There are two main categories of explanation for this latitudinal biodiversity gradient. The first is that most lineages originated in the tropics (Bowen et al., 2013; Cavender-Bares et al., 2011; Jablonski et al., 2006), and many of these species remain confined to low latitudes because they have become adapted to relatively benign conditions and are unable to colonise harsher abiotic environments (Roy et al., 2009). The second is that high temperatures increase rates of evolution (Machac et al., 2012; Wright et al., 2011) and high productivity means a larger number of species can be supported in the tropics (Kilpatrick et al., 2006; O' Brien et al., 1998). Species diversity is generally negatively associated with population density, which may result in rarity in the tropics (Hubbell, 2001). Barnache et al.’s (2016) global study on reef-fish communities found that population density declines as species community richness increases, potentially because competition creates smaller niche breadths (MacArthur, 1984; Symonds & Johnson, 2006; Vázquez & Stevens, 2004). A species’ niche breadth (i.e., the multi-dimensional space of resources that species need to survive and reproduce) determines geographical range size (Slatyer et al., 2013) and therefore population density (Rapoport, 2013). This is positively associated with latitude because it is assumed that tropical environments are productive and predictable, which should favour greater specialisation (Slatyer et al., 2013; Vázquez & Stevens, 2004). However, Symonds and Johnson (2006) and found no relationship between niche breadth and abundance in Australian passerines (Meliphagoidea). Latitudinal patterns are currently not well studied in mammals and warrant further investigation.

Many of the biological patterns found across latitudes also exist over elevational gradients. For example, animal niche breadth is greatest towards the poles (MacArthur, 1984), and animals have broader niches at high elevation (Rasmann et al., 2014). However, there is still conjecture over whether latitudinal patterns related to biodiversity and population density are replicated over elevation. For example, mammal species richness and abundance show many different patterns on mountain ranges (Brown, 1995; Brown et al., 33

1996; McCain, 2004). Bateman et al. (2010) and Heaney (2001) found a positive relationship between elevation and small mammal species richness and abundance in the Australian tropics and the Phillipines in relation to productivity and vegetation complexity. However, other studies have detected a mid-domain effect, where small mammal species diversity peaks at mid-elevation (McCain, 2005; Nor, 2001) and reasons for patterns over mountain ranges remain unclear.

Determining patterns and causes of rarity is important for species conservation and management, because if a species has a small geographic range and low population density, the likelihood of extinction is increased (Brown, 1995). We currently know relatively little about what causes low abundance of tropical species, or how patterns of rarity are related to elevation, especially in insectivorous vertebrates. This is particularly important for conservation under climate change, as more species begin to experience latitudinal and elevational range shifts (Parmesan & Yohe, 2003; Reside et al., 2013). Understanding the drivers of macroecological patterns might help us to predict where species will be most affected by climate change, and so discern mechanisms of range shifts. Many studies have been conducted on temperate zone species responding to increased temperatures by shifting their ranges, and recent studies of the effects of climate change on tropical and sub-tropical species predict they will respond particularly strongly (Chen et al., 2009; Feeley et al., 2011; Forero-Medina et al., 2011; Freeman & Freeman, 2014; Jump et al., 2012). Tropical high elevation species with small ranges are expected to suffer widespread extinction (Freeman & Freeman, 2014).

In Australia, rarity in the tropics has been documented for mammals by Johnson (1998a), who hypothesised that low abundance of tropical mammals may be related to food availability. To test this relationship it is necessary to measure population density in conjunction with food availability across multiple locations. Marsupials from the Family Dasyuridae are widely distributed in Australian forests, occur across a range of elevations and are primarily insectivorous. Long-term standardised arthropod monitoring has recently become feasible (Collett & Fisher, 2017), and there have been no previous latitudinal gradient studies on insect availability, although arthropods provide food for a high proportion of species.

Here we test associations between population density, latitude, elevation and food availability in Australia, in order to empirically test Johnson’s (1998a) hypothesis that the cause of low population density of marsupials at low latitudes is reduced food availability.

We examine the relationship between population density and arthropod availability for the Australian insectivorous dasyurids across latitudes. We then focus on the genus Antechinus at locations on an elevation gradient, and determine whether evolutionary age and species diversity are related to antechinus population density. Our first prediction is that dasyurid and antechinus populations at low latitude (closer to the equator) and at high elevations will have low population densities, and our second prediction is that food availability will be lowest at low latitude and high elevation, and vary in accordance with rainfall patterns.

Methods

Study taxa

Dasyuridae is a predominantly insectivorous family of marsupials that occur in Australia and Papua New Guinea, with high diversity in the forests on Australia’s east coast (Baker & Dickman, 2018). Ranges in eastern Queensland, Australia, form the centre of diversity in the dasyurid genus Antechinus. Nine species occur in this area and species are sometimes separated by elevation zones on the same mountain (Baker & Van Dyck, 2013). The antechinus diet is generalist and predominantly composed of arthropods, with some vertebrates and fruit (Gray et al., 2017b; Mason et al., 2015; Pearce et al., 2017). Antechinus species in our study weigh 15g to 170g (Baker et al., 2012). Two of the mountain-top species, Antechinus arktos and Antechinus argentus, have very restricted ranges and are listed federally as endangered (EPBC, 1999) and a third, Antechinus godmani was listed as near-threatened in 2008 and has not been assessed since (EPBC, 1999).

Sampling design

To determine whether insectivorous dasyurids show a latitudinal trend in population density, we compiled local population density (Nha) for 17 species of Dasyuridae from published and unpublished studies, excluding antechinus species included in our study. Antechinus data collected during this study was not included, because population density was calculated during the breeding season. During the breeding season Antechinus activity levels increase, leading to very high estimates compared to other published dasyurid studies, where densities were calculated prior to the breeding season. We only included species found in wooded habitats east of 140°E to minimise longitudinal variation

35 in habitat. This comprises a continuous area of wooded habitat and species range from 39°S to 12°S (Johnson, 1998a).

We conducted aluminium box trapping (WA poultry equipment) of eight antechinus species at four mountains in Queensland, Australia: Springbrook National Park (28°, elevation 1050m), Conondale National Park (26°, elevation 800m), Kroombit Tops National Park (24°, elevation 950m) and Danbulla National Park (17°, elevation 1100m) (Figure 1). These locations included all of the antechinus species within the centre of diversity in Queensland. We set up three trapping grids on either side (east / west) of each range (6 per location and 24 in total), spread evenly from the base to the top of the mountain.

We set out 50 traps, 10m apart, in two rows of 25 at each site (Fisher, 2005; Mowat et al., 2015) and trapped each site for two consecutive nights per trip. 400 trap nights were conducted at Springbrook National Park, 2000 at Conondale National Park, 12600 at Kroombit Tops National Park and 1100 at Danbulla National Park, to trap enough antechinus to accurately calculate population density (Schwarz, 2001). We identified captured antechinus species using coat colour and mass (Van Dyck et al., 2013) and clipped their rump fur (for mark-recapture identification).

We used the trapping data to estimate local population size per hectare using the Lincoln- Petersen estimator for small sample sizes (Williams et al., 2002a). The Lincoln-Petersen estimator is suitable for calculating population size from two consecutive sampling events and shows comparable results to models used in the program MARK (Grimm et al. 2014; Williams et al., 2002a). In our study, capture rate was high on both the first and second night.

We used white-flash camera traps (Reconyx HyperFire Professional Series - PC850) with a modified focal length (250mm) to conduct long-term sampling of ground-dwelling arthropods (Collett & Fisher, 2017) at the same sites we trapped antechinus, to assess food availability. We placed a camera trap at each site on the elevational gradients = 6 cameras per location (mountain range), tied to trees and facing downwards 250mm above the ground. We set the time lapse function to take a photograph once every 15 minutes between 4pm and 6am (Collett & Fisher, 2017). We left the cameras at each location for two years to correspond with timing of live-trapping between 2015 and 2018, and changed the memory cards and lithium batteries every two to four months. We identified photographed arthropods to the taxonomic level of Order and recorded the date.

We used pitfall traps to collect a reference sample of arthropods to aid photo identification, and to ground-truth camera trap data (Fisher & Dickman, 1993b). We placed ten plastic cup pitfall traps, flush with the ground and half filled them with 70% ethanol, at each antechinus trapping site at 10m intervals over 100m. We also sampled arboreal arthropods using two Buzz brand 16cm long sticky-traps attached to trees, 2m above the ground at each site. We left both the pitfalls and the sticky traps for two days at each site per trip. The total number of traps nights was 140 for pitfalls and 28 for sticky traps at each location (mountain range) (Dickman, 1991; Fisher & Dickman, 1993b; Green, 1989). We identified pitfall and sticky-trap arthropods to Order and recorded the date (Fisher & Dickman, 1993b).

We recorded annual rainfall and total winter rainfall for the years we collected arthropod availability at each location using data collected by the Bureau of Meteorology (Meteorology, 2016).

We took the dates of divergence for each antechinus species from Bayesian evolutionary analysis sampling trees (BEAST) created by Mutton (2018). The number of antechinus and other Dasyuridae species living at each location was collated using species lists for each location (Queensland Government, 2018), combined with personal trapping records.

Data analyses

To test our first prediction that dasyurid population density will increase with latitude, we analysed the association between population density of 13 insectivorous Dasyuridae species (data taken from the literature) and latitude using phylogenetic generalised least squares (PGLS) models, with mass incorporated as a predictor. We ran the analyses using the packages ape (Paradis et al., 2004) and nlme (Pinheiro et al., 2018). Interspecific autocorrelation due to phylogenywas accounted for by using a recent marsupial phylogeny (May-Collado et al., 2015; Symonds & Blomberg, 2014).

We tested whether antechinus populations at high elevation and low latitude (closer to the equator) have low population densities and determined whether population density is related to evolutionary age by analysing the associations between the response variable: population density, and predictor variables: latitude, elevation, diversity and BEAST date, using linear mixed models with location included as a random effect (McAllan et al., 2006; McKinnon et al., 2010; Wilson et al., 2007). We log-transformed population size, latitude,

37 elevation, arthropod availability and rainfall to normalise the distributions (Johnson, 1998a).

To test prediction two that food availability for insectivorous dasyurids is lowest at low latitude and high elevation, and varies with rainfall, we tested associations between the response variables: arthropod availability (overall and in the winter month with the lowest availability) and predictor variables: rainfall, winter rainfall and latitude, using linear mixed models with location included as a random effect. The same tests were then carried out after replacing latitude with elevation (McAllan et al., 2006; McKinnon et al., 2010; Wilson et al., 2007).

We then tested whether winter food availability is associated with antechinus population density by analysing the relationship between the response variable: population density and predictor variable: winter arthropod availability, using linear mixed models with location included as a random effect. We log transferred population density to normalise the distribution. Analyses were run in R 3.0.0 (R Development Core Team, 2013).

Results

Population densities

We found a latitudinal trend in population density for species of insectivorous dasyurid marsupials (excluding antechinus included in this study) living in forests on Australia’s east coast. Population density in 13 dasyurid species increased with latitude (Figure 3.2) (t = 2.53, p = 0.028, df = 14, slope = 0.09, se = 0.04).

Our analyses show that population densities of antechinus species are lowest at low latitude (tropical) (t = 3.09, p = 0.03, df = 5.35) and low elevation (t = 3.19, p = 0.02, df = 5.35) sites supporting our prediction that dasyurid populations at low latitudes will have low population densities, but disagreeing with the second part of our prediction that populations at higher elevations will have lower population densities. For each location, this was true both within and between species. For example, populations of Antechinus subtropicus at lower elevation had lower population densities than populations of A. subtropicus at higher elevation on the same mountain (Figure 3.3). There was a negative interaction between population density, latitude and elevation (t = -4.87, p = 0.004, df = 6), such that as latitude increases the effect of elevation on population density is reduced.

