Feeding Ecology of an Invasive Predator Across an Urban Land Use Gradient

Home , Garigal National Park, Red foxes in Australia

FEEDING ECOLOGY OF AN INVASIVE PREDATOR ACROSS AN URBAN LAND USE GRADIENT

Submitted by Ben Stepkovitch BSc (Advanced Science - Zoology)

A thesis submitted in requirement for the degree of Master of Research

Hawkesbury Institute for the Environment Western Sydney University

September 2017

Supervisory panel: Dr. Justin Welbergen, Hawkesbury Institute for the Environment, Western Sydney University (Principal Supervisor)

Dr. John Martin, Royal Botanic Garden & Domain Trust, Sydney (Principal Supervisor)

Professor Christopher Dickman, School of Biological Sciences, University of Sydney (Associate Supervisor)

ACKNOWLEDGEMENTS

The work undertaken for this study would not be possible without the contributions of many people and organisations. First and foremost, I must thank my supervisors Justin Welbergen, John Martin and Chris Dickman for all their help, support and expertise over the course of this project; and for going above and beyond to help explain concepts that I was unfamiliar with prior to this project. I must acknowledge the Hawkesbury Institute for the Environment for supporting the costs involved with this study and for allowing me to attend conferences to present my research where I had valuable opportunities to network with other people in the field of vertebrate pest management and wildlife research.

I would not have been able to put the time and effort into this project without the support of my parents, who kept a constant supply of leftovers in the fridge for me for when I would return home late from the lab or training. I must also thank my partner for putting up with me over the course of this project, even when I stunk out the car with roadkill foxes. Big thanks must also go out to my

Australian team mates for understanding my commitments for this project but also pushing me to find time to train in preparation for our competition this year.

To my employers, thank you for your understanding of my commitments towards field work (in other aspects of this project) and allowing me to be flexible with my work hours when necessary.

The amount of foxes obtained for this study would not have been possible without the assistance of National Parks and Wildlife Services (NPWS) Metro

North-East and the Desert Ecology Research Group (DERG) at the University of

Sydney, for their donation of old chest freezers that enabled me to set up fox carcass drop off points across Sydney. Thanks as well to David Phalen for providing freezer space at his clinic for carcasses to be dropped off there. I must thank the staff at the DERG again for taking me under their wing during this project, not only providing me with lab space but office space as well.

Fundamentally, this research could not have been carried out if it weren’t for the numerous pest controllers, land managers and numerous others who went out of their way to provide carcasses (or at least keep them fresh for me) for this project or alerted me to the presence of dead foxes that could be collected.

Thanks to all of you, we can now shed some light on the potential impacts of foxes on native species in Sydney. Especially, I must thank Jared McNaught

(NPWS Metro North East), Alison Towerton (Greater Sydney Local Land

Services), Jason Dimmuno (Stealth Pest Control) and the team at Australian

Feral Management (AFM) for their significant contribution of carcasses and local knowledge about foxes in Sydney.

There were many people who helped me out in the lab, whether that be providing advice on different techniques or helping me to process carcasses.

Juliana Brailey, Steph Yip, Josh Phillips and Bobby Tamayo thank you so much for all your assistance over the course of this project. To Justin Welbergen, Glen

Shea, and Jan Slapeta, thank you for taking the time to identify various prey or parasite remains and allowing me to bring smelly prey remains into your offices.

Also thank you to Jessica Meade and Vanya Jha for their assistance with mapping and extracting human population density data to be used for analysis.

There were a few aspects of this project that haven’t got off the ground yet, such as camera collars for foxes, but thank you to all that helped with the initial development of a prototype (yet to be tested). To Calmsley Hill City Farm, thank you for allowing me to try out prototypes on your captive red foxes; to Hugh

McGregor, thank you for your time in explaining the ins and outs of developing a similar design to what you used on feral cats; and thank you to Cam-Do

Solutions, Ragecams and Outdoor Cameras Australia for all your advice on the technical aspects of developing camera collar.

Lastly, thank you to Heather Crawford, Malcolm Kennedy, Joe Porter, Stephen

Sarre and Anna MacDonald for your various insights into different aspects of the project.

This research has been conducted under Animal Research Authority no. A11254 issued by Western Sydney University, approved 22/3/2016.

TABLE OF CONTENTS

TABLE OF CONTENTS ...... I LIST OF TABLES ...... III LIST OF FIGURES ...... IV LIST OF APPENDICES ...... VI LIST OF ABBREVIATIONS ...... VII SUMMARY ...... VIII

CHAPTER 1: INTRODUCTION & THESIS OVERVIEW ...... 9 1.1 General Introduction ...... 9 1.2 Red fox diet across environments ...... 14 1.3 Red fox morphology and condition across environments ...... 20 1.4 Study Aims ...... 22 1.5 Study Area ...... 23 1.6 Thesis Overview ...... 27 CHAPTER 2: DIET COMPOSITION OF AN INVASIVE PREDATOR ACROSS AN URBAN TO NATURAL LAND USE GRADIENT ...... 28 2.1 Abstract ...... 28 2.2. Introduction ...... 30 2.3 Methods ...... 33 2.3.1 Study area ...... 33 2.3.2 Carcass collection, measurement and dissection ...... 33 2.3.3 Diet assessment ...... 34 2.3.4 Land use categories ...... 35 2.3.4 Statistical analysis ...... 37 2.4 Results ...... 38 2.4.1 Diet across the Greater Sydney region ...... 38 2.4.2 Diet composition across a land use gradient ...... 43 2.4.2.1 Non-urban vs. Urban superclass ...... 46 2.5 Discussion ...... 47 2.5.1 Variation in diet composition among land use categories ...... 48 2.5.2 Variation in diet composition across the land use gradient ...... 49 2.5.2.1 Exploiting anthropogenic food ...... 50 2.5.2.2 Native and introduced mammals ...... 52 2.5.3 Implications for fox management in urban areas of Australia ...... 52

2.6 Conclusion ...... 56 CHAPTER 3: MORPHOMETRICS AND BODY CONDITION OF AN INVASIVE PREDATOR ACROSS AN URBAN TO NATURAL LAND USE GRADIENT ...... 57 3.1 Abstract ...... 57 3.2 Introduction ...... 58 3.3 Methods ...... 61 3.3.1 Study area ...... 61 3.3.2 Sample collection ...... 61 3.3.3 Land use categories ...... 63 3.3.4 Comparisons with global red fox morphology ...... 63 3.3.5 Statistical analysis ...... 65 3.4 Results ...... 68 3.4.1 Effects of diet on morphology along an urban land use gradient ...... 68 3.4.1.1 Body mass ...... 68 3.4.1.2 Skeletal size ...... 69 3.4.1.3 Body condition index ...... 70 3.4.2 Morphology among and along land use categories ...... 71 3.4.3 Comparisons of morphology between global fox populations ...... 72 3.5 Discussion ...... 74 3.5.1 Morphology versus diet along an urban land use gradient ...... 74 3.5.2 Morphology along a land use gradient ...... 75 3.5.3 Comparisons of morphology between other global red fox populations ...... 77 3.5.4 Implications for red fox management in urban areas of Australia ...... 79 3.6 Conclusion ...... 80 CHAPTER 4: CONCLUSION ...... 81 4.1 Summary of main findings ...... 81 4.2 Implications for fox management in urban environments in Australia ...... 82 4.3 Suggestions for future research ...... 83 4.3.1 Diet analysis during growth ...... 83 4.3.2 Camera collars...... 83 4.3.3 Genetic studies ...... 84 4.3.4 Cats ...... 85

APPENDICES ...... 86 REFERENCES ...... 96

LIST OF TABLES

Table 2.1. Predictions for how the relative proportion stomach volume of different prey items will change in relation to the land use gradient...... 32 Table 2.2. Classification of the land use categories that each fox carcass was assigned to...... 36 Table 2.3. Prey items identified from 108 red fox stomachs collected across the Greater Sydney region...... 40 Table 3.1. List of measurements (in mm) and their abbreviations...... 63 Table 3.2. Eigenanalysis of the correlation matrix and factor loadings for the principal components extracted from the morphometric variables...... 66

III

LIST OF FIGURES

Figure 1.1. Distribution of red foxes throughout Australia (West 2008)...... 13 Figure 1.2. Greater Sydney region- a) highlighted in yellow, in relation to rest of Australia, and b) outline of Greater Sydney region...... 24 Figure 2.1. Location of all red fox carcasses (n = 130) collected in the Greater Sydney region used for diet analysis...... 34 Figure 2.2. Location and land use categories of red fox carcasses, with food present in stomach (n = 108), across the Greater Sydney region...... 36 Figure 2.3 Accumulation curve for number of different prey items identified in 108 adult red fox stomachs with logarithmic regression...... 38 Figure 2.4. Mean proportion of stomach volume of prey categories for each land use category (± se; n = 108) listed in order of descending mean stomach volume: (a) plants, (b) insects, (c) mammals, (d) birds, (e) rubbish...... 44 Figure 2.5. Mean proportion of stomach volume by season for (a) insects, and (b) birds (± se)...... 45 Figure 2.6. Mean proportion of stomach values for native, introduced and unidentified mammals for each land use category...... 45 Figure 2.7. Comparison of diet between the superclasses of Non-urbanS and UrbanS in stomach contents of red foxes (n =108) (a) mean proportion stomach volume of rubbish (± se), (b) percentage of native mammals consumed (out of all mammals of known origin consumed)...... 46 Figure 3.1. Location and land use categories of 130 red fox carcasses used for morphological analysis across the Greater Sydney region...... 62 Figure 3.2. Illustration of the morphological measurements recorded from red fox carcasses: femur (F), short foot (SF), long foot (LF), nose to tail base (NTB), body length (BL)...... 63 Figure 3.3. Regressions of length measurements against body mass (kg) for red foxes in the Greater Sydney region: (a) nose to tail base (NTB) length (mm), (b) hind foot (HF) length (mm)...... 67 Figure 3.4. Mean body mass for red foxes that have different prey categories present or absent in their stomachs (± se; n = 99): (a) mammals, (b) birds, (c) insects, d) plants, (e) rubbish...... 68 Figure 3.5. Mean skeletal size index values for red foxes that have different prey categories present or absent in their stomachs (± se; n = 100): (a) mammals, (b) birds, (c) insects, d) plants, (e) rubbish...... 69 Figure 3.6. Mean body condition index for red foxes that have different prey categories present or absent in their stomachs (± se; n = 99): (a) mammals, (b) birds, (c) insects, d) plants, (e) rubbish...... 70 Figure 3.7. Mean morphological measurements of male (M) and female (F) red foxes against land use categories (± se; n = 116): (a) mass (n: M = 72, F = 42) (b) skeletal size index (n: M = 72, F = 45), (c) body condition (n: M = 71, F = 43)...... 72

Figure 3.8. Comparison of mean morphological measurements reported for male (M) and female (F) foxes in native and introduced populations in urban and non- urban environments across the globe. (a) body mass, (b) nose to tail base length (NTB)...... 73 Figure A1. Distribution of 130 red fox carcasses in relation to human population density (1 km2)...... 86 Figure A2. Location of all carcasses (n = 130) collected in the Greater Sydney region used for diet analysis. Image created using Google Earth...... 87 Figure A3. Comparison of different cities used for urban land use gradient studies on red foxes...... 88

LIST OF APPENDICES

Appendix 2.1. Justification of land use categories ...... 86 Appendix 2.2. List of vertebrates consumed by red foxes, according to location and Local Government Area (LGA)...... 89 Appendix 3.1. Morphological measurements of different red fox populations as reported by different studies with summary of combined sample size, mean and standard deviation for each class...... 91

LIST OF ABBREVIATIONS

BL Body length

CBD Central business district

EBPC Act 1999 Environment Protection and Biodiversity Conservation Act 1999

HF Hind foot

HPD Human population density

LF Long foot

NSW New South Wales

NTB Nose to tail base

SD Standard deviation

SE Standard error

SF Short foot

VII

SUMMARY

Urbanisation poses a major threat to biodiversity, often resulting in the local decline or extinction of native species. Urban and peri-urban areas, in general, contain a mosaic of fragmented natural habitats in which native species can find refuge. While, the persistence of native species is often tenuous in such refuges, little is known about how introduced predators, such as the European red fox (Vulpes vulpes), affect native prey in urban environments in Australia.

This study aims to address this knowledge gap by assessing the diet composition and morphology of foxes along an urban land use gradient, transecting the Greater Sydney Region, Australia. Diet composition was assessed through measuring the proportion of volume of each prey category in the stomachs of fox carcasses. Morphology was assessed in respect to skeletal measurements, body mass and body condition of those carcasses.

Diet composition varied considerably along the gradient, with mammals, birds, insects, plants and anthropogenic food representing significantly different proportions of the foxes’ diet in different land use categories. Native mammals were predominantly consumed in non-urban areas, whereas introduced mammals were mainly consumed in urban areas. Nevertheless, urban foxes still consumed a considerable amount of native marsupials, mainly comprising common ringtail possums (Pseudocheirus peregrinus) and common brushtail possums (Trichosurus vulpecula). No threatened species were identified in the diet of foxes in this study. Foxes exploiting anthropogenic food were also heavier and in better condition than foxes without access to this resource supplementation.