Populations at low latitude were only found at relatively high elevation sites, although suitable habitat occurred at lower elevations (Table 3.1). Antechinus population densities were highest at high latitude, high elevation sites and lowest at tropical, low elevation sites (Figure 3.3). Evolutionary age (BEAST date) (t = 1.25, p = 0.26, df = 5.36) and species diversity (t = 1.43, p = 0.69, df = 2) were not associated with antechinus population density. Each mountain had two to three species of antechinus and three or four species of other insectivorous dasyurid.

Arthropod availability

Johnson (1998a) hypothesised that the cause of low population density at low latitude is reduced food availability. Overall, arthropod availability was not lowest at low latitude (t=- 1.8, p=0.19, df=2.34) and high elevation (t = -0.5, p = 0.62, df = 9.29), in disagreement with our second prediction that food availability for dasyurids will be lowest in the tropics and at high elevation. However, we found that winter arthropod availability was related to amount of winter rain (t = 3.01, p = 0.01, df = 9) (Figure 3.4), supporting our second prediction that food availability for dasyurids varies with rainfall, and winter arthropod availability was lowest at tropical (t = 3, p = 0.02, df = 9) and low elevation sites (t = 2.81, p = 0.02, df = 7.57). There was a negative interaction between winter monthly arthropod availability, amount of winter rainfall and latitude (t = -2.99, p = 0.015, df = 9), so that winter rainfall has the greatest effect on winter arthropod availability at low latitude (Figure 3.4). Similarly, there was a negative interaction between winter monthly arthropod availability, amount of winter rainfall and elevation (t = -2.94, p = 0.02, df = 7.43). Elevation has a modest effect on food abundance where winter rainfall is high, and a large effect where winter rainfall is low (Figures 3.3 and 3.4).

For sites falling within the tropics, yearly rainfall patterns are similar and winter arthropod availability seems to be related to rainfall characteristics of the site, rather than varying strictly with latitude. For example, Kroombit Tops National Park (24°S) had lower winter rainfall, arthropod availability and antechinus population densities than Danbulla National Park (17°S), probably because while Kroombit Tops exhibits the same seasonal patterns, it has lower overall and winter rainfall possibly because it is further inland and a lower mountain.

Antechinus population density and winter arthropod availability

Antechinus population size was positively associated with arthropod availability during the winter month with the lowest arthropod availability (t = 3.53, p = 0.04, df = 2.87, slope = 0.07, se = 0.02). Antechinus populations that experienced relatively high winter arthropod availability maintained higher population size than populations that experienced low winter arthropod availability.

Figures

Table 3.1. Lowest elevation detected (m) and elevations sampled for antechinus species at four locations.

Site Species Lowest elevation Elevations detected (m) sampled (m) Atherton (17°S) Antechinus 900 600 – 1100 godmani Atherton (17°S) Antechinus 900 600 – 1100 adustus Atherton (17°S) Antechinus flavipes 755 600 – 1100 rubeculus Kroombit (24°S) Antechinus 894 450 - 903 argentus Conondales (26°S) Antechinus 180 180 - 784 mysticus Conondales (26°S) Antechinus 657 180 - 784 subtropicus Springbrook (28°S) Antechinus arktos 1023 331 - 1023

Springbrook (28°S) Antechinus stuartii 331 331 - 1023

Figure 3.1. Antechinus trapping and arthropod monitoring locations in Queensland.

Figure 3.2. Popuation density of insectivorous dasyurids in forests on Australia's east coast.

Figure 3.3. Population density of antechinus including 95% confidence intervals at low, medium and high elevations at four locations from 17°S to 28°S. Refer to Table 3.1. for species found at each location.

Figure 3.4. Total winter rainfall (mm) and winter arthropod availability (total counted on cameras) in the lowest month including standard errors at four locations from 17°S to 28°S.

Discussion

Globally, animal population density is typically low in the tropics (Stevens, 1989). Our result that in insectivorous dasyurids, population density is lowest at low latitude supports Johnson’s (1998a) finding that Australian forest mammals are rarest in the tropics. It also corroborates Watt’s (1997) discovery that population densities of antechinus in the wet tropics are some of the lowest anywhere in their distribution. Our study suggests that antechinus populations, and likely other insectivorous dasyurids in forest habitats, are regulated by winter arthropod availability, which is driven by amount of winter rainfall (Figures 3.2, 3.3 and 3.4). The density-dependent effect of food shortage is a well- supported mechanism to explain population density of seasonally-breeding predators (e.g., Ashmole, 1963; Bartoń & Zalewski, 2007; Goldberg et al., 2012; Lewis et al., 2001; 44

Prevedello et al., 2013). Ashmole et al. (1963) showed that oceanic birds, especially in the tropics, have limited prey availability during the breeding season, and this affects population density by reducing reproductive output and the number of birds that are able to breed. Dickman (1989) showed experimentally that population density of the agile antechinus, Antechinus agilis, could be limited by food supply, as supplementary food increased density and survival, especially in winter when insects were scarce.

Our result that antechinus population density is limited by energy availability during the winter (Figures 3.1 and 3.2) is supported by seasonal changes in antechinus behaviour. Some tree-cavity nesting antechinus are known to nest communally during the winter before their young are born and then alone in the spring and summer (Fisher et al., 2011), once arthropod availability and temperatures begin to rise. Fisher et al. (2011) explained communal nesting in antechinus species as a need for increased thermoregulation efficiency during the colder months since group size was negatively correlated with daily minimum temperature. Similarly to other small mammals, antechinus have high energy needs for their body size and use mechanisms to conserve energy such as torpor and huddling (Geiser, 1988). High energy needs and difficulty maintaining body temperature would make winter survival difficult in times of food shortage. Further, we found in this study that where antechinus species are sympatric in subtropical and tropical Queensland, the species with the larger body mass always had a lower population density. Larger species have higher energy requirements, and our finding that they always have lower population densities than smaller congeners suggests that there is restricted food availability in the environment (Currie & Fritz, 1993).

At our lowest latitude site, Danbulla National Park, Antechinus adustus and A. godmani are sympatric, and we found that during winter the smaller species (A. adustus) exhibits diurnal foraging behaviour, but this is not apparent in spring and summer. In the subtropics where Antechinus arktos and Antechinus subtropicus co-occur, both species were nocturnal. Diurnal foraging behaviour may be related to competition associated with winter food shortage. Dickman (1988) showed experimentally that removing the larger competitor of a pair of antechinus species freed the smaller species to use more productive microhabitats and safer foraging times. Studies of other predators, for example sea otters (Enhydra lutris) (Estes et al., 2003) and sea lions (Zalophus californianus and Zalophus wollebaeki) (Villegas-Amtmann et al., 2011) in California and the Galapagos have also suggested that competition for limited resources increased foraging specialisation. The seasonal switch from diurnal to nocturnal foraging behaviour in tropical A. adustus thus 45 further supports our conclusion that winter food abundance can limit dasyurid populations, and highlights the difference in food availability between the subtropics and tropics.

We did not detect an association between lineage age or dasyurid species diversity and antechinus population density. The lack of association between density and lineage age may be related to our small sample size, and the pervasive effect of arthropod availability. Although the two most ancient species in our study A. godmani and A. adustus occurred at our lowest latitude site and had low population densities, the effect of winter food availability was stronger than lineage age. A. argentus is relatively recently evolved within the genus (Mutton et al., 2018) and had the lowest population density in our study. In terms of the association between antechinus population density and species diversity, our results indicate that dasyurid diversity was not significantly different between sites. Competition between insectivorous dasyurids is therefore unrelated to rarity at low latitudes. However, high diversity of other taxa at low latitudes may cause increased competition for resources such as food and nesting space. Globally, there is strong evidence of a latitudinal gradient in mammal diversity (Badgley & Fox, 2000; Lyons & Willig, 2002; Stevens & Willig, 2002; Willig et al., 2003), but Kaufman (1995) and Ruggiero (1994) found that diversity patterns differ among mammalian orders. Peaks in species diversity occurred within 30 degrees of the equator for most orders. However, Insectivora attained maximum richness in the temperate zone. Additionally, Kaufman (1998) detected a plateau where there was no difference in diversity between latitudes in tropical areas. All of our sites are within 30 degrees of the equator in subtropical and tropical Queensland, so it is possible that mammal biodiversity does not increase with decreasing latitude in our study region.

We found that winter rainfall was related to winter arthropod availability, and therefore plays a large role in maintaining insectivorous marsupial populations. This may mean that dasyurids are particularly susceptible to the predicted changes in rainfall patterns and productivity under climate warming (Isaac, 2009; Song et al., 2006) and higher variability between wet and dry years (Boer et al., 2000; Giorgi et al., 2004; Räisänen, 2002; Rowell, 2005; Watterson, 2005). Populations of the endangered northern bettong (Bettongia tropica) in tropical Queensland are also regulated by food availability and have experienced declines associated with climatic variation and droughts which are predicted to increase with climate change (Bateman et al., 2012a). Inter-annual climate variability is likely to lead to strongly fluctuating population densities (Morris et al., 2008), which disadvantages short-lived species such as small insectivorous birds, as they are cannot 46 ride out a year of failed reproduction (Jiguet et al., 2007). This is particularly important for antechinus, because most individuals breed only once.

Our results show that antechinus population density increases with elevation, is correlated with winter arthropod availability that changes with elevation and is lowest in winter at low elevation. This study took place in subtropical and tropical latitudes, and our highest elevation site was 1100m (Table 1). Elevation here is low in the global context, and climate does not become extreme at the tops of these mountains (there is no alpine grassland or tree-line, unlike some parts of the tropics). In the range of elevations at our sites, precipitation and primary productivity increase with elevation (Rowe, 2009; Williams et al., 2002b; Williams & Middleton, 2008; Woinarski et al., 2005). This means that high elevation sites will experience more rainfall (even in seasons of low rainfall) than low elevations, leading to higher winter arthropod abundances and therefore antechinus population densities. In our study this was true both within and between species. For example, A. stuartii was distributed over the entire elevational range at Springbrook National Park and population density increased with elevation. A similar effect of rainfall has been documented in Costa Rican premontane birds that experienced an upward shift in their range because of decreasing dry-season mist frequency (Pounds et al., 1999).

We found that antechinus population densities were highest at high elevation. Similarly, Rickart et al. (1991) showed that the distribution of insectivores depends on prey availability, as high elevation, detritus-rich forests were favoured by insectivorous mammal species in the Phillipines because they supported a large number of earth worms. The importance of high elevation sites is also evident from Bateman et al.’s (2010) study of small mammal species richness and abundance along an elevational gradient in the Australian tropics. Bateman et al. (2010) found that small mammal richness peaked where the climate is most favourable, in high precipitation, humid environments at high elevation (Currie, 2003; Nor, 2001).

Although our study focused on the effect of rainfall patterns and prey availability on population densities, antechinus may also be affected by habitat quality, including direct effects of temperature. Reside et al.’s (2013) analysis of ecological refugia under climate change showed that habitat for species which are endemic to upland areas will disappear by 2085. The endangered Antechinus arktos only occurs in high rainfall, fog-drip areas above 900m, and already appears to have experienced upward range shifts (Baker et al., 2014b). As reported by Gray et al. (2017a), we found that A. arktos (mean 80g) is much

47 rarer than its congener A. stuartii (mean 30g), possibly because of increased energetic requirements imposed by larger size and the potential that it now only occurs at the very edge of its climatic range (Channell & Lomolino, 2000; Gaston et al., 2000). Likewise, the endangered silver-headed antechinus, A. argentus, is only found in forests with frequent mists above 850m, and may have recently shifted to higher elevation (Baker et al., 2014a; Mason et al., 2017). We found that although A. argentus occurs at the highest elevation on Kroombit Tops mountain range, it is subject to extremely harsh winter conditions of low rainfall and food availability, which may in part explain its very low abundance.

Conclusions

Antechinus and insectivorous dasyurids from Australian subtropical and tropical forests follow latitudinal and elevational trends in population density, so that low latitude and low elevation species are sparse. This pattern is correlated with winter rainfall and associated patterns of arthropod availability. As winter food resources appear to limit population densities, modest changes in rainfall may have severe consequences for persistence. It is likely that this is also applicable to other insectivores globally, although associations between latitude, elevation and population density will depend on local rainfall patterns, and a more complex pattern may occur on very high elevation mountain ranges. The highest elevation sites are crucial for maintaining year-round food to conserve threatened Australian montane dasyurid species.

CHAPTER 4: Do resource pulses drive latitudinal and elevational timing of breeding in the insectivorous marsupial genus Antechinus?

This chapter has been prepared for publication in Journal of Biogeography

Image: A black-tailed antechinus (Antechinus arktos) (Emma Gray); B subtropical antechinus (Antechinus subtropicus); C silver-headed antechinus (Antechinus argentus) (Eugene Mason); D rusty antechinus (Antechinus adustus); E Atherton antechinus (Antechinus godmani); F yellow-footed antechinus (Antechinus flavipes). 49

Abstract

Seasonally breeding vertebrate species time reproduction so that young are born when food availability is highest. Rate of change of photoperiod is the predominant cue that triggers breeding, but there is some evidence that breeding can also be triggered by local environmental stimuli such as temperate and rainfall. If species are relying on photoperiodic cues to trigger breeding and timing of peak food availability changes with global warming, phenological mismatch may result in population declines. We collected data on breeding timing, arthropod availability and lineage age for populations of the insectivorous marsupial genus Antechinus in Queensland, Australia. We test whether antechinus species across elevations and latitudes have breeding season separation consistent with adaptation to timing of peak food availability and whether the oldest antechinus species are restricted to mountain-tops and have less flexibility in their breeding timing. We found that across mountains, antechinus populations have breeding season separation where higher elevation populations breed progressively later, but we found no association between breeding season and latitude. Breeding timing was related to the peak in arthropod availability, as populations had young in the nest when arthropod abundance was highest, and across mountains, flushes in arthropod availability occurred later as elevation increased. Phylogenetically older antechinus species occurred in high elevation sites and bred later than younger species, which had larger distributions. Previous studies have shown that antechinus breeding is strongly associated with rate of change of photoperiod, but our results suggest that breeding may also be triggered by specific environmental conditions experienced at each site. This allows antechinus to increase their chances of successfully weaning young depending on patterns of climate and resource availability experienced at different elevations and latitudes. As antechinus appear to be able to react to local environmental conditions, they may be able to adapt to small changes in patterns of arthropod availability with global warming. However, their facultative, semelparous life history means that periodic climatic changes such as failure of seasonal rains may result in loss of young and lead to large species declines.

Introduction

In seasonally breeding vertebrates, reproductive events are timed so that food availability is highest when nutritional demands of breeding are highest (Hau, 2001; Hinsley et al., 2016; Nager & van Noordwijk, 1995; Van Noordwijk et al., 1995). Increasing food availability directly triggers breeding in some species (Hau, 2001) but many use indirect cues. Known environmental stimuli that trigger seasonal breeding include rate of change of photoperiod (McAllan et al., 2006), temperature (Hinsley et al., 2016; Nager & van Noordwijk, 1995; Reading, 1998; Van Noordwijk et al., 1995) and rainfall (Hau, 2001). The type and complexity of triggers may vary with climate and latitude. For example, in temperate environments photoperiod is often the most important cue (Cresswell & Mccleery, 2003; Williams et al., 2015), and local environmental conditions contribute more to reproductive timing at lower latitudes and in variable environments (Hau, 2001; Svensson, 1995). In environmentally variable areas, relying solely on photoperiod may result in failure to synchronise breeding with food availability, and in some species timing can change between years and locations if environmental triggers are variable across time and space (Hinsley et al., 2016). Historically, ecologists studying birds and mammals have emphasized the role of photoperiod, and other environmental cues have been suspected to be less important (Perfito et al., 2004).

Climate change is likely to lead to greater variability in food availability in some regions (e.g., (Song et al., 2006), resulting in reduced reproductive success in seasonally breeding species, if reproduction no longer coincides with periods of high food availability (Isaac, 2009). For example, great tits (Parus major) in the UK and pied flycatchers (Ficedula hypoleuca) in the Netherlands have suffered population declines over the last 20 years because reproduction increasingly fails to coincide with peak caterpillar abundance (Both et al., 2006; Visser et al., 2006; Visser & Both, 2005). Different temperature cues affect the timing of caterpillar emergence and the onset of breeding in great tits, resulting in phenological mismatch (Visser et al., 2006). Studies on arthropod availability and breeding timing have been heavily biased towards birds, but there are many threatened, seasonally breeding insectivorous mammals that may be at risk from changes in food availability patterns.

In marsupials, late stages of lactation are extremely energetically costly, so females and young benefit if breeding is timed so that late lactation coincides with a peak in food abundance (Dickman et al., 1983; Lee et al., 1982; Westman et al., 2002). Fisher et al.

(2013) showed that the month of weaning was most commonly the month of peak prey abundance in insectivorous marsupial species in which females produce one litter per year (or in a lifetime). However, this analysis was at a monthly scale averaged per species, and we lack understanding of how food cycles influence reproductive ecology of female marsupials at a population scale. Timing of breeding differs between populations of Australian insectivorous marsupials in the genus Antechinus (McAllan et al., 2006). The mating period lasts for one to three weeks during winter or early spring, depending on the species and location (Braithwaite & Lee, 1979; Woolley, 1966), and females give birth a month later. Male antechinus only reproduce once in their lifetime, and females reproduce either once or (less commonly) twice. Breeding during the time of peak food availability is likely to be crucial to population persistence (Fisher et al. 2013).

In antechinus species and populations, differences in timing of breeding between sites are associated with rate of change of photoperiod, which triggers breeding and varies among latitudes (McAllan et al., 2006). Rate of change may be a better cue than absolute photoperiod, because in Australia, peaks of insect abundance through the year are influenced by early increases in temperature at high latitudes and by late increases in rainfall at low latitudes (McAllan & Dickman, 1986; Van Dyck, 1981). A given rate of change of photoperiod occurs later in the year as latitude decreases, allowing antechinus to take advantage of south-north arrival of food peaks; different species respond to different rates of change (McAllan et al., 2006).

Antechinus species are distributed in an elevational gradient of species replacement on some mountain ranges, and at other locations species occur in sympatry (Mutton et al., 2017). Available data suggest that antechinus populations at low elevation breed earlier than those at high elevation at the same latitude (McAllan et al., 2006; Mutton et al., 2017), but it is unclear whether environmental cues other than photoperiod influence breeding timing. Additionally, it has been suggested that breeding season separation between antechinus populations may have led to speciation (Dickman et al., 1988). For example, if two populations experience different patterns of arthropod abundance because they inhabit different elevational ranges, separation of breeding timing can create reproductive isolation (Coyne & Orr, 2004; Dickman et al., 1988). There are very few examples of such allochronic isolation (i.e., differences in breeding times) leading to speciation in vertebrates (Friesen et al., 2007; Rolshausen et al., 2010).

Conversely, antechinus speciation may have been driven by physical separation of populations by geological processes (vicariance) (McCormack et al., 2010; Wiens, 2004). In Australia, rainforest is the ancestral habitat where much radiation of species in the Family Dasyuridae occurred. Australian rainforest has expanded and contracted during glacial–interglacial cycles over the past 10 million years (VanDerWal et al., 2009), and high elevation areas with long-term stability have acted as refugia where species can evolve or persist. These refugia may contain ancient species with restricted distributions, because they are relics of previously widespread taxa, or they have evolved in situ and failed to disperse to other habitats because of narrow niche specialisations (Fjeldsaå & Lovett, 1997; Roelants et al., 2004). We expect that antechinus species that diverged earlier may be restricted to high elevation refugia because of a long history of adaptation to high elevation, narrow niches, and more recently derived species are likely to occur at lower elevations.

Antechinus arktos, A. argentus and A. godmani have small ranges restricted to mountain- tops (IUCN, 2018). They are threatened by small population processes and climate change through increased temperatures and loss of montane habitat (Baker et al., 2014a; Baker et al., 2014b; Baker & Van Dyck, 2013), and may be vulnerable to changes in food availability and seasonality. At a landscape scale, breeding in antechinus is triggered by changes in photoperiod, but seasonal flushes of abundance of their arthropod prey are driven by rainfall and temperature, thus food availability and antechinus breeding time may become uncoupled. At a local population scale, social odour and pheromones act as cues to tightly synchronise breeding (Bradley & Monamy, 1990; Jones et al., 2003; McAllan et al., 2006). Thus, low population densities could exacerbate the negative effects of climate change on reproductive success of these threatened species (Calabrese & Fagan, 2004).

We hypothesise that: 1) Breeding season separation is a mechanism of fine-scale reproductive isolation between antechinus species with adjacent distributions on elevational gradients, therefore within a mountain range, antechinus species will show breeding season separation, such that higher elevation species breed progressively later; 2) Latitude affects breeding season separation between species at a macroecological scale in the subtropics and tropics through the mechanism of rate of change of photoperiod, therefore among mountain ranges, antechinus populations at higher latitudes will breed earlier; 3) The timing of cycles of prey availability is the mechanism of breeding season separation at the elevational spatial scale, so elevational breeding season separation will be consistent with adaptation to timing of peak food availability. We predict 53 that flushes in arthropod availability will occur later as elevation increases within each sampled latitude. We also predict that breeding season variation between latitudes will reflect the timing of arthropod abundance, so peak arthropod availability will occur earlier at higher latitude; 4) The most ancient species are restricted to high elevation refuge habitat, so species of older lineage age (i.e., that diverged earlier) will be restricted to mountain tops rather than lower elevations, so will breed later.

Methods

Breeding season separation

To determine breeding timing, gestation, birth and weaning, and distributions of eight antechinus species over elevational and latitudinal gradients, we sampled using Elliott-type (aluminium box) trapping at four mountains in Queensland, Australia: Springbrook National Park (28°, maximum elevation 1050m), Conondale National Park (26°, maximum elevation 800m), Kroombit Tops National Park (24°, maximum elevation 950m) and Danbulla National Park (17°, maximum elevation 1100m). Queensland is the centre of antechinus diversity (Baker & Dickman, 2018) and sampling at these locations allowed us to look at all possible species clusters with respect to elevation. At each location, we set up elevational transects on either side (east/west) of the mountain range, with at least three trapping sites spread from the base to the mountain-top (minimum six in total). We set out 50 traps, 10m apart, in two rows of 25 and trapped at each site for two consecutive nights per trip (100 trap nights) (Fisher, 2005; Mowat et al., 2015). In total, 1000 trap nights were conducted at Springbrook National Park, 2000 at Conondale National Park, 12000 at Kroombit Tops National Park and 1100 at Danbulla National Park.

We timed trapping trips to collect data on timing of breeding, gestation, birth and weaning. At each site we trapped for several days a minimum of once during the breeding season (winter), twice when young were attached to teats (spring), and once around the anticipated weaning date (summer). We identified captured antechinus to species using keys based on external morphology (Van Dyck et al., 2013) and recorded their location, indicators of breeding, and stage of life cycle. We recorded: mass, state of pouch, number of young, crown-rump lengths and lactation in females. As female antechinus age and enter the breeding season their mass increases, and their pouches develop and change in appearance (Woolley, 1966). Once the young are born, crown-rump lengths can be used to determine their age (Marlow, 1961), and if a female is lactating but has no young attached to her teats this indicates that young are in a nest. In captured male antechinus, 54 we recorded mass, testes width and length, tail width, fur patchiness and presence of ectoparasitic mites. Mass and testes size are indicators of breeding (Fisher et al., 2013). During the mating period, male condition deteriorates. Indicators include increased mite loads, fur loss, weight loss, decreased tail width and shrunken, pendulous testes. There is complete male mortality during the course of the mating season (Bradley, 2003). We determined timing and duration of the breeding season for antechinus populations from when female pouches began to redden until the last male was captured (McAllan et al., 1991). The divergence date of each antechinus species was taken from Mutton et al. (2018), who created a bayesian evolutionary analysis sampling tree (BEAST) phylogeny for antechinus.