Thus, foxes are highly opportunistic and adaptable predators of a wide variety of prey in Australian urban environments; however, further research is required to confirm the magnitude of their impacts on native species in urban refugia.

VIII

CHAPTER 1

INTRODUCTION & THESIS OVERVIEW

1.1 General Introduction Urbanisation is an important driver of local declines and extinctions of native species worldwide (McKinney 2002). Out of the seven and a half billion people on earth, over 50% inhabit urban areas, and this proportion is expected to exceed 70% by 2050 (United Nations 2012). Therefore, the rate of urban expansion is expected to increase, placing further pressure on the native flora and fauna. These pressures can be exacerbated by the presence of introduced predators that sometimes thrive in more urbanised areas (Fischer et al. 2012; Sorace 2002). However, little is known about how such predators impact on native species assemblages in urban environments (Jokimäki & Huhta 2000).

Urbanisation is a challenge for conservation biologists because the anthropogenic changes to the environment are often long term, and the loss of habitat connectivity favours a select suite of introduced or non-endemic native species (McKinney 2006). Fragmentation increases with increasing human population density, moving from surrounding rural areas toward an urban centre (McDonnell et al. 1997). Such natural-rural- urban gradients allow ecologists to study the effects of habitat fragmentation on species richness, as well as underlying differences in ecosystem processes between urban centres and low density peripheral settlements (Nilon & Pais 1997; Pickett et al. 2001).

Numerous studies assessing land use gradients for a wide range of flora and fauna, have shown that the richness of non-native species increases towards urban centres whilst that of native species decreases (Blair & Launer 1997; Mackin-Rogalska et al. 1988; Marzluff 2001; McIntyre 2000). In some areas, urbanisation can lead to a net gain in species when non-native species replace native species faster than they are lost (McKinney 2006). This can be attributed to increased primary productivity from humans through the local importation of traditionally limiting factors, such as water, fertiliser, and anthropogenic food sources (McKinney 2008). Although local species

richness may increase, global biodiversity is subsequently decreased by the extinctions of unique endemic species (McKinney 2006). Changes in species richness can also vary between taxa. For example, between 1836 and 2002 in Adelaide, Australia, the number of plant species increased by 46% across the city while the number of native mammals declined by 50% (Tait, Daniels & Hill 2005). Other apparent trends along urban land use gradients include lowered sensitivity to predation risk by prey species as inferred by these prey species consuming more food in urban habitat patches (such as lower ‘giving up densities’) (Bowers & Breland 1996; Tsurim, Abramsky & Kotler 2008) and closer proximity that potential threats can encroach before escape behaviour is employed (such as shorter ‘flight initiation distance’) (Møller 2008) in urban prey species when compared to their rural conspecifics.

Despite overall declines in the richness of native species in urban areas, some native animal species are able to adapt and persist within urban refugia. Such species may be ‘urban adapters’ (Blair 2001), that are dietary generalists, exploiting the rich and varied anthropogenic food sources, and/or that can find shelter from intensive human activity (McKinney 2002). Some vertebrates are also able to adapt to living in or on urban structures that loosely resemble habitats from their natural environment, such as cliff dwelling birds (Blair 1996; Lancaster & Rees 1979) and tree-climbing lizards (Germaine & Wakeling 2001), that are able to exploit vertical surfaces of buildings in urban areas. However, the abundance of anthropogenic food resources in cities can also support populations of predators, with varying ecological effects that can benefit the predators but consequently negatively affect other urban wildlife (Newsome et al. 2015).

Rare and threatened species can also occur in urban habitats and this presents an opportunity for their conservation. A recent study identified that Australian cities contain considerably more threatened species than non-urban areas, per unit of area (Ives et al. 2016). The creation of artificial habitats, such as ponds and wetlands for amphibians (Chovanec 1994; Garcia-Gonzalez & Garcia-Vazquez 2012), artificial rocks for reptiles (Webb & Shine 2000), or nest boxes for hollow-utilising fauna (Goldingay & Stevens 2009; Harper, McCarthy & van der Ree 2005), can assist in conserving threatened species in urban environments.

The assemblages of native species finding refuge in urban environments differ from those in natural communities (McKinney 2006), which suggests that urban native species assemblages may be shaped by mechanisms unique to urban environments, with predation proposed as playing a primary role (Shochat et al. 2006). In natural communities, top-down regulation of species through predation can limit prey population sizes below levels that would otherwise be supported from available resources (Newton 1998). However, prey species in urban areas may experience decreased predation rates that can release them from top-down regulation (Gering & Blair 1999; Shochat et al. 2006; Stracey 2011; Valcarcel & Fernández-Juricic 2009), resulting in native species finding refuge in urban areas. The high urban population densities of bird (Hough 2004; Tomiałojć & Profus 1977) and pest species (Jokimäki & Suhonen 1998; Richards 1989) have been hypothesised to result from the lower abundance of predators in urban areas (Erz 1966; Luniak & Mulsow 1988). However, not all predator taxa decrease in abundance in urban areas. For example, higher densities of raptors, omnivorous birds and mammalian predators have been observed in urban parks (Sorace 2002). This highlights the need for further research to delineate the contrasting effects of urbanisation on predator and prey species (Fischer et al. 2012).

The abundance of large carnivores tends to decrease with increasing urbanisation (Fischer et al. 2012) as large carnivores are replaced by smaller, more abundant mesopredators instead (Estes et al. 2011; Prugh et al. 2009). These mesopredators are generally able to replace large predators by becoming commensal with humans, exploiting the wide variety of anthropogenic food sources made available from human activity, such as scavenging garbage, road kill, agricultural crops and the pests associated with these crops (Newsome et al. 2015; Yom‐Tov 2003). In countries like Australia, these mesopredators are often introduced predators that replace large apex predators like the dingo (Canis dingo) and smaller native predators such as quolls (Dasyurus spp.) (Glen & Dickman 2008; Johnson & VanDerWal 2009).

Introduced mesopredators such as wild ‘domestic’ cats (Felis catus) and the red fox (Vulpes vulpes) can place greater pressure on native species than native predators because of prey naiveté (Carthey & Banks 2016; Cox & Lima 2006; Parsons et al. 2017). As such, introduced cats and red foxes have been listed as ‘Key Threatening

Processes’ under the Environment Protection and Biodiversity Conservation Act 1999 (EBPC Act, Commonwealth of Australia 2009) due to their impacts on Australian native species (DEWHA 2008). Consequently, intensive management and eradication regimes have targeted cats and red foxes with the aim of alleviating predation pressure on native species in natural habitats and neighbouring agricultural areas (Saunders, Gentle & Dickman 2010); urban areas, however, have received considerably less attention.

Red foxes have been extensively studied along urban-rural gradients in their native distribution of Europe, North America and Asia. These studies have identified various changes of fox biology along urban gradients, such as shifts in habitat use (Odell & Knight 2001; Randa & Yunger 2006), diet (Lavin et al. 2003), causes of mortality (Gosselink et al. 2007), and home range sizes (Šálek, Drahníková & Tkadlec 2015; Walton et al. 2017). In this context, however, foxes have been a naturally occurring species moving between areas of human settlement, agriculture and natural habitats, as well as the competition and/or predation from larger carnivores, such as coyotes (Canis latrans), where locally present. In such circumstances, red fox predation may still impact on other native species seeking shelter in human-altered landscapes.

What happens when native species seeking refuge in urban areas encounter introduced predators? The red fox is one such species that can be studied to investigate the impacts of introduced predators on native species in urban environments. The red fox was introduced into Australia in the mid-19th century for hunting by European settlers (Rolls 1969), and today this species occurs across the majority of Australia (Fig. 1.1), excluding the arid and tropical regions in the north of the continent (Saunders et al. 2010). However, most of the research on red foxes has focused on rural and natural areas. Few studies have assessed urban red fox ecology in Australia (Marks & Bloomfield 2006; Robinson & Marks 2001), and none has assessed their ecology across an urban-rural-natural landscape gradient.

Figure 1.1. Distribution of red foxes throughout Australia (West 2008).

While red foxes in Australia are predators of introduced species, such as the European rabbit (Oryctolagus cuniculus) (Long 1988), black rat (Rattus rattus) and house mouse (Mus musculus) (Davis et al. 2015), they also prey on native species (Saunders et al. 2010). Urban and agricultural landscapes offer refugial areas for a range of native species (Fischer et al. 2012; McKinney 2002; Møller 2012) and the importance of such areas for conservation is receiving increasing attention (Ives et al. 2016; Marzluff & Ewing 2001; McKinney 2002). Given that introduced red foxes occur in the majority of Australia’s urban areas, this project aims to address the implications of red fox predation on native species across an urban to natural land use gradient.

1.2 Red fox diet across environments The red fox has the largest distribution of all wild canids, naturally occurring from the Arctic Circle to North Africa, Eurasia and North America. It occupies a broad range of habitats across this range, including arctic tundra, deserts and even urban environments (Baker & Harris 2004). Red foxes are opportunistic generalists with no specific dietary requirements, which likely contributes to their extensive global distribution (Long 2003; Saunders et al. 1995).

1.2.1 Native habitats There has been extensive research into the diet of red foxes across their native home range, in relation to variation with climatic conditions and habitat type. The diet of red foxes in Europe ranges from small rodents (Yoneda 1982), lagomorphs (Reynolds 1979), earthworms (Macdonald 1980), and fruits and insects (Ciampalini & Lovari 1985), depending on the habitat and season. Red foxes are also known to scavenge on ungulate carcasses when available (Balestrieri, Remonti & Prigioni 2011; Cagnacci, Lovari & Meriggi 2003; Kolb & Hewson 1979; Meisner et al. 2014). Studies of red foxes in Italy, within Mediterranean coastal ecosystems, have demonstrated that their diet correlates with the seasonal abundance of food, confirming the behavioural plasticity of red foxes to exploit different food resources seasonally. In winter, juniper berries (Juniperus spp.) have been shown to be the staple resource of red fox diets along the Tuscan coast (Cavallini & Lovari 1991), whilst small mammals (rodents - Rodentia), were mostly consumed from mid-winter to early spring (Calisti et al. 1990; Ciampalini & Lovari 1985). Radio tracking by Cavallini & Lovari (1991) demonstrated that red fox activity during this period predominately occurred in pinewood habitat where those food sources were abundant. Conversely, in late spring to midsummer, red foxes spent more time foraging in meadows where beetles (Coleoptera) and crickets (Orthoptera) were seasonally abundant (as inferred from meteorological factors). In dune ecosystems, spatial and temporal modulation of red fox foraging activity has also been observed. For example, in Burano, Italy, red foxes were predominately eating invertebrates, particularly beetles, during the warmer seasons (Ricci et al. 1998). In addition to taking advantage of different zones along the dune system to hunt different invertebrates; red foxes would forage for burrowing invertebrates when they were

active above ground, or conversely exploit the invertebrates’ diurnal and nocturnal resting sites (Ricci et al. 1998).

Red foxes can vary their diet in order to exploit locally abundant and profitable resources, known as prey switching (Murdoch 1969). Across Europe, numerous examples of prey switching by red foxes in different habitats are evident. In Danish wetland ecosystems, birds (especially Anseriformes) are the predominant prey consumed by red foxes (Meisner et al. 2014), contrasting other European studies where mammals comprise most of their prey (Dell'Arte et al. 2007; Goldyn et al. 2003; Goszczyński 1974). In mountainous environments, red foxes consume more fruit than they do at lower elevations (Balestrieri et al. 2011). Red foxes have also been reported switching prey when new species have been introduced into certain areas. For example, in north-west Italy, red foxes selectively prey upon introduced eastern cottontail rabbits (Sylvilagus floridanus), for which lagomorphs are usually a secondary food resource (Balestrieri, Remonti & Prigioni 2005). In semi-arid environments, red foxes have been shown to exploit prey rich in water to compensate for a lack of water resources. On the island of Djerba, Tunisia, red foxes fed on the most abundant food items, insects and dates, which in turn were also rich in water (Dell’Arte & Leonardi 2009). Feeding on fluid rich prey, whereby predators compensate for a lack of access to drinking water, is one example of the adaptations that allow generalist predators to persist in arid environments (Dell’Arte & Leonardi 2005; Winstanley, Buttemer & Saunders 2003).

1.2.2 Red foxes in urban areas in their native range

Given the opportunistic nature of red foxes it is not surprising that they have colonised urban environments across their native distribution. Red foxes in urban environments commonly exhibit small home ranges and maintain high population densities, suggesting that urban areas provide highly favourable habitats (Baker & Harris 2004; Gloor 2002; Harris 1981a; Macdonald & Newdick 1982). Urban red foxes have greater access to anthropogenic foods (Baker et al. 2000), consequently they consume greater amounts of this resource through scavenging than their counterparts in rural or natural areas (Contesse et al. 2004; Harris 1981b). Anthropogenic food eaten by red foxes generally comes in the form of rubbish and compost, cultivated fruit and crops, or food left out for pets and wildlife by residents

(Contesse et al. 2004; Doncaster, Dickman & Macdonald 1990; Harris 1981b; Reig, Cuesta & Palacios 1985). The amount of anthropogenic food scavenged by red foxes in their native and introduced (for example, Australia) range is poorly understood, but this resource is likely to be highly important for supporting populations at their current levels in urban environments (Bateman & Fleming 2012).