Arthropod monitoring

We conducted arthropod monitoring to determine if antechinus time lactation to coincide with peak in arthropod availability, and how latitude and elevation affect the timing of peaks in arthropod abundance. We used 10 camera traps (Reconyx HyperFire Professional Series - PC850) on two elevational transects (east/west) at each mountain to conduct long-term sampling of ground dwelling arthropod availability (Collett & Fisher, 2017). We placed cameras facing downwards, 250mm above the ground to enable arthropod identification and set them on time lapse to take a photograph once every 15 minutes between 4pm and 6am (Collett & Fisher, 2017). We left the cameras at each location for two years and in total 40 cameras were deployed. Photographed arthropods were identified to the taxonomic level of Order and we calculated the number of arthropods captured on each camera per week of the year (Fisher & Dickman, 1993a).

Pitfall trapping arthropods

We used 10 plastic cup pitfall traps (at 10m intervals over 100m) at each of the camera trap sites to collect a reference sample of arthropods, to aid photo identification and to ground-truth camera data (140 trap nights per mountain range). We also sampled arboreal arthropods in trees using two 16cm long sticky traps (‘Buzz’ brand) at each site (28 trap nights per mountain range) (Dickman, 1991; Fisher & Dickman, 1993a; Green, 1989). We identified arthropods sampled with pitfalls and sticky-trap to Order (Fisher & Dickman, 1993a).

Data analyses

We used linear mixed effect logistic regression models with location included as a random factor to test associations between: 1) start of the breeding season (Julian week), elevation and latitude (Fisher et al., 2006); 2) arthropod availability and presence of young in the nest (yes or no) per Julian week; 3) highest arthropod availability (Julian week), elevation and latitude (Fisher et al., 2006); 4) mid-elevation of each species range and divergence date (Mutton et al. 2018). Arthropod availability per Julian week data was log transformed to normalise the distribution (Johnson, 1998a). We ran analyses in R 3.0.0 (R Development Core Team, 2013).

Results

We confirmed our first hypothesis that breeding season separation is a fine-scale mechanism of reproductive isolation between antechinus species with adjacent distributions on elevational gradients. Within each mountain range, antechinus populations on an elevational gradient showed breeding season separation such that higher elevation populations bred progressively later (Table 4.1; Figure 4.1). This was true both within and between species, for example lower elevation populations of Antechinus stuartii, A. mysticus and A. subtropicus bred several weeks earlier than higher elevation populations of the same species.

We refuted our second hypothesis that breeding seasons are separated consistently by latitude at a macroecological scale in the subtropics and tropics. Among mountain ranges in our sample, there was no statistical difference in breeding season between antechinus populations at different latitudes (Table 4.1). However, with the exception of the lowest latitude location (Danbulla National Park, 17°S) antechinus bred earlier at lower latitudes. For example, if all species and elevations are included, the breeding season commenced in June at Kroombit tops (24°S), July at the Conondales (26°S) and August at Springbrook (28°S) (Figure 4.1).

Our third hypothesis was that adaptation to the timing of cycles of prey availability is the mechanism of breeding season separation at the elevational and latitudinal spatial scales. Our results supported this hypothesis at the finer elevational scale, but refuted it at the larger latitudinal scale. Overall, timing of breeding was associated with the annual peak in arthropod availability. Populations had young in the nest (the high-demand period of late lactation) when arthropod abundance was highest (t = 3.84, p < 0.005, d.f = 459.7).

Elevational breeding season separation was consistent with adaptation to the timing of peak food availability, because flushes in arthropod availability and late lactation both occurred later as elevation increased. However, consistent with our finding that latitude had no consistent effect on the timing of breeding across species, there was no association between timing of peak arthropod availability and latitude (Table 4.1).

Our results supported our fourth hypothesis that the most ancient species are restricted to high elevation refuge habitat and breed later. Across mountains, older species occurred at high elevation sites, and younger species were found at lower elevation or had larger distributions that encompassed a wider elevational range (Table 4/1). As older species occurred at high elevation sites and had small distributions, they always bred later than younger species. For example, the Endangered Antechinus arktos (divergence approximately 3.5 mybp) is restricted to the highest elevation at Springbrook and bred several weeks later than the sympatric widespread species A. stuartii (divergence approximately 1.5 mybp), which has a distribution spanning a much larger elevational range (Figures 4.1 and 4.2).

Figures

Table 4.1.

Mixed linear models showing the association between altitude and latitude on Julian week antechinus commence breeding, Julian week arthropod availability is highest, and antechinus evolutionary age (BEAST). The evolutionary age model only included altitude.

Estimate se T value Pr Breeding Altitude 0.006 0.002 2.55 0.04 Latitude 0.185 0.127 1.26 0.25 Arthropods Altitude 0.009 0.003 2.98 0.03 Latitude -0.244 0.206 -1.19 0.29 BEAST Altitude 0.005 0.002 2.56 0.03

Danbulla National Park (17°S)

Kroombit Tops National Park (24°S)

Conondale National Park (26°S)

Springbrook National Park (28°S)

Figure 4.2. Antechinus distribution across mountains and lineage age of species (my = million years) captured in this study at Springbrook National Park (28°S), Conondale National Park (26°S), Kroombit Tops National Park (24°S) and Danbulla National Park (17°S).

Discussion

We found that timing of breeding in antechinus is associated with peaks in arthropod availability at small and large spatial scales, so that mothers are in the most demanding stage of lactation when food is most plentiful. McAllan et al. (2006) investigated breeding timing of ten antechinus species across a range of latitudes, including five species in southern Australia. In contrast to the Australia-wide study by McAllan et al. (2006), we found no significant association between breeding timing and latitude in the subtropical and tropical latitudes of Queensland. Rather than being associated with latitude per se, breeding appears to be related to specific environmental conditions experienced at each site. Tropical Antechinus godmani bred much later than species in subtropical southern Queensland. Because we found evidence that antechinus breeding times track peaks of food availability, this is consistent with rainfall being the major climate driver of cycles of arthropod abundance at low latitudes, rather than temperature (Van Dyck, 1981). In Queensland, there is predominantly summer rainfall in the wet tropics, and spring rainfall at higher subtropical latitudes (BOM, 2016).

Our study was conducted throughout subtropical and tropical Queensland, and rate of change of photoperiod becomes difficult to detect near the equator (Bronson, 2009). Silverin et al. (2008) showed that photoperiod has a large influence on breeding timing of 62 great tits (Parus major) at high latitudes, but the relative importance of environmental cues increased at low latitudes. The response of mammals to photoperiod significantly decreases at latitudes lower than 30 degrees (Bronson, 2009) and lack of photoperiodic response has been documented in tropical rodents (Demas & Nelson, 1998; Bronson & Heideman, 1992). We still have little understanding of how seasonal breeding is triggered in tropical mammals. In our study, they used local environmental cues associated with predictable annual changes in food availability.

Our results suggest that antechinus time breeding to increase the chance of successfully weaning young, because climate and timing of seasonal flushes of prey availability vary with latitude in the subtropics and tropics. A similar strategy occurs in birds that time their migration to arrive when reproductive success is most likely (Both, 2010; Both & te Marvelde, 2007; Conklin et al., 2010). For example, Conklin et al. (2010) found that bar- tailed godwits (Limosa lapponica baueri) vary migration schedules to coincide with timing of snow-melt and thus food availability at their respective breeding sites. Similarly, Loe et al. (2005) compared timing of red deer (Cervus elaphus) breeding between France and Norway and found that breeding began earlier in France because of an earlier peak in forage digestibility.

Our study corroborates results from research on Antechinus agilis and A. mimetes in the Australian high country, and A. subtropicus and A. mysticus in subtropical Queensland (Dickman et al., 1983; McAllan et al., 2006; Mutton et al., 2017) where antechinus populations at low elevation bred first and timing was delayed with increasing elevation. This was true not only between species, but also within populations of the same species at our study locations. Although previous studies have shown that rate of change of photoperiod is the main trigger of antechinus breeding (McAllan et al., 1991; McAllan et al., 2006), photoperiod remains relatively constant across elevations. Our finding that breeding timing is different between species and populations of antechinus across elevations suggests that photoperiod is not the only environmental cue that triggers breeding. Within latitudes, timing of peak arthropod availability occurred later as elevation increased, indicating that antechinus breeding is partly associated with a local environmental stimulus such as increased energy intake or temperature, which varies in a constant manner with elevation (Brown, 2001). This mechanism is in agreement with the conclusions of Perfito et al., (2004) in song sparrows (Melospiza melodia morphna), who found that although photoperiod is considered to be the primary reproductive trigger, montane populations of this bird have later reproduction than coastal populations, coinciding with the opening of 63 spring shoots and buds. In antechinus, patterns of spring arthropod availability depend on the timing of arthropod emergence, which is driven by small temperature changes. Higher elevations warm slightly later in spring, delaying arthropod emergence time (Forrest & Thomson, 2011; Tulp & Schekkerman, 2008) and therefore antechinus reproduction.

In our study, multiple antechinus species occurred on each mountain, and species with ranges restricted to mountain-tops were always more ancient. We found that where antechinus species are sympatric in Queensland, the more recently-evolved species always had a larger range extending down the mountain, and an earlier breeding time. This corroborates a recent study by Gray et al. (2017a) who found that A. stuartii always breeds earlier than its symptric congener A. arktos in southern Queensland. Ancient species have smaller ranges, and are often restricted to high elevation sites (Bridle & Vines, 2007). Long periods of evolution in stable, mountain-top conditions may mean that these ancient, range-restricted species have become highly specialised, resulting in reduced adaptability to varying temperatures and patterns of arthropod availability. This in turn restricts their dispersal into lower elevation habitats and potentially makes them more vulnerable to a changing climate (Fjeldsaå & Lovett, 1997; Galbreath et al., 2009; Gür et al., 2018; Waltari & Guralnick, 2009).

Dickman et al. (1998) suggested that allochronic isolation through differences in breeding timing may have lead to speciation in antechinus, however Mutton et al. (2018) concluded that speciation in antechinus has generally resulted from biogeographic barriers and increasing aridity. Geographical isolation of rainforest patches caused by climate oscillations has driven divergence across all major animal groups in Australia, with particularly strong phylogeographic patterns in montane tropical and subtropical rainforests (Byrne et al., 2011). Our results suggest that the most ancient antechinus were restricted to mountain-tops as a result of continental drying, and therefore breed at a time that suits mountain-top conditions of relatively late peak arthropod availability. More recently-evolved congeners may have subsequently dispersed from other locations to the lower elevations of these mountains, and breed earlier, to coincide with arthropod emergence at low elevations. After long-term isolation when dispersal with other regions is possible, ecological interactions including competition influence species distributions (MacArthur, 1984; Price & Kirkpatrick, 2009). Whether closely-related species become sympatric is partly associated with both phylogenetic time since divergence and the morphological differences between them (Pigot & Tobias, 2013). In some cases, antechinus species have remained separated across elevational zones, and in other cases species are 64 sympatric on mountain-tops. In all sites where species were sympatric there was large body size difference between them, suggesting a role of competition (Dickman, 1986).

Dickman et al. (1983) showed that in the southern (cool temperate zone) Australian alps, A. mimetes has a larger elevational range than A. agilis, breeds earlier when the two species are sympatric at low elevation, and delays reproduction with increasing elevation. Antechinus agilis does not significantly change its timing of breeding with elevation. Dickman et al. (1983) hypothesised that at low elevation, the two species breed at different times because they have different foraging strategies; A. mimetes hunts in leaf litter and digs for prey, and A. agilis preys on arboreal and litter arthropods. These prey may show different cycles of abundance. At high elevation, niche separation and therefore difference in breeding timing is reduced because of a decline in food availability. Recent phylogenetic research suggests that A. agilis is at least two million years older than A. mimetes (Mutton 2017) and is likely to have been restricted to rainforest refugia during the Pleistocene (Beckman et al., 2007). This specialisation may also contribute to the smaller range and lack of flexibility in breeding timing seen in A. agilis.