A study of the diet of urban red foxes in Zurich, Switzerland (Contesse et al. 2004), found that over half of the average stomach contents from these foxes contained anthropogenic food. Red foxes closer to the city centre of Zurich also had a higher proportion of anthropogenic food in their stomachs in comparison to red foxes from the peri-urban zones. A similar study by Harris (1981b), demonstrated that red foxes closer to the city centre of London, United Kingdom, ate significantly more scavenged food, and preyed upon fewer earthworms, domestic pets, and native mammals, than red foxes around the city fringe. The diet of urban red foxes in the British cities of Oxford (Doncaster et al. 1990) and Bristol (Saunders et al. 1993) have also been studied, with the selection of prey items by red foxes roughly similar between all three cities. However, red foxes in Bristol consume more items by scavenging than the other two cities, which has been attributed to differences in available habitat (Harris & Rayner 1986) and resident’s attitudes towards feeding wildlife (Harris & Woollard 1991).

In urban areas where there is an abundance of different food sources available all year round, seasonal trends in red fox diet are less pronounced than in rural and wilderness areas (Harris 1981b). Any seasonal differences that arise are due to changes in the abundance of non-scavenged items, such as rodents and rabbits (Doncaster et al. 1990; Saunders et al. 1993). However, urban red foxes are not largely dependent on one food source, allowing them to maintain high population densities all year round (Harris & Smith 1987).

1.2.3 Red foxes in Australia

In countries where red foxes have been introduced, such as Australia, their diet has been extensively studied in natural and agricultural landscapes due to their impacts on native fauna and livestock production (Saunders et al. 2010). Profitable foraging patches have been created for red foxes in Australia through fragmentation of forested habitats for agriculture, and the introduction of familiar prey (rabbits and

sheep) (Saunders et al. 2010). Furthermore, Australian native species are evolutionarily naïve of red foxes and, lacking fox-specific adaptations, are particularly susceptible to predation (Cox & Lima 2006; Salo et al. 2007). Studies have found that in most remnant vegetation and rural ecosystems, mammals formed the main component of red fox diets, followed by invertebrates and plants (Crawford 2010; Lugton 1993; Molsher, Gifford & McIlroy 2000; Ryan & Croft 1974; Seymour, Harris & White 2004). Consequently, red foxes have been implicated in the regional decline and extinctions of a broad range of medium-sized ground dwelling mammals and ground-nesting birds (Office of Environment and Heritage NSW 2011), and consequently are considered a Key Threatening Process for small mammals in Australia (DEWHA 2008).

Across Australia there is mounting evidence that red foxes will eat the most abundant or accessible food items available in their environment. For example, in agricultural environments red foxes have been shown to mainly prey upon abundant introduced species, such as European rabbits and house mice, in addition to exploiting sheep (Ovis aries) carrion (Coman 1973; Crawford 2010; Croft & Hone 1978; Lugton 1993; McIntosh 1963a). On the other hand, in natural environments, such as national parks and bushland, red foxes predominately consume more native species (where locally present) such as common ringtail possums (Pseudocheirus peregrinus) (Meek & Triggs 1998; Triggs, Brunner & Cullen 1984), Antechinus spp. and native rodent species (such as Mastacomys fuscus and R. fuscipes) (Green & Osborne 1981; Lunney, Matthews & Triggs 2001). Reptiles generally do not form a substantial part of red fox diets in Australian ecosystems, except in arid environments (Brooker 1977; Burrows et al. 2003; Paltridge 2002; Read & Bowen 2001). Birds are a common part of red fox diets in Australia (Burrows et al. 2003; Kirkwood, Dann & Belvedere 2005; Rose, Augee & Smith 1994); however, overall, birds tend to be consumed less often than mammals and invertebrates (Crawford 2010).

Seasonal variation of red fox diets in Australia has not been as extensively studied as in the foxes’ natural range. Furthermore, few studies of red fox diets in Australia have demonstrated a seasonal variation in diet. A key limitation here has been small sample sizes (Crawford 2010) and the fact that Australia has less-pronounced seasons than environments in the northern hemisphere where red foxes naturally occur. While mammals tend to form the staple diet of red foxes throughout the year,

some studies have observed increased consumption of invertebrates in spring and summer corresponding with the time when these prey are more abundant (Green & Osborne 1981; Lugton 1993; Meek & Triggs 1998; Molsher et al. 2000; Palmer 1995; Risbey, Calver & Short 1999). It is important to note that the evidence of different prey categories in red fox diets does not accordingly correspond to the impact foxes have on those prey populations (Banks 1999). For example, predation on individuals may have no effect at a population level if these individuals are part of the ‘doomed surplus’ (Banks 1999) of individuals that are otherwise excess to the population.

While evidence of fox predation may not equate to impacts on prey populations, prey populations can still be negatively impacted by foxes even when they are not abundant in fox diets. For example, birds and reptiles generally not forming a large proportion of red fox diets, however, foxes have been implicated in the decline of marine birds in Australia including short-tailed shearwaters (Puffinus tenuirostris) (Norman 1971), little terns (Sterna albifrons) (NSW National Parks & Wildlife Service 2003), and little penguins (Eudyptula minor) (Bourne & Klomp 2003); as well as terrestrial birds including malleefowl (Leipoa ocellate) (Priddel & Wheeler 1997), bush stone-curlews (Burhinus grallarius) (Carter 2010) and ground feeding and nesting passerines (Ford et al. 2001). Likewise for reptiles, severe predation by red foxes has been recorded on marine (Heppel et al. 1996) and freshwater (Thompson 1983) turtle nests. Thus, broader approaches are required to assess impacts of red fox predation, rather than diet analysis alone.

1.2.4 Red foxes in urban Australia

Red foxes are common in urban environments across the Australian continent (Saunders et al. 2010); however, few studies have assessed the ecology, let alone the diet of foxes in urban Australia (Marks & Bloomfield 1999, 2006; Robinson & Marks 2001). Studies on the diet of urban red foxes in Australia are limited to areas of remnant vegetation surrounded by urban development (Coates & Wright 2003; Kennedy 1995; Rose et al. 1994) or semi-urban riparian areas on the suburban fringe (White et al. 2006). Here, red foxes living near urban environments consume a smaller variety of mammalian prey than foxes in non-urban areas (Mitchell & Banks 2005; White et al. 2006), with a considerable reliance on introduced rodents, rabbits,

ringtail and brushtail possums (Trichosurus vulpecula). Red foxes have been recorded consuming native species that find refuge within remnant vegetation in urban areas, such as southern brown bandicoots (Isoodon obesulus obesulus) and ringtail possums in urban greenspace (parks) and national parks on the suburban fringes of Melbourne (Coates & Wright 2003) and Sydney (Kennedy 1995; Rose et al. 1994). Red foxes have also been observed moving between remnant vegetation and surrounding urban developments (Rose et al. 1994), predominately consuming native prey in the former and introduced mammals in the latter (Kennedy 1995). Increased knowledge of urban red fox diets is required to enable further research on the implications of fox predation for native species living in urban environments.

1.3 Red fox morphology and condition across environments

Adult body size in mammals is dependent on the length of time where individuals have access to high quality food during their period of growth (Geist 1987). Consequently, the environmental conditions experienced during growth have a major bearing on the eventual body size of adult animals (Henry & Ulijaszek 1996). Similarly, the body condition of mammals has been linked to the amount and quality of food resources they have access to (Brand & Keith 1979; Lindström 1983; Schulte-Hostedde et al. 2005). Across the extensive range of the red fox, they inhabit a variety of fragmented habitats corresponding to different degrees of land use. Hence red foxes exhibit variable body size and condition in relation to the availability of local resources (Cavallini 1995).

A meta-analysis (Cavallini 1995) based on red fox morphology data from various global populations concluded that on a global scale, latitude significantly explains variation in body size, with animals becoming larger towards the poles in accordance with Bergmann’s rule (Mayr 1970). In the past two decades, since Cavallini’s (1995) meta-analysis, further research on the effect of global warming and body size in various taxa (Smith, Browning & Shepherd 1998; Yom-Tov 2001; Yom-Tov & Yom-Tov 2004) has seemingly supported Bergmann’s rule, despite Geist (1987) previous claims that the rule was invalid. Nevertheless, subsequent studies on body size in the red fox have demonstrated contradictions to Bergmann’s rule on smaller scales (Yom-Tov, Yom-Tov & Baagøe 2003; Yom-Tov et al. 2007). This reflects Cavallini’s earlier analytical findings (1995), where on smaller scales latitude did not explain variation in body size, likely due to effects of local variation in red fox population density and food supply. Further research into red fox morphology on local scales has revealed anthropogenic factors affecting fox body size. In agricultural habitats in Spain with high productivity, red foxes are larger than those from areas of lower productivity (Gortazar, Travaini & Delibes 2000). Similarly, increased access to anthropogenic food sources over the course of the 20th century has resulted in increased body size of the red fox in Spain (Yom-Tov et al. 2007) and Denmark (Yom-Tov et al. 2003) as well as other predators (Newsome et al. 2015; Yom‐Tov 2003).

Whilst urban red foxes have been extensively studied within their natural range (Baker et al. 2007; Baker & Harris 2004; Contesse et al. 2004; Gloor 2002; Harris & Rayner 1986; Harris & Trewhella 1988), there is little information regarding anthropogenic influences on morphology in urban areas where there is an abundance of anthropogenic food.

There have been few morphological studies of non-native red foxes (McIntosh 1963a; Winstanley, Buttemer & Saunders 1999) and the morphology of urban foxes in Australia has not been studied at all. Yet, if Australian red foxes differ from their counterparts in native populations, this could have important implications for the management of foxes as a pest species in Australia, due to the effects of morphology on the reproductive success and survival of wild carnivores (Boertje & Stephenson 1992; Iossa et al. 2008; Matlack & Evans 1992).

1.4 Study Aims

This thesis aims to increase our knowledge of the dietary ecology and morphology of red foxes across an urban to natural land use gradient in Sydney, Australia. The findings of this study aim to further our understanding of red foxes ecological role and interactions with native wildlife, which is critical for informing the management of both foxes and their native prey. In accordance with this objective, the specific study aims are to:

1. Assess how red fox diet composition changes across an urban to natural land use gradient. 2. Assess how red fox morphology and body condition changes across an urban to natural land use gradient. 3. Examine whether diet composition along the urban to natural land use gradient is related to red fox morphology and body condition.

1.5 Study Area

1.5.1 Description of study area

This study was carried out in the Greater Sydney region, located on the east coast of New South Wales (NSW), Australia (32.4 to 35.7°S, 148.8 to 152.4°E) and covers an area of about 12,400 km2 (Fig. 1.2). The lower-lying areas of this region have a temperate climate with mild winters and warm summers, whereas the elevated regions to the west (Blue Mountains National Park) experience cool winters and mild to warm summers (Mitchell & Banks 2005; Stennett & Beggs 2004).

The Greater Sydney region encompasses the city of Sydney, Australia’s oldest and largest city (Spearritt 2000), as well as three large national parks to the north, south and west. The Greater Sydney region currently supports over five million people, which represents a fifth of Australia’s human population. The population within urban areas of Sydney is currently 4.6 million people and is rapidly increasing (Australian Bureau of Statistics 2016). Sydney’s central business district (CBD) is located on the southern edge of Sydney harbour, in the east of the region. The alluvial plains, where the majority of human settlement occurs, are dominated by shale, whereas the national parks surrounding Sydney are dominated by sandstone (Benson, Howell & McDougall 1996; Walker 1960). There is a wide variety of remnant vegetation in the region, including dry sclerophyll forests and woodlands, heath, moist forests and swamps (Mitchell & Banks 2005). The western suburbs of Sydney are largely built over the Cumberland Plain Woodland, now a Critically Endangered Ecological Community (EPBC Act, Commonwealth of Australia 2009) as only 92-94% of its historical distribution remains (Tozer, Leishman & Auld 2015).

Figure 1.2. Greater Sydney region- a) highlighted in yellow, in relation to rest of Australia, and b) outline of Greater Sydney region. Image created using ArcMap 10.4.1.

1.5.2 Impact and management of red foxes within the Greater Sydney region

The red fox is thought to be common across the Greater Sydney region, including Sydney’s urban areas (Department of Environment and Climate Change 2007). It is listed as a Key Threatening Process to six native species that occur within the Greater Sydney Region (DEWHA 2008), including two mammals, spotted tail quoll (Dasyurus maculatus maculatus), southern brown bandicoot (I. o. obesulus); one bird, eastern bristlebird (Dasyornis brachypterus); one reptile, broad headed snake (Hoplocephalus bungaroides); and two amphibians, giant burrowing frog (Heleioporus australiacus), green and golden bell frog (Litoria aurea).

Predation by red foxes has also been recorded for other threatened species that occur in the Greater Sydney region, such as the long nosed bandicoot (Perameles nasuta), little tern (Sterna albifrons), pied oystercatcher (Haematopus longirostris) and little penguin (Eudyptula minor) (Department of Environment and Climate Change 2007; Office of Environment and Heritage NSW 2011). In the last 30 years, red fox predation has been attributed to the local extinction of many ground nesting birds and

medium sized mammals from the Woronora Plateau in the south and Cumberland Plain in Western Sydney (Department of Environment and Climate Change 2007). These locally extinct species include the bush stone-curlew, ground parrot (Pezoporus wallicus), eastern bristlebird, parma wallaby (Macropus parma), red- necked pademelon (Thylogale thetis), long nosed potoroo (Potorus tridactylus) and southern brown bandicoot.

Due to the impact of red fox predation on threatened species, three sites within the Greater Sydney region, where isolated populations of threatened species occur have been listed as priority treatment sites by the Office of Environment and Heritage NSW (2011). These include Garigal National Park (southern brown bandicoot) and North Head (long nosed bandicoot and little penguin) to the north of Sydney Harbour, and Towra Point (little tern and pied oystercatcher) to the south of Botany Bay. Individual foxes have been reported killing multiple individuals in some of these isolated populations (Banks 2004; Van Dooren 2011), thus management in these areas is paramount to ensuring the survival of these threatened species despite Sydney’s urban sprawl.

Red fox predation has also been recorded on many other native species within the Greater Sydney region, including some that find refuge within urban environments such as the common brushtail possum and common ringtail possum (Augee, Smith & Rose 1996; Kennedy 1995; Rose et al. 1994). In remnant bushland on the fragmented Cumberland Plain Woodland in Sydney’s west, red foxes have been recorded consuming mostly rabbits but also a moderate combined frequency occurrence of native mammal species (Adderton 1998). In national parks comprising the west of the Greater Sydney region, foxes have been recorded consuming a wide variety of mammalian prey such as small dasyurids, native rodents, gliders, possums, macropods and rabbits (Mitchell & Banks 2005).

Red fox management across the Greater Sydney region is not uniform. In urban areas fox management is largely limited to trapping and shooting, as poison baiting is not practicable in most urban areas (Marks et al. 1996), with the exception of some peri- urban national parks and nature reserves (Brown & Bernhard 2010), due to the risks to pets. Not all national parks in the region carry out intensive fox management unless there are locally endangered fauna present (M. Hall, personal

communication), for example, the isolated little penguin colony and long nosed bandicoot population at North Head, Sydney Harbour National Park (Banks 2004; Bourne & Klomp 2003). In Sydney, foxes are managed most intensively within the northern beaches region as this contains the greatest proportion of national parks (Ku-ring-gai Chase, Garigal and Sydney Harbour National Parks) and a disproportionate amount of threatened native species; including the southern brown and long nosed bandicoots, and little penguin. Management elsewhere in Sydney is generally carried out on an ad-hoc basis, mainly by contracted pest controllers at work sites, golf courses and parks where foxes are regularly sited. Local councils also carry out fox management but it is not uniformly applied across the Greater Sydney region due to the small proportion of area where foxes are thought to be exerting pressure on threatened species.

1.6 Thesis Overview

This thesis consists of the current introductory chapter (Chapter 1), two data chapters, and one concluding chapter.

In Chapter 2, I present results on the diet analysis of red foxes across the Greater Sydney region, to determine if diet composition varies across an urban land use gradient. The data and results presented in this chapter address a key knowledge gap of urban fox diets in Australia and provide locally-relevant information for the Greater Sydney region where foxes are thought to have an impact on native species.

In Chapter 3, I report how the morphology of red foxes’ changes in relation to diet across the Greater Sydney Region. Having identified that foxes in urban areas are larger than their non-urban counterparts, I quantify the effects of the presence of different prey types, especially anthropogenic food sources, to determine whether that is contributing towards increased body size in urban environments.

In Chapter 4, I present a summary of the results and place my research in the broader context of invasive species management in urban environments in Australia. Here I also consider directions for future research.

Chapters 2 and 3 have been prepared as standalone papers for submission to peer- reviewed journals – this means that there will inevitably be some overlap, especially with Chapter 1 (introduction) and between the methods sections.

All references in this thesis have been formatted according to the guidelines of the journal Animal Behaviour.

CHAPTER 2

DIET COMPOSITION OF AN INVASIVE PREDATOR ACROSS AN URBAN TO NATURAL LAND USE GRADIENT

2.1 Abstract The red fox (Vulpes vulpes) is the most widely distributed wild canid species, occupying a vast range of different environments, including urban areas, which has been attributed in part to their high dietary plasticity, with their adaptive behaviour also a key factor. In Australia, where red foxes were introduced in the 19th century, their impact on native species and livestock in natural and agricultural areas has been well documented. However, little is known about how red foxes impact native species in Australia’s urban environments. This study aims to address this knowledge gap by assessing the diet composition of foxes along an urban land use gradient, transecting the Greater Sydney Region, New South Wales. The stomach contents of 130 red foxes collected across the study region were analysed, of which 108 contained measurable quantities of food, and the proportional stomach volume of different prey categories was recorded. The findings indicate that the diet of red foxes is highly variable across land use categories. As expected, the proportion of native mammals consumed decreased towards urban areas along the land use gradient, whilst the proportion of introduced mammals and anthropogenic food sources increased towards urban areas. The wide range of prey items consumed confirms that red foxes maintain a high degree of dietary plasticity across an urban to natural land use gradient. In urban areas, red foxes consumed a considerable proportion of native species, mainly comprising common ringtail possums (Pseudocheirus peregrinus) and common brushtail possums (Trichosurus vulpecula), that are known urban adapters. Interestingly, no threatened species were recorded in the stomach contents of red foxes in this study. Hence, while red foxes prey on native species in urban Australia, this study found that their diet predominantly comprised of plants and introduced mammals. The findings from this study expand our

understanding of the ecological role red foxes perform in urban areas compared with agricultural and natural areas.

2.2. Introduction The red fox (Vulpes vulpes) is the most widely distributed extant wild canid species. It is naturally found across the Northern Hemisphere, from the Arctic Circle to North Africa, Eurasia and North America, where it occupies a broad range of habitats, including arctic tundra, deserts and even urban environments (Baker & Harris 2004). The extensive global distribution of the red fox, including colonising urban areas (Contesse et al. 2004; Harris 1981b), has been attributed to the dietary and behavioural plasticity of this species (Long 2003; Saunders et al. 1995). Across the native range of the red fox, the main trend across all diet studies is the extreme variability of food items consumed (Calisti et al. 1990; Goldyn et al. 2003; Goszczyński 1974; Kidawa & Kowalczyk 2011; Lloyd 1980; Meisner et al. 2014). In natural habitats in Europe, small mammals such as voles and rabbits form the staple part of red fox diets (Reynolds 1979; Yoneda 1982). However, when seasonally abundant, red foxes also consume high proportions of invertebrates and fruits (Cavallini & Lovari 1991; Ricci et al. 1998). Behavioural adaptations, such as selectively feeding on fluid rich food items (insects and dates), to compensate for a shortage of drinking water has allowed red foxes to colonise the semi-arid environments of North Africa (Dell’Arte & Leonardi 2005, 2009). Thus, red foxes adaptability allows this species to inhabit a wide range of environments.

Behavioural adaptations have allowed red foxes to colonise urban areas in their native home range, including the cities of London and Bristol in the United Kingdom (Baker & Harris 2004; Harris 1981b), Zurich in mainland Europe (Gloor 2002) and Toronto in North America (Adkins & Stott 1998). Urban red foxes are able to exploit the abundance of food resources made available by humans, such as rubbish, cultivated plants, domestic pets and livestock, and food left out for pets and wildlife (Contesse et al. 2004; Doncaster et al. 1990; Harris 1981b), and seem to tolerate the presence of high human activity (Gloor 2002). The proportion of anthropogenic food in the diet of red foxes has been shown to increase with their proximity to city centres (Contesse et al. 2004; Harris 1981b), and can account for over 50% of the total food ingested by foxes in some urban areas (Contesse et al. 2004).

The phenotypic plasticity of red foxes has also enabled them to exploit a wide range of environments in areas where they have been introduced, particularly in Australia

(Dickman 1996; Saunders et al. 1995). The diet of red foxes in natural and agricultural areas of Australia, and their impact on native species and livestock have been well documented (reviewed by Saunders et al. 2010). Australian native species are particularly susceptible to red fox predation due naïveté, as a result of evolving in isolation from this predator (Cox & Lima 2006). However, red foxes have been shown to consume the most abundant or accessible food items, rather than preferentially exploiting native species where present. For example, in Australian agricultural areas red foxes main prey commonly includes rabbits (Oryctolagus cuniculus) and house mice (Mus musculus); two species from their native home range that have also been introduced to Australia (Coman 1973; Crawford 2010; Croft & Hone 1978; Lugton 1993; McIntosh 1963a). Whereas in areas dominated by natural Australian vegetation, such as national parks, native mammals are the dominant prey category identified in their diet (Green & Osborne 1981; Lunney et al. 2001; Meek & Triggs 1998; Triggs et al. 1984).

Red foxes are thought to be common in urban environments across most of Australia (Saunders et al. 2010), however few studies have assessed fox ecology, including their diet, in urban areas (Coates & Wright 2003; White et al. 2006). Hence, whether red foxes impact on native species in urban refugia is largely unknown. Increased knowledge of the diet composition of urban red foxes could reveal important information for the conservation of native species living in urban environments (Fischer et al. 2012; McKinney 2002). For example, whether red foxes are consuming threatened species found in urban Australian environments (Ives et al. 2016) and/or predating upon native species that have adapted to urban areas.

This study aims to assess red fox diets across an urban to natural land use gradient in the Greater Sydney region, Australia. Specifically, I expected that native mammals will occur in red fox diets at higher proportions away from urban centres (Table 2.1), as a global pattern of declining native species richness from natural to urban areas has been identified (Blair & Launer 1997; Mackin-Rogalska et al. 1988; Marzluff 2001; McIntyre 2000). Conversely, I predicted that non-native mammals would occur in red fox diets in higher proportions towards urban centres (Table 2.1), as their relative richness increases in this direction. I expected that birds would occur in higher proportions of red fox diets towards urban centres, which support higher

densities and abundances of birds (Garden et al. 2006; McKinney 2002; Sorace 2002). I predicted that reptiles and plants would also represent larger proportions of the red foxes’ diet in natural areas due to their increased abundance (Table 2.1). I predicted that invertebrates would occur in red fox diets in higher proportions in urban centres (Table 2.1) as a compensatory mechanism due to lower species richness of vertebrate prey in urban habitats. Lastly, I expected that food scraps and garbage would increase in red fox diets towards urban areas due to their greater availability (Table 2.1).

Table 2.1. Predictions for how the relative proportion stomach volume of different prey items will change in relation to the land use gradient, as the Natural and Urban land use categories are located at opposite ends of the gradient. Natural: zero human population density, such as national park or natural bushland outside areas of urban development. Urban: human population density greater than 3000 people per km2, including golf courses and parks located within areas of urban development. + indicates a higher mean proportion stomach volume at that end of the gradient than the opposite end and vice-versa for –. *Excludes anthropogenic sources of plant based material, for example, crops, animal feed.

Natural Prey item Urban

+ Native mammals -

- Introduced mammals +

- Birds +

+ Reptiles -

- Invertebrates +

+ Plants* -

- Food scraps and + garbage

2.3 Methods

2.3.1 Study area

This study was carried out in the Greater Sydney region, located on the east of New South Wales (NSW), Australia (32.4−35.7°S, 148.8−152.4°E). The region includes Australia’s largest city, Sydney, which currently supports 4.6 million people, and is rapidly increasing (Australian Bureau of Statistics 2016). The alluvial plains, where the majority of human settlement occurs, is dominated by shale, whereas the national parks surrounding Sydney are dominated by sandstone (Benson et al. 1996; Walker 1960) and contain most of the remnant vegetation in the region (Mitchell & Banks 2005). Sydney has a temperate climate with mild winters and warm summers, whereas the elevated regions to the west of the area (Blue Mountains National Park) experience cool winters and mild to warm summers (Mitchell & Banks 2005; Stennett & Beggs 2004).

2.3.2 Carcass collection, measurement and dissection

Red fox carcasses (n = 130) were collected across the Greater Sydney region, from late 2015 to 2017 (Fig 2.1). They were provided from routine pest management conducted by land managers; in addition, a small number of these carcasses (n = 11) were opportunistically collected due to road kill. The latitudinal and longitudinal coordinates of each carcass were recorded. Each carcass was frozen for storage and subsequently thawed for 2-3 days before dissection.

Red foxes were sexed and weighed using an electronic hook scale for body mass. The age of each red fox was estimated by assessing the tooth wear of the upper and lower incisors (Harris 1978). Carcasses were cut open from sternum to groin; the stomach was removed and placed in a jar of 70% ethanol. Only the stomachs of sub- adult and adult red foxes (aged greater than six months old) were included in the subsequent analysis of diet due to an inadequate sample size of cubs (n = 2) to otherwise allow for a comparison of juvenile and adult diets.