Climate Change has altered timing of food availability, resulting in phenological mismatch and population declines for species from a range of taxa including fish (Beaugrand et al., 2003; Edwards & Richardson, 2004), plankton (Winder & Schindler, 2004) and birds (Both et al., 2006; Visser et al., 2006). However, timing of breeding is thought to be a heritable trait (Price et al., 1988; Visser, 2008) and in many cases species have been able to adapt their breeding times to advances in spring phenology (Both, 2010; Parmesan, 2007; Rosenzweig et al., 2007; Tulp & Schekkerman, 2008). Our conclusion that local environmental conditions are associated with timing of antechinus breeding suggests that antechinus may be able to adapt to small changes in patterns of arthropod availability as a result of global warming. However, large climatic changes such as failure of seasonal rains may result in loss of young and lead to severe declines (Friend, 1985). Antechinus and other seasonally breeding insectivorous marsupials may be more adaptable than previously thought, however, Antechinus are constrained by short lifespans and male semelparity, putting them at substantial risk from climate change.

CHAPTER 5: Discussion and final remarks

Image: Springbrook National Park and the endangered Antechinus arktos (Gary Cranitch).

General discussion

This thesis has advanced understanding of the life history, biogeography and macroecology of the Family Dasyuridae, in particular antechinus, and has provided insight into why particular species are rare. The results presented have highlighted the importance of understanding the relationships between life history, climate, food availability, population dynamics and evolutionary history across large and small spatial scales. Specifically, four major findings have resulted from this study:

1. dasyurids have two separate axes of life history variation. The reproductive output axis is associated with productivity and overall food availability, and the second axis, which is a gradient from semelparity to iteroparity, is correlated with food predictability;

2. across eastern Australia, dasyurid population density is highest in temperate regions. In Queensland, antechinus population density is highest at high latitudes and elevations. Abundance of insectivorous marsupials is limited by winter food availability. This is related to winter rainfall, which is lowest in the tropics and at low elevation;

3. across mountains in Queensland, the oldest antechinus species are restricted to high elevations and have smaller ranges than more recently-evolved congeners. Breeding timing of antechinus populations differs across elevation, in accordance with timing of peak arthropod availability. Ancient antechinus species may be unable to extend their range into lower elevations because they cannot adapt to different patterns of prey availability or because they have highly specific climatic and habitat requirements;

4. in addition to anthropogenic threats and life history traits, dasyurid and antechinus rarity is evidently influenced by: 1) patterns of rainfall and food availability, which are related to latitude and elevation; 2) niche size and adaptability; 3) evolutionary history.

Climate change and life history

In her review of the effects of climate change on life history in mammals, Isaac (2009) stated that there is a paucity of research on climate change responses for species in the tropics and the southern hemisphere. She also concluded that our understanding of how climate change will affect species extinction risk is limited, because we lack knowledge of how life history traits co-vary. Chapters in this thesis concerning life history of dasyurid marsupials have clarified how life history traits co-vary and are related to climatic variables. This is valuable in predicting how climate change might affect insectivorous marsupials, and gives us a broader understanding of life history evolution that can be applied in a global context.

Many predictions of how species persistence will be influenced by climate change have been based on the fast-slow life history continuum (Benton & Grant, 1996; Tuljapurkar, 1990), or the r-K models of life history variation. r and K selection models focus on density- dependant population regulation, resource availability and environmental fluctuations to explain why different life history traits evolve (MacArthur & Wilson, 1967; Pianka, 1970). r selected traits are compatible with fast population growth, and include early maturity and high reproductive rate. Examples of K selected traits, which enhance persistence in competitive environments, are long lifespan and low fecundity. MacArthur and Wilson (1967) suggested that K-selected life histories are predominant in stable environments and that these species should be resilient to stochastic climatic events. It is assumed that species with r-selected life histories live in variable environments and will be adversely affected by extreme events but may be less prone to extinction in the long-term (Benton & Grant, 1996; Pribil & Houlahan, 2003; Tuljapurkar, 1990). I showed that life history variation in dasyurids does not neatly fit the fast-slow continuum or conform to r-K environmental assumptions. I found two life history axes, which are differentially associated with the environment. The reproductive output axis is associated with productivity, and the semelparity–iteroparity axis is correlated with food predictability. Contrary to predictions, long-lived dasyurid species occur in variable environments and short-lived species are found in predictable habitats. r and K selection went out of favour after the 1970s, and was replaced by the fast-slow continuum and demographic models (Stearns, 1992). Although life history theory no longer focuses on r and K selection, the results of chapter 2 concord with conclusions of Reznick et al. (2002) who demonstrated that density-dependant regulation, resource availability and environmental fluctuations are important parts of natural systems and life history evolution. 68

When determining species resilience to climate change, individual life histories and environmental requirements need to be taken into account. My results show that dasyurids in central deserts are generally iteroparous, and these species may be well equipped to cope with increased instability of climate and food availability, as they already live in unpredictable habitats and have bet-hedging strategies that allow populations to persist with loss of young. These species also often possess behavioural or physiological strategies for surviving food shortages. For example, there is evidence that long-lived, desert-dwelling dasyurids are capable of moving large distances to track rainfall (Dickman et al., 2011; Dickman et al., 2001; Haythornthwaite & Dickman, 2006). However, these habitats are generally unproductive, and resulting low reproductive rates mean that events such as wildfires can decimate populations and survivors are unable to rapidly recruit. Changed fire regimes that have increased the severity of wildfires have been implicated as a cause of extinction for several mammalian species in central Australia (Flannery, 2002; Letnic, 2003; Southgate & Masters, 1996), and there are predictions that fires may increase in frequency and intensity with climate change (IPCC, 2014; Williams et al., 2001).

Females of some dasyurid species such as antechinus are facultatively semelparous (they often die after weaning one litter) (Fisher & Blomberg, 2011) and live in productive environments. They have large litters and generally high population densities. High density is essential for antechinus persistence, because many species nest communally in winter for warmth and potentially also for social reasons (Fisher et al., 2011; Lazenby-Cohen, 1991). They have promiscuous mating systems in which both sexes mate with a large number of partners (Bradley, 2003; Kraaijeveld-Smit et al., 2002; Sale et al., 2013). Climate change is predicted to increase severe droughts in Australia (IPCC, 2014), and resulting reduction in antechinus population density may lead to a collapse of their mating system and subsequent local extinction. Drought has been implicated in range reductions and population declines of multiple antechinus species including: the agile antechinus (A. agilis) (Parrott et al., 2007), the dusky antechinus (A. swainsonii) (now A. mimetes) (Recher et al., 2009) and the swamp antechinus (A. minimus) (Sale et al., 2008).

Dasyurid species on the semelparous end of the spectrum are prone to local extinction in environments with unpredictable rainfall and food resources. For example, the red-tailed phascogale (Phascogale calura) is a facultatively semelparous dasyurid that was previously found throughout much of arid and semi-arid Australia. The range of Phascogale calura has contracted to climatically predictable remnant vegetation in south- 69 western Australia and now occupies less than one percent of its former range (Short & Hide, 2011). Kitchener (1981) suggested that the red-tailed phascogale has been lost from unpredictable, semi-arid habitat because increased reproductive failure due to droughts exacerbated by pastoralism was catastrophic for semelparous species. Similar to the genus Antechinus, phascogales appear to be particularly susceptible to drought because of its impact on invertebrate food supply and recruitment (Friend et al., 1996; Rhind & Bradley, 2002), and winter rainfall is declining by three to four percent per decade in Western Australia (Pearce et al., 2007).

Rainfall predictability is more likely to be altered by climate change than overall productivity (IPCC, 2014). My finding that the semelparity–iteroparity axis is associated with arthropod predictability suggests that this will therefore be more important than the reproductive output axis for predicting climate change threats to insectivorous marsupials. Semelparous species are likely to be most threatened by climate change because short, annual breeding seasons increase the chances of phenological mismatch, and one year of failed recruitment can jeopardise the persistence of local populations. There is a possibility that with decreasing rainfall and arthropod predictability, where there is phenotypic plasticity, insectivorous marsupials may become more iteroparous over time. Changes in life history strategy have been documented in dasyurids, suggesting that there is potential for adaptation. For example, since the emergence of the devil facial tumour disease, female Tasmanian devils (Sarcophilus harrisii) have changed from iteroparity in nearly all individuals to breeding in their first year, and most females having a single breeding season. There is selection for earlier reproduction in Tasmanian devil populations because adult survival has been reduced to a greater extent than juvenile survival, and it is now rare for females to survive long enough to breed twice. Thus, females that would breed in their second year have not passed on their genes (Jones et al., 2008). Similarly, male dibblers (Parantechinus apicalis) and northern quolls (Dasyurus hallucatus) are semelparous in some populations, but can survive for two years in others (Dickman & Braithwaite, 1992; Wolfe et al., 2004). We currently do not understand why there is difference in the semalparity between populations. Wolfe et al. (2004) suggested that male dibblers may survive to reproduce a second time in areas where seabird input increases productivity and therefore food availability. However, my findings indicate that degree of iteroparity is related to environmental predictability. Where arthropod availability and juvenile survival is unpredictable, it may be advantageous for males to breed in multiple years, leading to a change in life history strategy. However, Dollo’s Law, which states that

70 the loss of complex features in evolution is irreversible (Bull & Charnov, 1985), may mean that dasyurid species such as antechinus that have evolved extreme male semelparity are unlikely to be able to reverse their life history to suit unpredictable conditions, increasing their likelihood of extinction. Males exhibit spermatogenesis before the mating season, and there is no variation in this trait between individuals, which indicates it is not likely to be influenced by natural selection (Collin & Miglietta, 2008).

Distribution of food in time and space

My research investigated the relationship between annual rainfall, rainfall predictability and arthropod availability across Australia. The results suggest that the distribution of food resources across time and space is complex for insectivorous vertebrates. We found that areas with high productivity and high food availability per year are not necessarily predictable, and some regions with low food availability can be highly predictable. This result suggests that we need to consider multiple aspects of food availability when investigating how energy is associated with species life history and ecology. These complex relationships have also been noted by Morellet et al. (2013), who found that home range size of roe deer (Capreolus capreolus) across Europe decreased with increasing food availability, except at the southernmost and northernmost latitudes of the species’ range, where the pattern was reversed. This was related to seasonality and local environmental conditions, as species in far northern and southern latitudes had to compensate for a shorter growing season or summer droughts by foraging over larger areas. Although the tropics are considered to be highly productive with abundant food, the present study suggests that low latitudes also have large seasonal fluctuations in food availability for insectivorous species. The results also show that food availability is variable between locations at the same latitude and that other landscape features need to be taken into account. For example, I found that timing of peak arthropod availability changes substantially across elevation, consistent with differences in breeding timing between antechinus populations occurring at the same latitude. These small-scale differences in food availability may be particularly important for animals with low mobility, such as montane mammals with specific climatic requirements that exist in small habitat patches and are unable to track variation in food availability (Silva et al., 1997).

Rarity and food availability

My research showed that antechinus population density in Queensland is related to winter food availability, which is associated with rainfall. This could explain the rarity of 71 antechinus species in the seasonal subtropics and tropics with low winter rainfall, including the Endangered silver-headed antechinus (A. argentus) at Kroombit Tops, and the restricted Atherton antechinus (A. godmani) and rusty antechinus (A. adustus) at Danbulla National Park. The present results indicate that abundance of other dasyurid species may also be limited by winter food availability, as dasyurid population density increases with latitude across eastern Australia. For example, the white-footed dunnart (Sminthopsis leucopus) is almost 100 times more abundant at high latitude sites in southern New South Wales and Victoria (Laidlaw et al., 1996; Lunney & Ashby, 1987) than it is in north Queensland, where S. leucopus had not been captured since 1997 (Watt, 1997), until my project (Appendix A).