Figure 2.1. Location of all red fox carcasses (n = 130) collected in the Greater Sydney region used for diet analysis. Image created using Google Earth.

2.3.3 Diet assessment

The stomach contents were washed through a sieve and spread out onto a white enamel tray which had a 5 × 4 grid of 5 cm × 5 cm squares drawn onto the base. Stomach contents were visually assessed and separated into categories based on their morphological characteristics, for example, mammal, reptile, bird, invertebrate, plant and rubbish (Brunner, Lloyd & Coman 1975; Croft & Hone 1978; Yip et al. 2014). The cross sections of all hairs were examined following Brunner and Coman (1974) to identify the mammal species. Mammals that could be identified to a species level were either classified as ‘native’ or ‘introduced’ mammals, based or whether or not the species occurred naturally in Australia. Where possible, avian and reptile remains and gastro-intestinal parasites were identified to species or genus level based on their morphology with the assistance of relevant experts: (reptiles: Dr. Glenn Shea, Faculty of Veterinary Science, University of Sydney; birds: Dr. Justin Welbergen, Hawkesbury Institute of the Environment, Western Sydney University; parasites: Dr. Jan Slapeta, Faculty of Science, University of Sydney). Invertebrates were identified to order level based on morphological characteristics.

Prey items were scored as present and the volumetric contribution to each stomach was assessed by eye using the 5 x 4 square grid and expressed as a percentage. The number of each individual prey items in each stomach was recorded based on the 34

number of legs, carapaces or size of hair clumps (in relation to the size of the mammal identified). The frequency of occurrence of different prey items was calculated by dividing the number of samples containing a specific prey item by the total number of stomachs analysed, and presenting this as a percentage. The mean percentage volume of each prey item identified from the total sample of stomachs analysed was calculated by dividing the total sum of the percentage volume for each prey item by the total number of stomachs analysed.

Several measures of diet analysis are commonly used to overcome the biases that can occur if only one measure is used (Hart, Calver & Dickman 2002; Klare, Kamler & Macdonald 2011), such as the index of relative importance (Pinkas 1971) . However, in this study only volumetric percentage was suitable for statistical analysis of diet composition along the land use gradient, as other composite measures are limited to visual comparisons.

The presence, number and volume of gastrointestinal parasites, parts of traps (ingested before euthanasia; used as part of ongoing fox management), grooming hairs and whiskers were noted but not included in the respective prey categories.

2.3.4 Land use categories

The human population density (HPD) (Australian Bureau of Statistics 2011) within 1 km2 (Ives et al. 2016) around each foxes’ GPS coordinates were extracted using RStudio (version 0.99.903; RStudio Inc.; Boston, Massachusetts). The coordinates of red fox carcasses were classified into categories based on the land use surrounding the 1 km2 where the carcass was collected, whilst incorporating the extracted human population density values. Reported home ranges for red foxes in different Australian environments were also taken into account when considering the land use surrounding each foxes’ location (Carter, Luck & McDonald 2012; Coman, Robinson & Beaumont 1991; Marks & Bloomfield 2006; Meek & Saunders 2000; White et al. 2006). Thus, five ordinal categories were created to construct a land use gradient for the Greater Sydney region: Natural, Agricultural, Peri-urban, Suburban, Urban (listed in order of increasing ‘urbanisation’; Table 2.2).

To enable a comparison of diet in urban and non-urban areas, the land use categories were combined to create the superclasses of ‘Non-urban’ (Natural and Agricultural)

and ‘Urban’ (Peri-urban, Suburban and Urban). Hereafter referred to in text as non- urbanS and urbanS, where superscript ‘S’ denotes superclass as opposed to the five land use categories.

Figure 2.2. Location and land use categories of red fox carcasses, with food present in stomach (n = 108), across the Greater Sydney region. Land use categories- Natural (green), Agricultural (yellow), Peri-urban (blue), Suburban (orange) and Urban (red). Image: Google Earth.

Table 2.2. Classification of the land use categories that each fox carcass was assigned to. HPD = extracted human population density values.

Land use category Classification HPD = 0 AND located within National Park and/or natural bushland (greater Natural than 1 km from human development).

Agricultural HPD < 500 AND located within area of agricultural acreages.

HPD < 500 AND located in area of remnant bushland or woodland bordering Peri-urban human development; includes landfill.

HPD = 500 – 3000; OR if located in park, golf course etc. located within Suburban suburban area (if HPD < 500). Considered within “suburban area” if nearby foxes returned HPD values between 500 and 3000 from 2011 Census data.

HPD > 3000; OR if located in park or golf course located within high density Urban urban area (if HPD < 500). Considered within “urban area” if nearby foxes returned HPD values greater than 3000 from 2011 Census data.

2.3.4 Statistical analysis

All statistics were computed in Minitab for Windows (version 16.0; Minitab Inc., State College, Pennsylvannia). All tests were two-tailed, and significance was set at α = 0.05. Means are expressed ± standard error (se).

The relationship between land use categories and mean percentage volume of each prey category was tested using a general linear model (GLM). The effects of season and sex were controlled in the model. To test for variation among the land use gradient, the land use categories were not included as covariates. To test for linear variation along the land use gradient, the land use categories were included as covariates. Unless otherwise stated, reported significance values are from models investigating the effect of land use categories alone, in which case season was previously found to be not significant.

To compare the difference in consumption of native versus introduced mammals in urbanS and non-urbanS superclasses, the percentage of native mammals consumed out of all mammals consumed was calculated. The percentage of native mammals for each superclass was calculated as:

푀푒푎푛 푝푟표푝표푟푡푖표푛 표푓 푛푎푡푖푣푒 푚푎푚푚푎푙푠 Native % = x 100 푀푒푎푛 푝푟표푝표푟푡푖표푛 표푓 푎푙푙 푚푎푚푚푎푙푠 푐표푛푠푢푚푒푑

The difference between the percentage of native mammals and the superclass land use categories was tested using a two-tailed t-test.

2.4 Results

2.4.1 Diet across the Greater Sydney region

Of the 130 red fox carcasses assessed, 14 were missing stomachs due to vehicle collision or being eviscerated, six were empty and two were from cubs; these were not included in the following analyses. Out of the 108 stomachs analysed, 62 different prey items were identified (Fig. 2.3) across 10 prey categories (Table 2.3).

Culmulative number of different prey items 0 0 20 40 60 80 100 120 Number of stomachs analysed

Figure 2.3 Accumulation curve for number of different prey items identified in 108 adult red fox stomachs with logarithmic regression (solid line).

Plant material accounted for the greatest proportion of stomach content across all 108 stomachs (29.6% ± 3.0%) and was the most frequently consumed item, occurring in 92% of stomachs (n = 108). Grasses and woody material, such as bark, twigs and sticks, were the most common plant remains found in the stomachs. Seeds, nuts and fruit made up a small portion of the stomach contents, by frequency. Insects (22.3% ± 3.1%) and mammals (18.6% ± 3.1%), on average, were consumed in similar proportions across the study area; however, insects were found in 50% of stomachs, while mammal remains were only found in 37% of stomachs. Common ringtail

possums, (P. peregrinus), house mice (M. musculus) and black rats (R. rattus) were the most frequently consumed mammals, as well as the most common vertebrates. Orthoptera and Coleoptera were the most frequently consumed invertebrates. Birds (28.7%) and rubbish (29.6%) were found in similar frequencies across all stomachs and were consumed in similar proportions of volume (birds: 11.0% ± 2.4%; rubbish: 8.0% ± 1.9%). Non-insect arthropods (9.3%) were found more frequently than reptiles (1.9%), however, both categories accounted for very little of the mean stomach volume (non-insect arthropods: 0.2% ± 0.1%; reptiles: 0.8% ± 0.8%); as such, these two categories were excluded from further analyses. The remains of one fish were found but it was unable to be determined whether it originated from a freshwater or anthropogenic source; no amphibians were identified. Lastly, unidentifiable vertebrates accounted for 5.9% ± 1.5% of stomach contents and occurred in 18.5% of stomachs (Table 2.3).

Table 2.3. Prey items identified from 108 red fox stomachs collected across the Greater Sydney region.

Prey Item No. of No. of Frequency of Volume stomachs individual occurrence (%) containing prey items (%) prey item

Unidentified vertebrate 20 10 18.5 5.9 Mammal 40 42 37.0 18.6 Unidentified 7 7 6.5 2.0

Introduced 20 20 18.5 7.8 Rattus rattus 7 7 6.5 3.5

Rattus norvegicus 1 1 0.9 0.1

Mus musculus 8 8 7.4 2.1

Oryctolagus cuniculus 3 3 2.8 1.4 Lepus europaeus 1 1 0.9 0.9 Native 14 15 13.0 8.5 Trichosurus vulpecula 2 2 1.9 0.9

Pseupredocheirus peregrinus 9 9 8.3 5.1

Wallabia bicolor 2 2 1.9 1.6 Rattus fuscipes 2 2 1.9 0.9 Bird 31 31 28.7 11.0

Unidentified 23 23 21.3 6.9

Introduced 2 2 1.9 0.8 Gallus gallus domesticus 1 1 0.9 0.5

Pycnonotus jocosus 1 1 0.9 0.3

Native 6 6 5.6 3.3 Gallinula tenebrosa 2 2 1.9 1.1

Anas superciliosa 1 1 0.9 0.5

Acanthiza pusilla 1 1 0.9 0.1

Grallina cyanoleuca 1 1 0.9 0.8

Coturnix ypsilophora 1 1 0.9

Reptile 2 3 1.9 0.8 Chelodonia longicollis (adult) 1 1 0.9 0.8

Chelodonia longicollis (egg) 1 2 0.9 0.1

Fish 1 1 0.9 0.1

Unidentified 1 1 0.9 0.1

Table 2.3. Continued…

Prey Item No. of No. of Frequency of Volume stomachs individual occurrence (%) containing prey items (%) prey item

Invertebrates 54 1440 59.3 22.3

Insects 54 1428 50.0 22.0 Unidentified 14 14 13.0 2.6

Coleoptera (adult) 26 140 24.1 1.3

Coleoptera (larvae) 9 137 8.3 1.0

Orthoptera 46 840 42.6 14.0

Lepidoptera (larvae) 11 203 10.2 0.7 Odonata 10 12 9.3 1.0 Hymenoptera 3 24 2.8 0.04

Dermaptera 2 4 1.9 0.03

Blattodea 2 21 1.9 0.3

Hemiptera 2 28 1.9 1.0

Unidentfied pupae 1 5 0.9 0.01

Other invertebrates 10 12 9.3 0.2 Unidentified 2 3 1.9 0.0

Chilopoda 5 5 4.6 0.1

Arachnida 3 3 2.8 0.04

Decopoda 1 1 0.9 0.1

Plants 103 395 95.4 29.6 Grasses 86 86 79.6 11.4

Woody material (sticks, bark) 58 58 53.7 8.4

Casurina needles 3 3 2.8 0.1

Other leaves 27 27 25.0 1.4

Seeds and grains 27 215 25.0 1.7

Unidentified flowers 4 8 3.7 0.6

Nut/husk 5 5 4.6 0.5

Fig 6 6 5.6 1.4

Other fruit 12 14 11.1 1.8

Other vegetative matter 4 4 3.7 2.2

Table 2.3 Continued…

Prey Item No. of No. of Frequency of Volume stomachs individual occurrence (%) containing prey items* (%) prey item

Rubbish 32 58 29.6 8.0 Sultanas 1 12 0.9 0.1

Corn 2 2 1.9 0.1

Olive 1 1 0.9 0.04

Unidentified fruit and 12 12 11.1 1.6 vegetable Packaging, plastic or foil 13 13 12.0 2.3

Egg shells 3 3 2.8 0.05

Other food scraps 10 10 9.3 3.7

Fishing lure 1 1 0.9 0.05

Rubber 1 1 0.9 0.04 Knot of human hair 1 1 0.9 0.02 Other rubbish 2 2 1.9 0.1

Other 19 25 17.6 3.9 Animal scat 1 1 0.9 0.04

Rocks and gravel 4 10 3.7 0.3

Other (inorganic) 2 2 1.9 0.1

Unidentifiable matter (organic) 12 12 11.1 3.4

2.4.2 Diet composition across a land use gradient

Red foxes in natural, peri-urban and urban land use categories primarily consumed mammals and plants, whereas foxes in agricultural areas predominately consumed insects (Fig. 2.4). In the suburban land use category red foxes chiefly consumed plants, insects and birds (Fig. 2.4). Red foxes within the suburban and urban land use categories consumed relatively consistent amounts of all prey categories compared to foxes from other land use categories (Fig. 2.4).

There was a significant difference in the proportion of plant material in stomach contents between the land use categories (F3,104 = 7.21, p < 0.001), with consumption lowest in agricultural areas and highest in natural areas. The decrease in consumption across the gradient was significant (F1,106 = 9.61, p = 0.002) (Fig. 2.4a).

The proportion of insects in the diet of red foxes was highest in agricultural areas and was comparable in urban areas, with few insects consumed in natural areas (Fig. 2.4b). The variation in the proportion of insects consumed among the land use categories was significant (F3,91 = 8.71, p < 0.001), as was the effect of season

(F3,91 = 5.88, p = 0.001). The consumption of insects was highest in summer, lowest in winter with moderate consumption in spring and autumn (Fig. 2.5a). However, the proportion of stomach contents that contained insects did not increase (or decrease) significantly along the gradient (F1,106 = 1.04, p = 0.310; Fig. 2.4b).

There was significant variation between individual red foxes proportion of total stomach contents that was identified as mammalian (F4,103 = 2.63, p = 0.038); however, this proportion did not change (increase or decrease) from the natural to the urban land use categories (F1,106 = 0.18, p = 0.674) (Fig. 2.4c). There was significant variation in the consumption of both native (F4,103 = 2.51, p = 0.047) and introduced mammals (F4,103 = 2.72, p = 0.033) among the land use categories, with the proportion of introduced mammals increasing in frequency (F1,106 = 5.64, p = 0.019) towards high human density areas. The proportion of stomach content that were native mammals decreased towards urban areas, however, this was not significant

(F1,106 = 2.17, p = 0.143) (Fig. 2.6).

The average proportion of birds in the diet of red foxes varied among the land use categories, peaking in suburban areas (F4,91 = 3.01, p = 0.022; Fig. 2.4d). Seasonally,

birds were identified in stomach contents at the lowest frequency in summer, increasing throughout the year and peaking in spring (F3,91 = 2.82, p = 0.043; Fig. 2.5b). There was no linear effect of the consumption of birds across the land use categories (F1,106 = 3.08, p = 0.082; Fig. 2.4d).

The proportion of anthropogenic food consumed was higher in suburban and urban areas than the other land use categories (F1,106 = 6.02, p = 0.016; Fig. 2.4e). The variation in the proportion of anthropogenic food in stomach contents among land use categories was not significant (F3,104 = 1.76, p > 0.05; Fig. 2.4e).

(a) (b) 90 90

) 80 80

(

e 70 70

m u

l 60 60

o v

50 50

h c

a 40 40

o t

s 30 30

a 20 20

e M 10 10

0 0 Natural Agricultural Peri-urban Suburban Urban Natural Agricultural Peri-urban Suburban Urban

90 90

) 80 80

% (

70 70

e m

u 60 60

l o

v 50

h c

a 40 40 m

o 30 30

n 20 20

a e

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0 0 Natural Agricultural Peri-urban Suburban Urban Natural Agricultural Peri-urban Suburban Urban Land use category

(e) 90

) 80

% (

70 e

m 60

l o

v 50

c 40 a

m 30

t s

n a

e 10 M 0 Natural Agricultural Peri-urban Suburban Urban Land use category

Figure 2.4. Mean proportion of stomach volume of prey categories for each land use category (± se; n = 108) listed in order of descending mean stomach volume: (a) plants, (b) insects, (c) mammals, (d) birds, (e) rubbish.

) (a)

) (b)

(

70 ( 70

m u

l 60 60

h 50 50

a a

m 40 40

n 30 30

r t

20 r

o 20

r o

10 r 10

n a

0 a

e 0 e

M Spring Summer Autumn Winter Spring Summer Autumn Winter Season M Season

Figure 2.5. Mean proportion of stomach volume by season for (a) insects, and (b) birds (± se); N = 108 (Spring = 14, Summer = 14, Autumn = 36, Winter = 35, unknown season = 9).

)

% (

c 20

n a

e 10 M

0 I N U I N U I N U I N U I N U Natural Agricultural Peri-urban Suburban Urban Land use category

Figure 2.6. Mean proportion of stomach values for native, introduced and unidentified mammals for each land use category (± se; n = 108). N = native, I = introduced, U = unknown.

2.4.2.1 Non-urban vs. Urban superclass There was also an increase in rubbish consumption in suburban and urban areas after low consumption in the natural, agricultural and peri-urban areas, however this was not found to be significant. To further explore the emerging relationship between the differences in consumption of rubbish along the gradient, a special case was considered to analyse these differences using the land use superclasses urbanS and non-urbanS. Foxes from the urbanS areas consumed significantly more rubbish than S foxes from non-urban areas (T86 = -3.62, p < 0.001, Fig. 2.7a). A significantly higher proportion stomach content of native mammals, out of all mammals consumed, were ingested by red foxes in non-urbanS areas compared to urbanS areas

(t46 = 5.35, p < 0.001, Fig. 2.7b).

(a) (b) )

% 14 100

(

m 12 u

l 80

o v

c a

% 60

m 8

n 6

i t

r 4

o p

o 20

r 2

n a

e 0 0

M Non-urban Urban Non-urban Urban Superclass Superclass

Figure 2.7. Comparison of diet between the superclasses of Non-urbanS and UrbanS in stomach contents of red foxes (n =108) (a) mean proportion stomach volume of rubbish (± se), (b) percentage of native mammals consumed (out of all mammals consumed). Non-urbanS = Natural and Agricultural land use categories; UrbanS = Peri-urban, Suburban and Urban land use categories.

2.5 Discussion

As predicted, the proportion of introduced mammals and rubbish identified within red fox stomachs significantly increased across the land use gradient, from the natural to urban land use categories; whereas the proportion of native mammals and plants consumed decreased along the gradient. In contradiction to my prediction, the consumption of birds and insects did not vary across the gradient. Insufficient amounts of non-insect invertebrates and reptiles were consumed to allow testing of the original hypotheses; however, it was evident that consumption of these prey categories was low across the gradient. Overall, however, my findings further illustrate the dietary plasticity of red foxes and demonstrate that urban environments provide important foraging opportunities, especially involving non-native animals and anthropogenic food sources, and this may explain the relative success of red foxes in urban Australia as it does elsewhere in Europe (Contesse et al. 2004; Harris 1981b).

Most studies of red fox diets in Australia have shown mammals and invertebrates to form the major dietary components in temperate environments (Brown & Triggs 1990; Catling 1988; Lunney et al. 2001; Lunney et al. 1990; Saunders et al. 2004). In this study, invertebrates (predominately insects) still formed the major component of the diet of red foxes; however, mammals were replaced by plants as the predominant and most frequent food source. This finding is consistent with other studies that found plant matter as a major diet component of red foxes in Australia (Baker & Degabriele 1987; Green & Osborne 1981; Meek & Triggs 1998; Rose et al. 1994; Ryan & Croft 1974). The high frequency of grass ingested, but relatively low volume, reflects my finding that small amounts of grass was consumed by most individuals. There have been varying reports as to whether red foxes gain any nutritional benefit from ingesting grass (Lund 1962; Saunders et al. 2004); however, due to the high frequency of grass reported in both international (Ciampalini & Lovari 1985; Harris 1981b; Kidawa & Kowalczyk 2011) and Australian (Coman 1973; Crawford 2010; McIntosh 1963a) dietary studies, there is little doubt that foxes deliberately eat grass. It has been proposed that wild canids ingest grass to aid with digestion (Sueda, Hart & Cliff 2008) and/or assist in the removal of gastro-intestinal parasites (Hart 2011). In this study, carcasses were almost always associated from

vegetated areas, paddocks or urban parks, as such grass was readily available for consumption and it is likely that some grass was also incidentally ingested while consuming other items.

2.5.1 Variation in diet composition among land use categories

Consumption of insects by stomach volume varied considerably among land use categories, with the greatest volume occurring within agricultural areas and the lowest in natural areas. Insect consumption was found to vary seasonally, which has been identified previously (Cavallini & Lovari 1991; Ciampalini & Lovari 1985; Ricci et al. 1998); however, a confounding sampling bias could have influenced this result as, by chance, most of the carcasses from agricultural areas happened to be collected in summer and autumn when insects are most abundant. The high abundance of insects was reflected in the red foxes diets, with multiple individuals consuming greater than 50 crickets. Furthermore, a large proportion of the ‘natural’ category red fox stomachs were collected during winter, when insects are not abundant; this could explain the low consumption of insects by foxes from these areas. A consequence of these sampling biases is that the proportion of the other food categories that red foxes would consume at other times of the year may not be accurately represented in this study. Hence, this limited conclusions that could be drawn about the consumption of vertebrate prey categories in agricultural areas, as mentioned below. To accurately assess the effect of land use categories on the proportion of insects consumed, further collection of carcasses is required to even out the seasonal spread of samples across each land use category.

The proportion of all mammals consumed across the land use gradient varied significantly, with equally high proportions of mammals consumed in natural, peri- urban and urban areas and the lowest consumption in agricultural areas. Human settlement and agricultural land use across Western Sydney has seen native ground dwelling mammals, such as native rodents, bandicoots and dasyurids, essentially vanish from this region (Threatened Species Scientific Committee 2008). Rabbits have previously been reported as an important prey source for red foxes in Western Sydney (Adderton 1998) and other typical prey, such as common brushtail possums, are urban adapters and remain in this landscape (Tozer et al. 2015). Hence, it is more likely that the low consumption of mammals in agricultural areas was due to red

foxes primarily consuming seasonally abundant insects when they were collected, rather than a low availability of other prey species.

The consumption of birds by red foxes varied among the land use categories, peaking in suburban areas, although some of this variation was explained by season. Suburban birds most commonly forage on the ground (Emlen 1974; Falk 1976; Green 1984), which is where most of the birds found in this study were likely to have been predated upon by red foxes. Interestingly, the proportion of birds consumed was highest in spring, suggesting that they may be predating upon nestlings or fledglings. Predation on young altrical nestlings that lack feathers was indicated by the consumption of bird remains where no feathers were present, which were otherwise identified by the presence of hollow bones. Thus, young birds may be a seasonally important prey species for red foxes in urban areas, something that warrants further research.

The variation in diet composition found among the land use categories further illustrates the dietary plasticity of red foxes, and that this behaviour persists in the Greater Sydney region, Australia.

2.5.2 Variation in diet composition across the land use gradient

In general, urban environments support higher densities and abundance of birds, most of which are urban adapters (Garden et al. 2006; McKinney 2002; Sorace 2002), suggesting that the prey availability of birds should increase towards urban areas. However, there was no linear relationship in either direction in the consumption of birds along the land use gradient. Whilst the fragmented Cumberland Plain Woodland in Sydney’s west still supports strong communities of ground feeding and nesting birds (Threatened Species Scientific Committee 2008), in urban areas of Sydney, the relative abundance of ground and shrub nesting species that would be vulnerable to red fox predation is depauperate (Parsons, Major & French 2006). This has been shown for other urban areas of Australia (Sewell & Catterall 1998). In this study, all of the bird species identified in red fox stomachs are associated with nesting or foraging close to the ground, supporting the idea that a limited range of bird species are susceptible to fox predation.

Contrary to my expectation, the proportion of insects consumed by red foxes did not increase along the land use gradient. Insects are an important food source for red foxes (Cavallini & Lovari 1991; Ciampalini & Lovari 1985; Coman 1973; Croft & Hone 1978), and it is likely that they would be consumed in high proportions across all areas of the land use gradient when seasonally abundant. Further research is required, with a balanced distribution and temporal collection of carcasses across the gradient.

As predicted, the consumption of plants by red foxes decreased along the land use gradient. Red foxes in natural areas, where plant consumption was highest along the gradient, were mainly consuming grasses, bark and other herbaceous material rather than items of more energetic value such as fruit and nuts. As mentioned previously, some of this ingestion of herbaceous material was most likely deliberate. However, this result may be confounded by red foxes in natural areas frequently ingesting small amounts of plant matter whilst consuming relatively fewer types of other prey categories (Fig. 2.4a). Hence, plant matter accounted for the bulk of the proportional stomach volume for these foxes when the actual biomass of plant material ingested was low, which is a limitation of assessing diet by one measure alone (Klare et al. 2011).

Unsurprisingly, red foxes consumed the greatest proportion of anthropogenic food in suburban and urban areas which supported my hypothesis. Red foxes have been shown to consume greater proportions of anthropogenic food towards the city centres in other urban environments across the world (Contesse et al. 2004; Harris 1981b), however this is the first time it has been reported across a land use gradient in Australia.

2.5.2.1 Exploiting anthropogenic food The consumption of anthropogenic food in terms of frequency and volume by red foxes in the urbanS superclass in this study was lower than what has been reported for other populations of urban foxes around the world. Anthropogenic food in this study only accounted for 10% of the mean stomach volume and occurred in 34.6% of stomachs for foxes from the urbanS superclass category. In comparison, European studies have recorded anthropogenic food accounting for 35-50% of the mean

stomach volume and occurring in 50-83% of urban red fox stomachs (Contesse et al. 2004; Doncaster et al. 1990; Harris 1981b; Saunders et al. 1993). The variation in consumption of anthropogenic food by red foxes in these populations has been attributed to differences in available habitat (Harris & Rayner 1986) and attitudes of residents towards feeding wildlife (Harris & Woollard 1991) between these European cities. The lower occurrence of anthropogenic food record in this study warrants further investigation as we would anticipate that this resource is readily available, especially in urban areas of Australia (Oro et al. 2013), and highly nutritious (Murray et al. 2015).