My finding that population densities are associated with food availability during the harshest time of year is likely to be applicable to insectivorous endotherms globally (Silva et al., 1997; Williams & Middleton, 2008), but how patterns of rarity vary geographically will depend on local environmental conditions. The results from this thesis corroborate a recent study by Santini et al. (2018), which looked at global drivers of population density for vertebrates. Santini et al. (2018) found that population densities of birds and mammals were highest in mesic areas at temperate latitudes, and seasonal rainfall was negatively associated with mammal abundance. Novosolo et al. (2016) and Williams and Middleton (2008) also reported that precipitation can influence population density by affecting food fluctuations, which in turn regulates mortality. We still know little about how climatic conditions and food availability affect population density, and research in this area will be important for forecasting population trends under environmental change (Ashcroft et al., 2017).

Dasyurid species at risk

This thesis suggests that for the Family Dasyuridae in Australia, tropical dasyurids and species in seasonal areas with low productivity are likely to be most threatened by climate change. We found that tropical dasyurid species have high extinction risk because of low abundance caused by winter food shortage, which creates a population bottleneck. This may be compounded by increased predation rates in the tropics. Although data was not collected on predation rates in this project, a recent global analysis by Roslin et al. (2017) found that predation risk of model caterpillars increased towards the equator and at low elevations. These patterns were driven by arthropod predators, and there was no evidence for increased rates of predation by vertebrates. However, the idea that biotic interactions

72 are stronger in the tropics has a long history in the literature (Dobzhansky, 1950; MacArthur, 1984; Pennings & Silliman, 2005) and this warrants further investigation.

If regions with predictable rainfall become less predictable, and timing of peak prey availability changes, species that only produce one litter per year (or in a lifetime) may fail to wean young (Braithwaite & Lee, 1979). This may be particularly applicable to species living in seasonal areas with low productivity that are unlikely to have sufficient food if rainfall patterns change. For example, facultatively semelparous dasyurids such as the little red kaluta (Dasykaluta rosamondae) and the northern quoll (Dasyurus hallucatus) living in the semi-arid Pilbara, where seasonal rainfall events are predicted to become less frequent, may be particularly at risk (Hayes, 2018; Hernandez-Santin et al., 2016; McCaw, 2013).

For antechinus in Queensland, ancient species that are restricted to high elevations (A. arktos and A. godmani) are likely to be most at risk from climate change. These species have evolved in predictable habitats, and the present result that timing of breeding does not change significantly across their restricted elevational ranges, suggests that they may not be able to adapt easily to changes in timing of arthropod availability. Additionally, increased temperatures with climate change and contraction of cool-adapted forest to smaller areas of higher elevation land will likely severely affect mountain specialists (Colwell et al., 2008; Lenoir et al., 2008; Williams et al., 2007). Over the last 50 years, Antechinus arktos has retreated to mountain summits, and preliminary evidence from this study suggests that in north Queensland, A. adustus and A. godmani no longer occur at historical low elevation sites (Appendix B). The IUCN (2015) states that A. adustus and A. godmani are found above 600m, but I was unable to detect these species below 850m. More sampling needs to be conducted to confirm whether this is an ongoing trend. Likewise, modelling predicts that many other mammalian mountain specialists in north Queensland will undergo range contractions with climate change (Meynecke, 2004; Williams et al., 2003), but very few studies have been conducted to verify whether this is already occurring. Antechinus argentus at Kroombit Tops is most affected by low winter food availability and also has a small distribution restricted wettest habitat on mountain- tops, putting this species at substantial risk of extinction.

Concluding remarks

The results from this thesis show how distribution of dasyurid marsupials depends on the distribution of their arthropod prey in space and time. Food availability driven by rainfall 73 patterns is important in explaining the macroecology and life history evolution of dasyurid species. My finding that antechinus species in Queensland are distributed across elevations in accordance with lineage age suggests that mountain building vicariance events have influenced antechinus speciation (Mutton et al. 2017). The idea that allochronic isolation may have led to sympatric speciation seems less likely. The latter hypothesis assumes there is limited flexibility in breeding timing within species, whereas the present results indicate that antechinus populations across elevational ranges may adapt their breeding timing to suit changes in peak arthropod availability.

A substantial proportion of the world’s vertebrate fauna is insectivorous, and the prey base for these animals appears to be declining globally (Dirzo et al., 2014). Evidence suggests that invertebrates have declined even more severely than vertebrates over the past 500 years, but their cryptic and uncharismatic nature means that loss of invertebrate biodiversity has received relatively little attention (Dirzo et al., 2014; Hallmann et al., 2017). Additionally, loss of invertebrates is mainly discussed in relation to ecosystem services such as pollination, decomposition and nutrient cycling (Dirzo et al., 2014). Loss of invertebrates can also significantly affect food webs and predator persistence. For example, North American birds that feed on insects are experiencing widespread population declines, which are apparently linked to changes in aerial insect abundance (Fraser et al., 2012; Nebel et al., 2010; Paquette et al., 2014). Similar studies have not been conducted on other groups of insectivores, but understanding the relationship between predators and their prey is critical for preventing further extinctions. Maintaining arthropod abundance should be a high conservation priority, as these species are important in their own right, and declines are likely to have detrimental effects on insectivorous populations worldwide (Hallmann et al., 2017).

It is evident from the present study that climate change is likely to be a major threat to the persistence of dasyurid marsupials. With changed climatic conditions, insectivorous species will need protected areas with high arthropod availability that allow them to move to higher elevations or persist in the landscape (Reside et al., 2013). Thus, it is important to identify and preserve refuge areas. Most montane, high elevation habitats where dasyurid species occur have acted as refugia during past climatic changes and are currently in national parks. The present study found that many Australian mountain-tops maintain high arthropod availability year round because they receive moisture from cloud- drip and orographic rainfall, where mountains cause moist air to rise. This suggests that high elevation sites are likely to be suitable refuge areas under scenarios of ongoing 74 climate change. Unfortunately, we still have very little knowledge about what constitutes a suitable dasyurid refuge in arid regions. Small mammals in the arid zone occur across vast areas and much of this is under pressure from farming, pastoralism and tourism (Pavey et al., 2017). In order to persist through years of drought, species in the arid zone retreat to habitat patches where food is still available. Research has shown that refuges are species- specific, and that dasyurids rarely use vegetation patches historically assumed to be refuge areas (Dickman et al., 2011; Pavey et al., 2017). For example, the fat-tailed dunnart (Sminthopsis crassicaudata) and the stripe-faced dunnart (S. macroura) may retreat to non-vegetated patches of cracking clay that provide moisture during small, localised rainfall events (Brandle & Moseby, 1999; Pavey et al., 2014). More research needs to be conducted into arid zone refuges for insectivorous mammals, as current knowledge is extremely poor.

Finally, the present study found that timing of antechinus breeding relies in part on local environmental stimuli, and species with small ranges seem to have limited flexibility in breeding timing. This suggests that maintaining dispersal opportunities between populations is important for increasing the adaptive potential of life history characteristics. It is therefore essential to conserve habitat between refuge areas to increase connectivity and flow of individuals exposed to different environments.

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APPENDICES

Image: Sminthopsis leucopus from Danbulla National Park (Gary Cranitch)

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Appendix A

Table 1. Dasyurid life history traits for each species included in our analyses. FML = female maximum lifespan (years), MLS = mean litter size, WRS = length of reproductive season (weeks), NBE = number of breeding events, SY = supernumerary young (yes or no), RSS = rainfall seasonality sine (Colwell’s P value), AR = annual rainfall (millilitres), and M = mass (grams).

Species FML MLS WRS P NBE SY RSS AR M Antechinomys laniger 3 6 28 Yes 2 No 0.62 198.8 20 Antechinus agilis 2 10 4 No 1 Yes 0.50 1201 18 Antechinus bellus 2 10 2 No 1 Yes 0.86 1709.6 34 Antechinus flavipes 3.5 8.4 4 No 1 Yes 0.61 883.2 34 Antechinus godmani 2 6 3 No 1 Yes 0.80 819 61 Antechinus leo 2 9.6 2 No 1 Yes 0.78 1583 54 Antechinus minimus 2 7.4 3 No 1 Yes 0.72 605.5 42 Antechinus stuartii 2 7.15 2 No 1 Yes 0.61 1091.2 20 Antechinus subtropicus 2 6.9 3 No 1 Yes 0.59 1200 22 Antechinus mimetes 2 8.9 4 No 1 Yes 0.53 1176.8 41 Dasycercus cristicauda 3 4 20 No 1 No 0.69 393.5 100 Dasykaluta rosamondae 3 6.3 3 No 1 No 0.72 285.7 30 Dasyuroides byrnei 6 4.3 32 Yes 2 Yes 0.67 213.6 100 Dasyurus hallucatus 2.5 6.63 4 No 1 Yes 0.7 890 400 Dasyurus viverrinus 4 6 6 No 1 Yes 0.48 900 880 Ningaui ridei 2 6.1 20 No 1 No 0.64 284.9 8 Parantechinus apicalis 2 7.1 4 No 1 Yes 0.75 611.9 58 Parantechinus bilarni 2.5 4.8 3 No 1 Yes 0.85 1352.2 25 Phascogale calura 3 5.5 4 No 1 Yes 0.66 391.9 43

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Phascogale tapoatafa 4 6.1 8 No 1 Yes 0.52 676.6 156 Planigale gilesi 5 6.5 20 Yes 2 No 0.55 214.9 6.9 Planigale ingrami 1.3 8.5 6 Yes 2 No 0.99 612.6 5 Planigale maculata 3.5 9 20 Yes 2 No 0.76 1840 10 Planigale tenuirostris 3 6.5 24 Yes 2 No 0.55 215.6 5.3 Pseudantechinus macdonnellensis 2.5 5.9 6 No 1 Yes 0.68 290.2 30 Pseudantechinus ningbing 2 6 4 No 1 Yes 0.89 832.2 25 Sminthopsis crassicaudata 4.3 7.4 28 Yes 2 Yes 0.42 705.9 15 Sminthopsis douglasi 2 7.7 3 Yes 2 Yes 0.80 462 70 Sminthopsis griseoventer 2.5 6 6 No 1 No 0.67 611.9 19 Sminthopsis leucopus 2.5 8 12 Yes 2 No 0.72 931.8 19 Sminthopsis macroura 3 6.5 36 Yes 2 No 0.69 550.3 20 Sminthopsis murina 2 8 24 Yes 2 No 0.59 1206.8 14 Sminthopsis ooldea 3 5.5 20 No 1 No 0.59 246 15 Sminthopsis virginiae 1.75 2.5 20 Yes 2 No 0.72 1509.3 34

Table 2. Dasyurid species included in this study and the published studies data was collated from.

Species Studies Antechinomys Valente, A. 1995 Kultarr In The Australian Museum complete laniger book of Australian Mammals (ed. R. Strahan) pp. 121-122. Sydney: Reed Books. Woolley, P. A. 1984 Reproduction in Antechinomys laniger ("spenceri" form) (Marsupialia: Dasyuridae): Field and laboratory investigation Australian Wildlife Research, 11, 481-490. Antechinus agilis Dickman, C.R. 1995a Agile antechinus In The Australian Museum complete book of Australian Mammals (ed. R. Strahan) pp. 100- 101. Sydney: Reed Books. Personal trapping records.

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Appendix B

Table 1. Site locations, survey periods and effort (total trap nights) for one live and two camera trap captures of Sminthopsis Leucopus in north Queensland.