As with other studies on the diet of urban red foxes, it is difficult to quantify all food sources available to foxes in such a large urban environment (Harris 1981b). Red foxes in this study may have consumed less anthropogenic food than reported in other urban diet studies as they are less reliant on scavenging due to the variety of other food sources available in urban Australia. The other studies reporting urban red fox diets are from populations within their natural distribution and hence predation on vertebrates in these cities is largely limited to locally native prey species that have evolved with foxes. In urban environments of Australia, red foxes have access to ‘introduced’ species that evolved with the fox, such as rodents and rabbits, in addition to Australian native species that did not evolve with this predator, and hence are susceptible to fox predation as a result of naïveté (Cox & Lima 2006). Whether red foxes preferentially select ‘introduced’ prey that they have evolved to hunt or ‘naïve’ native prey in urban environments is yet to be determined, but it is not supported by the findings of this study. An alternate explanation for the lower occurrence of rubbish in the diet of red foxes in this study is the relative lack of access to anthropogenic food sources such as garbage bins and food left out for wildlife, when compared to European cities where urban fox diets have been studied. Unlike Contesse et al. (2004) and Harris (1981b), surveys to assess anthropogenic food available to red foxes from garbage bins and residents were not undertaken. Further research is required to determine the relative availability of anthropogenic food sources to urban red foxes in the Greater Sydney region; however it is evident that they are not dependent on a supply of anthropogenic food alone.

2.5.2.2 Native and introduced mammals As predicted, the proportion of native and introduced mammals varied along the land use gradient. Proportionally more introduced mammals, primarily rodents, were consumed towards the urbanised end of the gradient and conversely more native mammals, predominately possums, were consumed towards the natural end of the gradient. Rodents form the staple diet of foxes across most of their natural distribution (Calisti et al. 1990; Ciampalini & Lovari 1985; Dell'Arte et al. 2007; Goszczyński 1974; Kidawa & Kowalczyk 2011; Yoneda 1982) and urban environments support high populations of non-native species such as rodents (Mackin-Rogalska et al. 1988; McKinney 2002; Sorace 2002). Therefore it is unsurprising that red foxes would predominately consume introduced rodents in urban areas of Australia.

Intriguingly, a greater proportion of native mammals were consumed at the urban end of the gradient compared to introduced mammals at the low density end. In natural areas where native mammals were primarily consumed, only three native species were identified, the common ringtail possum, swamp wallaby (Wallabia bicolor) and the bush rat. Ringtail possums accounted for the greatest proportion of stomach volume of the native mammals consumed by foxes in natural habitats. However, more individual ringtail possums were consumed in urban areas (n = 6) than natural areas (n =3). Brushtail possums were only consumed in urban areas, and both species are notable urban adapters. In Australia, predation by foxes on both these possum species has been reported in semi-urban areas (White et al. 2006) and in remnant vegetation on the periphery of suburban areas (Coates & Wright 2003; Kennedy 1995), but never before in such a high density urban environment.

2.5.3 Implications for fox management in urban areas of Australia

My findings demonstrate that red foxes in the Greater Sydney region exploit a wide variety of food sources, confirming the dietary plasticity of foxes. The wide availability of different food sources in urban areas of Australia may have a similar lack of interaction on breeding success as has been reported in other urban fox populations around the world (Harris 1981b). As such, urban foxes in Sydney are not likely to be limited by the availability of their food resources, but further studies are required to validate this.

This initial examination on the diet composition of red foxes in urban Australian environments would not cause much concern for conservation due to the relatively low frequency of native species identified in the diet of red foxes, and the absence of any threatened species. However, the extent to which native species living in urban environments in Sydney are placed under pressure by predation from foxes requires further research. Our identification of prey species in the stomachs of foxes was limited to mammal remains that had hair present and other vertebrate remains with diagnostic feature present, such as skulls, feet and scales (reptiles). As such, many bird and vertebrate remains were left unidentified and the true impact of fox predation on native species in the Greater Sydney region is likely underestimated. DNA barcoding (Dunshea 2009; Santos et al. 2015) and stable isotope analysis (Lavin et al. 2003) of stomach remains has become a useful complementary tool to morphological analysis in recent times. Stable isotope analysis can also reveal diet composition data over a longer period of time than possible by stomach analysis, due to the retention of isotopes in less metabolically active tissues over longer periods of time (Hobson & Clark 1992; Tieszen et al. 1983). They were not considered in this study because there is a lack of reference material for the wide range of Australia fauna that red foxes consume (A. Macdonald & K. Brandis, personal communication).

Urban adapters, the common brushtail and common ringtail possums, were the only native mammal species consumed in high density areas. Neither of these species are currently listed as threatened and they both maintain high densities in urban environments (Hill, Carbery & Deane 2007) despite the presence of introduced predators such as foxes, cats and dogs and risks posed by vehicles (Augee et al. 1996; Barratt 1997; Pietsch 1994). Possums may not be threatened, however, they face an increasingly fragmented urban environment (Hill et al. 2007) and additional pressures, such as fox predation, which could contribute to their decline in time. On the other hand, estimates of predation or presence of prey in the diet of predators do not necessarily correlate with relative impact on prey populations (Banks 1999; Barratt 1998). Thus, further research is required to determine whether foxes are impacting populations of native urban adapters at the population level in Australian urban environments.

No threatened species were recorded in the diet of foxes in the Greater Sydney region in this study. However, predation by foxes has been recorded for threatened species known to occur within the Greater Sydney region, such as long nosed bandicoots, little terns, pied oystercatchers and little penguins (Department of Environment and Climate Change 2007; Office of Environment and Heritage NSW 2011). The absence of these species recorded in the diet of foxes in this study is likely due to the large scale over which foxes were collected in relation to the small distribution over which these species are found in the Greater Sydney region. For a generalist predator such as the red fox, the effects of predation on these locally endemic species when they are not the predominant prey source can still be depensatory on the density of these prey species (Sinclair et al. 1998), placing them at risk of local extinction.

Only two foxes contained the remains of reptiles and no foxes were found to have consumed any amphibians. Australian studies have demonstrated that reptiles do not form a major component of fox diet in non-arid environments, where other vertebrates such as birds and mammals are more frequently consumed, unless there is a shortage of the latter (Catling 1988). Of the two reptile remains found, both were eastern snake-necked turtles (Chelodonia longicollis); with one fox having consumed an adult turtle and the other having predated upon late term eggs. Although turtle predation was not frequent in this study, it has been observed previously in Sydney (White & Burgin 2004) and the impact of red foxes on freshwater and marine turtle nests elsewhere in Australia has been well documented (Heppel et al. 1996; Thompson 1983). Only 12 out of 39 (Crawford 2010; Davis et al. 2015; Glen et al. 2011; Spencer, Crowther & Dickman 2014) studies on fox diet in Australia have recorded the presence of amphibians in their diet, so it is not surprising that they were not recorded here. Thirty species of frogs are known to occur in the region and are considered common in areas with creeks or ponds (White & Burgin 2004) where foxes commonly occur. Furthermore, red foxes have been identified as a Key Threatening Process to two threatened amphibian species that occur in the Sydney Basin, the giant burrowing frog (Heleioporus australiacus) and green and golden bell frog (Litoria aurea) (DEWHA 2008). Hence, despite the absence of predation on these species in this study, it is paramount that the sites where the threatened species mentioned above are present, are continued to be listed as priority fox management

sites by the NSW state government (Office of Environment and Heritage NSW 2011).

The mitigation of threats posed by invasive species is more effective when the community understands and supports the need for management action (DEWHA 2008). Furthermore, educating the community is a crucial tool in urban ecology as it provides an opportunity to promote effective conservation of native species (Kendle & Forbes 2013) clinging on to refugia in urban areas. It is hoped that educating the public on the diet of foxes in Sydney, such as predation on native possums, will increase their support for fox and in turn decrease public resistance or backlash to fox management undertaken in urban areas.

2.6 Conclusion This is the first time the diet of red foxes has been described across an urban land use gradient in Australia. Red foxes in the Greater Sydney region exhibited high dietary plasticity, with insects and plants the most common prey categories consumed. The increased proportion of introduced mammals, birds and anthropogenic food consumed in urban areas highlights foraging opportunities for urban red foxes. While the proportion of native mammals consumed decreased towards urban areas, possums still formed a considerable proportion of their diet in urban areas. Thus, this study confirms that native urban adapter species are still susceptible to fox predation in urban environments in Australia. No threatened species were identified in any of the stomachs in this study however there are localised populations of threatened species within the Greater Sydney region that are vulnerable to fox predation.

Further research is required to determine whether predation by foxes equates to having an impact on populations of native species living in refugia in urban environments. A complementary analysis of red fox scats collected across a land use gradient in the Greater Sydney region could strengthen the findings in this study as scats will provide information from areas where it is difficult to source carcasses. It is anticipated that the findings of this study will inform land managers and the general public within Sydney of the evidence of predation on native species in urban environments, and highlight areas where native species are most affected by fox predation.

CHAPTER 3

MORPHOMETRICS AND BODY CONDITION OF AN INVASIVE PREDATOR ACROSS AN URBAN TO NATURAL LAND USE GRADIENT

3.1 Abstract Adult body mass and condition are crucial for reproductive success and survival in mammals and other animals. The red fox (Vulpes vulpes) is one such predator that, across its extensive global distribution, displays varying body mass and condition that has implications for individual fitness and population dynamics. Studies on native red foxes living in the proximity of human settlements, suggest that these foxes are larger due to the availability of anthropogenic food. However, few studies have demonstrated morphological variation of red foxes in areas where they have been introduced. The red fox was introduced into Australia in the mid-19th century, where it is known to be a successful urban adapter as well as a highly effective predator of naïve native species; yet, no studies have compared morphological differences of introduced red foxes inhabiting Australia’s urban and non-urban environments. This study assesses the morphology of 130 red foxes along an urban to natural land use gradient in the Greater Sydney region, Australia, in relation to their diet. Red foxes from high human population density areas were significantly larger than foxes from low human population density areas. In addition, red foxes that had consumed anthropogenic food were in better condition than those that had not. The consumption of different prey categories by adult red foxes had no significant effect on skeletal size across the land use gradient. To the best of my knowledge this is the first Australian study to report that anthropogenic modification of the environment has influenced the body size and condition of red foxes. This has implications for the management of red foxes in urban areas of Australia as human behaviour is likely to be supporting inflated numbers of foxes through access to anthropogenic food, which would not only benefit these predators but in turn place increased pressure on native prey species in urban environments.

3.2 Introduction

Adult body size and mass are crucial for fitness in mammals. For males, these traits often play a role in the acquisition and defence of mates or territories (Iossa et al. 2008); whereas for females, they are important for fecundity as well as offspring size and survival (Festa‐Bianchet, Gaillard & Jorgenson 1998; Moehlman & Hofer 1997). Similarly, body size and mass is directly related to the energy expended by mammals through the costs of thermoregulation and locomotion, and hence influences energy requirements and associated dietary needs (Taylor, Heglund & Maloiy 1982; Taylor, Schmidt-Nielsen & Raab 1970).

The energetic state of an animal is often defined as its body condition, where an animal in good condition is assumed to have greater energy reserves relative to its size than those in poor condition (Schulte-Hostedde et al. 2005). Wild mammalian carnivores that have a better body condition tend to have higher reproduction and survival (Boertje & Stephenson 1992; Matlack & Evans 1992), so that body condition can be used as a proxy for fitness in many mammalian populations (Kirkpatrick 1980).

Despite the challenges facing carnivorous mammals in urban environments, a number of medium sized carnivores have successfully colonised urban areas around the world (Bateman & Fleming 2012). These mesopredators are generally able to replace large predators by becoming commensal with humans, exploiting the wide variety of anthropogenic food sources made available from human activity, such as scavenging garbage, road kill, agricultural crops and the pest mammals, birds and/or insects associated with these crops (Newsome et al. 2015; Yom‐Tov 2003). In turn, an abundance of food sources and protection from predators has resulted in increased growth rates and improved body conditions in many urban carnivores, with concomitant positive effects on the fitness and population densities of individuals in urban settings (Bateman & Fleming 2012).

The influence of humans on the morphology and body condition of urban carnivores has received much recent attention. Urbanisation has been attributed to increased body mass in black bears (Ursus americanus) (Beckmann & Lackey 2008), kit foxes (Vulpes macrotis) (Cypher 2010) and Eurasian badgers (Meles meles) (Roper 2010) in urban areas; as well as increased body condition in urban racoons (Procyon lotor) 58

(Rosatte, Power & MacInnes 1991). Similar effects have also been found in other carnivores that are commensal with humans and take advantage of anthropogenic food sources. Analyses of museum specimens of red foxes (Vulpes vulpes) and European badgers in Denmark (Yom-Tov et al. 2003), and the striped hyena (Hyaena hyaena), golden jackal (Canis aureus), wolf (Canis lupus), and European badger in Israel (Yom‐Tov 2003) have undergone an increase in body size during the 20th century. This has been associated with an increase in the availability of anthropogenic food sources in these areas, due to increased agricultural production and the availability of garbage dumps surrounding human settlements. Therefore, by providing access to anthropogenic food sources, humans are inadvertently influencing the morphometrics of urban carnivores (Bateman & Fleming 2012).