Site Location Survey Latitude & Elevation Pitfall Elliott Camera ID Period Longitude (metres) trap trap trap nights nights nights 17°44'41" Tully 26/7/14– SVD1 145°32'02" 820 15 150 - Falls N.P 29/7/14

17°43'55" Tully 26/7/14– SVD2 145°32'30'' 865 12 150 - Falls N.P 29/7/14

17°43'53" Tully 26/7/14– SVD3 145°32'24'' 867 15 150 - Falls N.P 29/7/14

17°07'45" Danbulla 30/7/14– KY1 145°37'20'' 693 6 58 - N.P. 2/8/14

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17°07'44" Danbulla 30/7/14– KY2 145°37'15'' 690 6 38 - N.P. 2/8/14

17°07'02" Danbulla 30/7/14– KY3 145°36'17'' 728 9 38 2 N.P. 2/8/14

17°07'34" Danbulla 30/7/14– KY4 145°36'25'' 730 6 38 2 N.P. 2/8/14

17°07'42" Danbulla 30/7/14– KY5 145°36'24'' 709 9 38 2 N.P. 2/8/14

S17'07.727 Danbulla 1/8/16– E145'37.341 RC9 728 – 100 100 N.P. 4/8/16

S17'07.710 Danbulla 1/8/16– E145'36.380 RC10 755 – 100 100 N.P. 4/8/16

S17'07.711 Danbulla 1/8/16– E145'36.372 RC11 900 – 50 100 N.P. 4/8/16

S17'06.191 Danbulla 4/8/16– E145'36.682 RC12 900 – 100 100 N.P. 7/8/16

S17'05.643 Danbulla 4/8/16– E145'36.637 RC13 1000 – 100 100 N.P. 7/8/16

Danbulla 4/8/16– S17'05.433 RC14 1100 – 100 100 N.P. 7/8/16 E145'37.298

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Appendix C

Table 1. 2016 captures of Antechinus godmani and Antechinus adustus at sites within their historical distribution in north Queensland.

Location Survey Latitude Elevation Elliot A.godmani A.adustus period and (metres) trap captures captures longitude nights

S17'46.465 Tully Falls 9/6/16– E145'32.985 715 50 Nil Nil N.P 12/6/16

S17'07.727 Danbulla 4/8/16– E145'37.341 728 100 Nil Nil N.P. 7/8/16

S17'07.710 Danbulla 4/8/16– E145'36.380 755 100 Nil Nil N.P. 7/8/16

S17'47.748 Tully Falls 9/6/16– E145'32.478 781 50 Nil Nil N.P 12/6/16

S17'43.880 Tully Falls 9/6/16– E145'32.435 856 100 1 male Nil N.P 12/6/16

S17'41.953 Tully Falls 9/6/16– E145'31.391 889 100 Nil Nil N.P 12/6/16

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S17'07.711 Danbulla 4/8/16– Males and E145'36.372 900 50 1 male N.P. 7/8/16 females

S17'06.191 Danbulla 4/8/16– Males and E145'36.682 900 100 Only males N.P. 7/8/16 females

S17'05.643 Danbulla 4/8/16– Males and Males and E145'36.637 1000 100 N.P. 7/8/16 females females

S17'41.084 Tully Falls 9/6/16– E145'31.371 1014 100 Nil Nil N.P 12/6/16

S17'05.433 Danbulla Males and Males and 4/8/16– E145'37.298 1100 100 N.P. 7/8/16 females females

Appendix D

This appendix has been published as:

Collett, R.A. and Fisher, D.O. (2017) Time-lapse camera trapping as an alternative to pitfall trapping for estimating activity of leaf litter arthropods. Ecology and Evolution, 7(18), 7527–7533.

Time-lapse camera trapping as an alternative to pitfall trapping for estimating activity of leaf litter arthropods

Rachael A. Collett and Diana O. Fisher

School of Biological Sciences, The University of Queensland, St Lucia, QLD, 4072, Australia.

Corresponding author: [email protected]

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Summary

1. Pitfall trapping is the standard technique to estimate activity and relative abundance of leaf litter arthropods. Pitfall trapping is not ideal for long-term sampling, because it is lethal, labour intensive and may have taxonomic sampling biases. We test an alternative sampling method that can be left in place for several months at a time: horizontally placed time-lapse camera traps that have a short focal distance, enabling identification of small arthropods.

2. We tested the effectiveness of these time-lapse cameras, and quantified escape and avoidance behaviour of arthropod orders encountering pitfall traps by placing cameras programmed with a range of sampling intervals above pitfalls, to assess numerical, taxonomic and body size differences in samples collected by the two methods.

3. Cameras programmed with one minute or 15 minute intervals recorded around twice as many arthropod taxa per day and a third more individuals per day than pitfall traps. Hymenoptera (ants), Embioptera (webspinners) and Blattodea (cockroaches) frequently escaped from pitfalls so were particularly under-sampled by them.

Synthesis and applications

The time-lapse camera method effectively samples litter arthropods to collect long-term data. It is standardised, non-lethal, and does not alter the substrate, or require frequent visits.

Key words

Invertebrate sampling, time lapse, insects, insectivorous, prey availability

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Introduction

Pitfall trapping is the most commonly used method to estimate activity and relative abundance of ground-dwelling arthropods in ecological studies, and for monitoring (Spence & Niemela 1994, Lovei & Sunderland 1996). For example, researchers have used pitfall trapping data to calculate measures of prey availability in studies of dietary ecology (Fisher & Dickman 1993a, Fisher & Dickman 1993b) and life history evolution (Fisher et al. 2013), as indicators of disturbance in studies of fire and logging (Lawton et al. 1998; Barrow, Parr & Kohen 2007), to estimate rates of extinction (Dirzo et al. 2014), to test hypotheses in community ecology and biogeography (Dickman 1988; Driscoll 2005), and in agricultural pest management (Kromp 1999). To date, there have not been any practical alternative methods for such studies (Spence & Niemela 1994).

Pitfall trapping can be a useful method to sample arthropod availability, because the traps are cheap and simple to deploy, and daily samples from each trap can be kept in preservative and used to collect further information (Topping & Sunderland 1992, Santos et al. 2007); to identify the samples to species, use as reference collections in dietary analysis, or obtain genetic samples

Pitfall trapping also has a number of logistical drawbacks. It can be labour intensive if pitfall traps must be emptied and refilled with preservative frequently to obtain replicates, and to ensure that they are still sampling effectively (e.g. Parker et al. 1997, Fisher & Dickman 1993a, McKinnon et al. 2012). If left unmonitored, pitfall traps can be flooded, dug out of the ground and destroyed by animals, or otherwise disturbed. Sampling of remote areas is thus limited to relatively short periods during field trips. Pitfall traps can also by-catch small vertebrates, meaning that their use is increasingly restricted by animal ethics committees (Lange & Weisser 2011). Digging in pitfall traps is unacceptable at some sites such as land of special significance to indigenous owners or environmentally sensitive areas, and too difficult in some substrates, such as rock pavement.

A large methodological issue with using pitfall traps is that they do not sample taxa at random from the leaf litter arthropod community (Luff 1975; Baars 1979; Topping & Luff 1995). For example, Luff (1975) found that large Coleoptera (beetle) individuals were not efficiently caught by pitfall traps, and that escape rates were high. Baars (1979) compared two species of carabid beetle and found that one was eight times more likely to be trapped than the other. Pitfall trap captures can vary with trap design, preservative type, and surrounding substrate (Spence & Niemela 1994; Melbourne 1999; Pekar 2002; Schmidt et 118 al. 2006) and soil disturbance can lead to more individuals of particular taxa being sampled immediately after traps are set (Greenslade 1973; Schirmel et al. 2010). Until now, the magnitude and direction of capture bias has not been studied in natural environments, and in whole communities of arthropods.

A large proportion of the world’s vertebrate fauna is insectivorous. Many birds and mammals, and most lizards and frogs eat arthropod prey. The prey base for these animals appears to be declining globally (Dirzo et al. 2014). Long term, repeatable studies of arthropod community composition and relative abundance will allow us to better detect and act on declines. However, published studies vary in their pitfall trapping methods. Variation between studies in the number of traps, configuration, preservative type and amount, and failure to report exact protocols means that comparison of relative abundance of arthropods between published studies and between past and present is problematic. Here we present a new method to assess arthropod relative abundance, activity and community composition using time-lapse camera traps. We use the Reconyx PC850 model, customised with a short focal distance (250mm) (Soininen et al. 2013), so that tiny arthropods are in sharp focus. Camera traps are now commonplace for monitoring vertebrates (Meek et al. 2014, De Bondi et al. 2010, Vine et al. 2009) but have not previously been used to collect extensive field data on litter arthropods.

The major aim of this study is to test the effectiveness of camera trapping versus pitfall trapping to sample litter arthropods, specifically:

1) To determine whether there is a difference in the number of arthropod taxa sampled in pitfall and camera traps.

2) To determine whether there is a difference in the mean body length of arthropods sampled in pitfall and camera traps.

3) To quantify the differential escape behaviour of arthropod taxa in the wild using time- lapse camera traps placed above pitfall traps.

We quantify captures using cameras programmed with four recording intervals in Australian rainforest and schlerophyll (Eucalypt) forest between 2012 and 2015.

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Methods

Sampling and measurement of arthropods

We used five sites at two locations in south-east Queensland, Australia: site one was in upland rainforest at Springbrook National Park (-28.23ºS, 153.28ºE, 900 m asl) and sites two to five were at Conondale National Park, (-26.55°S, 152.44°E, 100 – 800m asl) including lowland and upland rainforest and schlerophyll forest. We sampled at Springbrook for three weeks, in spring and summer 2012 and summer 2014. We sampled at Conondale National Park for sixteen weeks in winter and spring 2015.

At each site we buried five pitfall traps (200 ml white plastic cups with diameter of 70 mm) flush with the ground at 20m intervals and half filled them with 70% ethanol. We chose to use plastic cups because they (or similar plastic containers) are widely used for arthropod pitfall trapping (e.g. Fisher & Dickman 1993a, Fisher & Dickman 1993b, Driscoll 2005). Traps were checked at dawn every morning. Each day we stored arthropods from pitfall traps in individual specimen jars containing 70% ethanol, for identification to order, and body length measurement, in the laboratory. We positioned 17 cameras vertically (with the lens and camera facing the ground) (Meek et al. 2014, Rovero et al. 2013), 250 mm above the ground (the fixed focal distance), on frames attached to trees. Cameras photographed individual pitfall traps and the surrounding field of view (200 x 150 mm) for seven to eight consecutive days at Springbrook, and 14 consecutive days at Conondale National Park at each pitfall location. The field of view of cameras was 0.03 m 2 (30000 mm 2), around eight times as large as the area of the pitfall trap. In 2012, we programmed cameras to take a photograph once every 15 seconds, 30 seconds or 60 seconds (with three replicates for each time interval) between 4 pm and 6 am. In 2014 we programmed cameras to take three pictures on rapidfire with a fifteen minute interval between picture sets for 24 hours. In 2015, we programmed all of the cameras to take three photographs in succession on rapidfire every 15 minutes between 4pm and 6am. Thus, there were five treatments: cameras with 15 second intervals (n = 7 camera locations), cameras with 30 second intervals (n = 2 camera locations), cameras with 60 second intervals (n = 4 camera locations), cameras with 900 second intervals (n = 11 camera locations), and pitfall trap lines at cameras that were emptied every 24 hours (n = 24 locations). The total number of trap nights at all sites was 125 for the cameras and 555 for the pitfalls.

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Under each camera, we placed a clear plastic or wooden ruler on one side of the field of view, in order to measure the body length of individual arthropods in photographs. Although the cameras are waterproof, to prevent water pooling and entering the cases in torrential rain, we fashioned rain covers out of 25cm x 18cm plastic containers.

Published studies commonly report relative abundance of arthropods in broad categories of order or body size (e.g. Fisher & Dickman 1993a, Douglas et al. 2010, Siemann et al. 1999). We identified photographed and captured arthropods to the taxonomic level of order in most cases. We classified larvae (Coleopteran and Lepidopteran), Oligochaetes and Opiliones in these separate categories. We refer to all categories as ‘orders’ or ‘taxa’. Only arthropods and larvae larger than 1 mm were included in the analysis, because this was the minimum size for accurate identification to order from photographs. However, we still recorded the presence of arthropods smaller than 1mm in the datasheet if we found them in camera or pitfall trap samples. In most cases, identification to order could be made in five seconds. Sequential time-lapse photographs are nearly identical, so we could quickly discard photographs without arthropods or vertebrates. On average it took us 40 seconds to analyse one day of photos recorded using the fifteen minute time lapse interval. We classified an arthropod sighting as an ‘escape’ if successive time-lapse photographs showed the arthropod walking over the edge of a pitfall trap and then back out. A sighting was classified as an ‘avoidance’ if an arthropod walked to the rim of a pitfall trap and then changed direction, preventing it from falling in. If the same arthropod appeared in consecutive time-lapse photographs it was only recorded once.

Statistical analysis of arthropods

We used a mixed-effects model with a Poisson distribution to test if the number of taxa sampled per location per day differed between cameras and pitfalls, with daily trap identity as a random factor (in the R package MASS, Venables & Ripley 2002). To test if there was a difference in the mean body length of arthropods sampled by cameras and pitfall traps, we used linear mixed-effects models with daily trap identity as a random factor. We used a Chi-squared test to find if the proportion of escapes and avoidances of pitfall traps varied between arthropod taxa.

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Results

When the camera sampling intervals were combined, cameras recorded 37% more taxa than did pitfall traps at the same locations and times; cameras recorded a mean of 6.8 

0.56 (s.e.m) orders per day and pitfalls 4.29  0.41 (t = -4.53 15,48 , P < 0.001). In two week sampling periods, the cumulative number of taxa sampled by cameras outstripped the number sampled by pitfall traps from the first day (Fig 1). The mean number of individuals encountered per location per day, including all camera time intervals, was 14.05  2.67 (s.e.m.) for cameras and 9.67  1.76 for pitfalls. When we compared the number of orders sampled per day in the five treatments (cameras with 15 second intervals, cameras with 30 second intervals, cameras with 60 second intervals, cameras with 900 second intervals, and pitfall traps at cameras) in a mixed effects model, pitfall traps sampled around half the number of orders per day (4.3 + 0.4 orders) than cameras with 900 second intervals (7.7 + 1, t = 4.1 3,29 , P = 0.0003) and 60 second intervals (7.8 +

0.8, t = 4.2 3,29 , P = 0.0002), but not significantly fewer than the limited number of cameras with 30 (6.5 + 1.5, t = 1.7 3,29 , P = 0.10) or 15 second intervals (5 + 0.6, t = 1.3 3,29 , P = 0.21). The mean body length of arthropods sampled did not differ between cameras and pitfall traps (Fig 2, t = -1.28 25,2952 , P = 0.20).

The camera trap record of escapes and avoidances showed that a quarter of the photographed arthropods that approached pitfall traps did not fall into the fluid, and sampling by pitfall traps was taxonomically biased (Chi-squared test, χ-squared = 916, df = 4, P << 0. 0001). Ants (Hymenoptera) escaped or avoided traps 25% of the time, webspinners (Embioptera) 31%, and cockroaches (Blattodea) 46%. Spiders (Araneae) were occasionally (12% of the time) able to escape, but were never seen avoiding pitfall traps (Fig 3). Other taxa did not avoid or escape from pitfalls (Table 1).

Although the proportion of time when photographs were actually being taken each day was small (less than 2% of the day), examination of successive photographs showed that individual arthropods were typically at risk of recording or capture for periods of time that included multiple photographs. For example in the 15 minute interval samples, individual arthropods (assumed to be the same individual based on appearance and position in successive frames) stayed in the frame for a mean time of 32  13 minutes, and only 5% of arthropods appeared in only one frame. One caterpillar took four hours to traverse the frame, and a spider remained in view (apparently hunting in a ‘sit and wait’ posture) for 15.5 hours.

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Discussion

Detection of taxa

Since the 1980s researchers have sought ways to collect mid to long term, time-stamped, standardised and replicated data on relative abundance of terrestrial arthropod taxa. Our new camera method is a simple and effective way to sample relative abundance and activity of leaf litter arthropods. The cameras can provide time-stamped data, to the taxonomic level of order, over large temporal and spatial scales. Our cameras detected the presence of leaf litter arthropod orders more quickly than pitfall traps and were just as efficient at detecting the range of prey body sizes in rainforest and sclerophyll forest.

It is likely that more taxa were detected by the cameras than the pitfalls because more individuals were sampled by the cameras, increasing the chance of observing rare taxa. Cameras captured 37% more individuals than pitfalls per day, probably because the sample area is around eight times larger and cameras recorded many individuals that did not fall into the pitfall traps (26% percent of individuals photographed approaching pitfall traps avoided or escaped being trapped).

Arthropods are at risk of capture in pitfall traps 24 hours a day, but can only be photographed by time-lapse camera traps for a fraction of this time. This did not decrease the effectiveness of the cameras, as we found that arthropods remained in the field of view for more than 30 minutes on average. A time-lapse schedule set to take a photograph every 15 minutes for a week or more was as effective for detecting arthropod orders as a regime of daily pitfall trapping. There was no advantage in very short (15 or 30 second) intervals between pictures. Using a fifteen minute time-lapse interval gives a battery life of up to four months, resulting in a tractable (although large) number of photographs to analyse.

Inferences concerning population abundance and long-term sampling

Instead of using pitfall traps, arthropod densities and body size distributions are sometimes calculated using leaf litter heat extraction, suction sampling, or fenced photoeclectors, as it is assumed these techniques can census all individuals in an area (Lang 2000, Spence & Niemela 1994, Holland & Smith 1999, Zhao et al. 2013). This assumption is untrue, because large arthropods have been shown to flee more effectively when approached, and as a result, these methods sample smaller mean body sizes than pitfall traps (Spence & Niemela 1994, Lang 2000). No current method can measure absolute abundance, 123 because the number of undetected individuals is unknown, unlike in mark-recapture or distance sampling of larger fauna (Pollock et al. 1990, Buckland, Anderson & Laake 1993). Similarly, the camera method presented here cannot estimate absolute abundance. However, camera trapping does not deplete local arthropod populations over time. This means that camera traps can provide more accurate data about long-term arthropod activity in an area than lethal trapping. Schirmel et al. (2010) showed that for most arthropods, capture rate in pitfall traps decreased with longer sampling intervals, suggesting that repeated pitfall trapping depleted local populations.

Long-term sampling methods should to be able to separate samples into short time intervals, because long-term cumulative samples are inadequate for most ecological questions. Some time-sorting pitfall traps have been developed to collect daily samples remotely, but these have had limited and very specific applications. For example, Shuman, Coffelt & Weaver (1996) developed a time-stamped pitfall method for monitoring increases in grain pests in indoor silos, and a rotating apparatus programmed to sample day and night separately has received some use (Chapman & Armstrong 1997, Kliewe 1998, Buchholz 2009). These field methods have not been widely adopted by ecologists, because they are limited to small areas for short time periods, are not commercially available, require mechanical and electronic expertise to construct, and are labour intensive in comparison with pitfall traps. The camera trap time lapse sampling method overcomes these issues.

Differential escape behaviour of arthropod taxa in the wild

Our analysis of the behaviour of arthropods encountering pitfall traps is the first to show the direction of taxonomic sampling bias in a natural environment, comparing multiple orders of arthropods. Ants, cockroaches, webspinners and spiders were under-sampled by conventional pitfall trapping. The ability of different arthropod taxa to escape pitfall traps seems to be related to behaviour and style of locomotion. Beetles blundered over the edge of pitfall traps, while ants, spiders, and cockroaches were able to climb up and down the walls and sometimes avoided the preserving fluid. Cockroaches and ants have specialised tarsi enabling adhesion to smooth surfaces and long antennae which help them to detect the rim of a pitfall trap and retreat (Halsall & Wratten 1988, Arnold 1974). In one case, a spider was not at risk of capture because it remained motionless in an apparent sit-and- wait hunting posture throughout most of the sampling day. Embioptera were abundant in our camera trap samples with concurrent pitfall trapping, but it is unusual to see them on

124 the soil surface (Ross 2000). Soil disruption associated with pitfall trapping may have unnaturally increased their surface activity (Digweed 1995). Crickets observed on camera never escaped pitfall traps, because they jumped directly into the preserving fluid. Sperber et al. (2007) have shown that crickets can be over-sampled in short-term pitfall traps, because vibration from human activity causes a leaping response.

While the time lapse camera method solves the pitfall trapping bias of taxonomic differences in arthropod ability to escape and avoid traps, similarly to pitfall trapping (and all other available arthropod sampling methods) camera traps cannot accurately measure absolute abundance. The camera method quantifies arthropod availability (a combination of activity and abundance) because the likelihood of capturing an arthropod will be influenced by movement rate, behaviour and locomotion. Certain orders of arthropods are likely to remain in the frame for longer periods of time, increasing their chances of being detected.

Applicability of camera trapping

Time-lapse camera traps can be used to replace or complement pitfall trapping to sample leaf litter arthropods for many different types of ecological studies or monitoring scenarioes. For example, they can be used in studies of: 1) prey availability (e.g. Fisher & Dickman 1993a, Dickman 1988) 2) arthropod behaviour - looking at interactions between individuals (e.g. Machado & Raimundo 2001) or monitoring growth and activity 3) community ecology - for example looking at the zonation of arthropods in time and space (Jaramillo et al. 2003) or 4) environmental disturbance - such as looking at the effect of fire on arthropod populations (e.g. Collett & Neumann 1995). We are currently using camera traps to look at large scale biogeographical patterns of arthropod seasonality and availability. We propose that time lapse cameras are particularly suitable for studies of prey availability because they sample in the same way that a predator encounters prey. For example, the cameras are more likely to capture a slow moving caterpillar than a cricket, but a predator would also be more likely to encounter and capture the caterpillar.

Limitations of using camera trap sampling are that leaf litter arthropods can only accurately be identified to order, tiny arthropods cannot be identified, and physical specimens are not collected. This means that camera trapping is not suitable for studies requiring species identification, genetic samples, or focusing on very small species. Additionally, changing conditions may make arthropods more difficult to identify the longer the cameras are left in

125 the field. For example, fallen branches or soaking rainfall may make it difficult to detect arthropods.

Conclusions

Camera traps with programmable time-lapse recording and short focal distance are suitable for ecological studies and monitoring of leaf litter arthropods. Cameras can solve biases associated with pitfall trapping, including differing escape abilities of arthropod taxa and provide a standardised, long-term sampling method.

Author’s contributions

R.C. and D.F. conducted the field work. R.C. performed the lab work (arthropod identification). R.C. and D.F. did the statistical analysis and contributed equally to the manuscript.

Acknowledgements

We thank Simon Blomberg for assistance with R scripting, entomology student volunteers from the University of Queensland for help with data entry, QNPWS staff at Springbrook and Daniela Parra Faundes for fieldwork support, and Myron Zalucki for initially suggesting the idea of time lapse recording.

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Figures and tables

Table 1. Number of escapes from and avoidances of pitfall traps for each major arthropod order detected by cameras (15, 30, and 60 second intervals pooled) placed over pitfall traps.

Order Escapes and avoidances / total captures (for pitfall traps)

Blattodea 6 / 13 Hymenoptera 234 / 920 Embioptera 130 / 419 Araneae 2 / 17 Coleoptera 0 / 22 Orthoptera 0 / 14 Hemiptera 0 / 16 Chilopoda 0 / 11 Diptera 0 / 6 Amphipoda 0 / 6 Spirobolida 0 / 6 Larvae (Coleoptera and Lepidoptera pooled) 0 / 2 Thysanoptera 0 / 1 Stylommatophora 0 / 1 Phasmatodea 0 / 1 Opiliones 0 / 1

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Figure 5.The cumulative number of arthropod orders detected per day by pitfall and camera traps (15, 30, 60 second and 15 minute time intervals pooled).

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Figure 6.The distribution and mean body length of arthropods captured by pitfall and camera traps (15, 30, 60 second and 15 minute time intervals pooled).

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Figure 3.Three consecutive photographs from a camera trap, showing a cockroach escaping a pitfall trap.

Figure 4. 35mm spirobolida

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Appendix E

Figure 1. University of Queensland animal ethics approval certificate.

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