In most studies to date, urban carnivores are native species and the main implications of their presence is applying predation pressure on other native species persisting in human modified habitats and potentially human-wildlife conflicts. However, in areas where mesopredators have been introduced, the presence of predators in urban environments can have significant implications for native urban wildlife, as is the case for feral cats (Felis catus) and red foxes introduced to Australia. In addition to human commensal species, urban habitats can support rare and threatened species, presenting an opportunity for their conservation. A recent study identified that urban areas in Australia contain considerably more threatened species than non-urban areas per unit of area (Ives et al. 2016). The creation of artificial habitats, such as ponds and wetlands for amphibians (Chovanec 1994; Garcia-Gonzalez & Garcia-Vazquez 2012), artificial rocks for reptiles (Webb & Shine 2000), or nest boxes for hollow- utilising fauna (Goldingay & Stevens 2009; Harper et al. 2005), can assist in conserving threatened species in urban environments.

In Australia red foxes can place greater pressure on native species, including in urban environments, as a result of prey naiveté (Cox & Lima 2006), and as such have been listed as a Key Threatening Process wherever they occur by state and federal governments (DEWHA 2008) due to their impacts on native species. The morphology (Cavallini 1995; Fairley 1970; Hattingh 1956; Kolb 1978; Kolb & Hewson 1974; Storm et al. 1976; Takeuchi 2010) of red foxes throughout their natural home range has been extensively studied. However, few studies have directly examined the effects of diet on the morphology of red foxes (Lindström 1983;

Soulsbury et al. 2008), let alone outside of their natural range. While red foxes are common in urban environments across Australia (Saunders et al. 2010), no studies have investigated the influence of anthropogenic food sources and native prey on the morphology and body condition of foxes in these environments.

Predator management is commonly undertaken incorporating biological knowledge of the prey in combination with that of the predator (Saunders et al. 1995); however, information on the morphology and body condition of urban red foxes is important for their management as they are crucial fitness components enabling this introduced predator to persist in Australia’s urban settings. For example, increased body size benefits the ability of red foxes to move in and out of fragmented habitats in urban environments (Bateman & Fleming 2012; Gehring & Swihart 2003). By identifying areas along land use gradients where body condition in red foxes is low, such as areas where foxes experience nutritional stress and increased demand for prey biomass, this information might identify areas to conduct poison baiting programs in order to maximise bait uptake (Winstanley et al. 1999).

Here, I investigate the morphology of red foxes along an urban land use gradient in Sydney, Australia, in relation to diet. I expected that, as a result of increased access to anthropogenic food sources, the body size, mass and body condition of red foxes would increase across the land use gradient towards urban areas. I further examine the morphology of urban foxes in Australia in relation to other red fox populations around the world. I expected that red foxes would exhibit similar degrees of sexual dimorphism to other populations around the world, however, red foxes would be larger in urban Australia, due to the combination of anthropogenic food sources and evolutionary naïve native prey.

3.3 Methods

3.3.1 Study area

This study was carried out in the Greater Sydney region, New South Wales, Australia (32.4−35.7°S, 148.8−152.4°E). The study region includes Australia’s largest city, Sydney, which currently supports 4.6 million people, and is rapidly increasing (Australian Bureau of Statistics 2016). The alluvial plains, where the majority of human settlement occurs, is dominated by shale, whereas the national parks surrounding Sydney are dominated by sandstone (Benson et al. 1996; Walker 1960) and contain most of the remnant vegetation in the region (Mitchell & Banks 2005). Sydney has a temperate climate with mild winters and warm summers, whereas the elevated regions to the west of the area (Blue Mountains National Park) experience cool winters and mild to warm summers (Mitchell & Banks 2005; Stennett & Beggs 2004).

3.3.2 Sample collection

Red fox carcasses (n = 140) were collected from across the Greater Sydney region from late 2015 to 2017 (Fig. 3.1). They were provided from routine pest management conducted by land managers; in addition, a small number of these carcasses (n = 11) were opportunistically collected due to road kill. The geographic coordinates of the location where each carcass was found were recorded. Each carcass was frozen for storage and subsequently thawed for 2-3 days before processing.

Red foxes were sexed and weighed using an electronic hook scale for body mass. Each carcass was weighed three times, with mass recorded to the nearest 5 g, and an average of the three weights recorded. The age of each red fox was estimated by assessing the tooth wear of the upper and lower incisors (Harris 1978).

Six morphometric measurements were taken for each red fox (Table 3.1, Fig. 3.2). Femur, short foot and long foot length were measured using Vernier callipers to the nearest 0.1 mm, while nose to tail base, and tail length were measured with a material tape measure to the nearest 5 mm. Each measurement was repeated three times and the average was recorded to increase precision (Blackwell, Bassett & Dickman 2006).

Only measurements from red foxes aged older than six months were used in subsequent analyses, as juvenile foxes are near fully grown by six months of age, or otherwise indistinguishable from adults based on size alone (Fairley 1970). The body mass and morphological measurements of any pregnant females, damaged or decomposing carcasses were excluded from data analysis. Sources of damage to carcasses occurred from shooters removing tails for trophies and absent visceral mass as a result of vehicle collision. Thus, 130 red fox carcasses were included in subsequent analyses.

Figure 3.1. Location and land use categories of 130 red fox carcasses used for morphological analysis across the Greater Sydney region. Land use categories- Natural (green), Agricultural (yellow), Peri-urban (blue), Suburban (orange) and Urban (red). Image: Google Earth.

Table 3.1. List of measurements (in mm) and their abbreviations

Measurement Acronym

Femur length (proximal knob of femur bone to patella) FL

Short foot length (from edge of calcaneum to tip of metatarsal pad) SF

Long foot length (from edge of calcaneum to tip of third phalange, with phalanges LF extended)

Nose to tail base length (from nasal speculum to sacrococcygeal joint) NTB

Tail length (from sacrococcygeal joint to tail end) TL

Body length (from nasal speculum to tail end) BL

Figure 3.2. Illustration of the morphological measurements recorded from red fox carcasses: femur (F), short foot (SF), long foot (LF), nose to tail base (NTB), tail length (TL), body length (BL).

3.3.3 Land use categories

The human population density (HPD) (Australian Bureau of Statistics 2011) within 1 km2 around each red foxes’ GPS coordinates were extracted using RStudio (version 0.99.903; RStudio Inc.; Boston, Massachusetts). Each carcass was classified into a land use category, based on its location and HPD value as reported in Chapter 2.

3.3.4 Comparisons with global red fox morphology

Studies from around the world reporting morphometric measurements of red foxes were collected and compared to the results from this study, for male and female adult

foxes. Studies reporting red fox morphometrics included: five from the British Isles (Fairley 1970; Hattingh (1956); Iossa et al. (2008); Kolb (1978); Kolb and Hewson (1974)); four from mainland Europe (Cavallini 1995; Gomes & Valente 2016; Gortazar et al. 2000; Travaini & Delibes 1995); two from North America (Hoffman & Kirkpatrick 1954; Storm et al. 1976); one from Asia (Takeuchi 2010); and five from Australia (Berghout 2000; McIntosh 1963b; Meek & Saunders 2000; Read & Bowen 2001; Winstanley, Saunders & Buttemer 1998).

Measurements used for comparison were body mass (BM), nose to tail base length (NTB) (reported as head and body length in some studies), total body length (BL), and hind foot length (reported as LF in this study). The fox population studied was either classed as ‘native range’ (natural distribution) or introduced (non-native Australian distribution), and urban or non-urban based on their location. These categories were combined to create four classes of red fox populations- ‘Native range: non-urban’, ‘Native range: urban’, ‘Australian: non-urban’ and ‘Australian: urban’. Only one other study reported the morphometrics of a population of ‘native range: urban’ foxes (Bristol, United Kingdom) and they only reported body mass values. All of the studies reporting the morphometrics of introduced red foxes in non-urban environments were from Australia.

Red foxes from the Greater Sydney region in this study were classed as ‘Australian: non-urban’ if they were from the ‘Natural’ and ‘Agricultural’ land use categories and classed as ‘Australian: urban’ if they were from the ‘Peri-urban’, ‘Suburban’ and ‘Urban’ categories.

Sexual dimorphism in morphological measurements was calculated as the difference between the means for males and females. Sexual dimorphism and standard deviation was calculated as follows:

Sexual dimorphism (x̅diff) = x̅푚푎푙푒 − x̅푓푒푚푎푙푒

2 2 휎 휎푓푒푚푎푙푒 Standard deviation of sexual dimorphism = √ 푚푎푙푒 + 푛푚푎푙푒 푛푓푒푚푎푙푒

where x̅푚푎푙푒/푓푒푚푎푙푒 represents the mean of male or female measurements, σmale/female the standard deviation of male or female measurements, nmale/female the sample size of males or females.

3.3.5 Statistical analysis

A principal components analysis was conducted on the morphometric data of all red foxes collected in this study, including cubs (skeletal dimensions: length of femur, short foot, long foot, nose to tail base and body length). The first principal component was retained as it had an eigenvalue greater than 1 and explained 82.3% of the total variance (Table 3.2). The value from the first principle component was used to create an additional variable of skeletal size for each fox- hereafter referred to as the ‘skeletal size index’. A measure for body condition was created, using the residuals from a regression of body mass on skeletal size index, hereafter referred to as ‘body condition index’.

The residuals from an ordinary least squares regression of body mass on some linear skeletal dimension are commonly used as estimators for body condition and fat content in mammals (Schulte-Hostedde et al. 2005). To this end, a body condition index was calculated from an ordinary least squares regression of body mass on the skeletal size index values for each red fox. Adult red foxes that scored high on this index were considered to be in better condition and to have more fat reserves than individuals that scored low; see Huot, Poulle and Crête (1995) and Lunn and Boyd (1993).

To assess the effect of diet on morphology, an extra variable recording the presence or absence of a particular prey category in the stomach of each fox was created (from Chapter 2). The relationship between the presence of different categories and mean skeletal size and body condition index was tested using a general linear model.

The relationship between body mass, skeletal size index and body condition index among the land use gradient were analysed using a general linear model. The effects

of sex were controlled in the model. To test for variation among the land use gradient, the land use categories were not included as covariates. To test for linear variation along the land use gradient, the land use categories were included as covariates.

Table 3.2. Eigenanalysis of the correlation matrix and factor loadings for the principal components extracted from the morphometric variables.

Principal component PC1 PC2 PC3 PC4 PC5

Eigenanalysis of the correlation matrix

Eigen value 4.113 0.433 0.332 0.079 0.042

Percentage variance explained 82.3 8.7 6.6 1.6 0.8

Culmulative percentage variance explained 82.3 90.9 97.6 99.2 100

Factor loadings

Femur length 0.422 0.256 -0.839 0.227 -0.002

Short foot length 0.449 0.373 0.495 0.574 -0.291

Long foot length 0.457 0.457 0.197 -0.633 0.378

Nose to tail base length 0.444 -0.616 0.105 0.260 0.587

Body length 0.463 -0.455 -0.010 -0.389 -0.654

For the meta-analysis of global red fox morphology, the reported sample size, mean measurements and standard deviation for classes were all combined using the following calculations:

Combined sample size (ncomb) = 푛1 + 푛2 + … + 푛푖

(푛1+ x̅1) + (푛2+ x̅2)+ … + (푛푖 + x̅푖) Combined mean (x̅comb) = 푛푐표푚푏

Difference in mean (di) = x̅푖 − x̅푐표푚푏

2 2 2 2 2 2 푛1(휎1 + 푑1) + 푛2(휎2 + 푑2)+ … + 푛푖(휎푖 + 푑푖 ) Combined standard deviation (σcomb) =√ 푛푐표푚푏

where ni represents the sample size, x̅푖 the mean measurement and σi the standard deviation of foxes in the ith study. The reporting of nose to tail base length (n = 12), body length (n = 7) and hind foot length (n = 12) were not consistent across all studies. To simplify the comparison between body size between population classes, the frequently reported length measurement would be used for further analysis.

However, nose to tail base and hind foot length were both reported in 12 studies (not the same studies though). Thus, a regression against body mass was created (Fig. 3.3) to determine which measurement correlated the most with body mass and hence was the best indicator of size. Nose to tail base length (R2 = 0.45) correlated slightly more with body mass than hind foot length (R2 = 0.40), thus, nose to tail base length was used for size comparisons between population classes.

(a) (b)

8 8

7 7

)

g k

k 6 6

(

s a a 5

5 M M

4 4

3 3 500 550 600 650 700 750 130 140 150 160 170 NTB (mm) HF (mm)

Figure 3.3. Regressions of length measurements against body mass (kg) for red foxes in the Greater Sydney region: (a) nose to tail base (NTB) length (mm), (b) hind foot (HF) length (mm). N = 130. Linear regression line is shown in black.

The combined measurements for ‘Native range: non-urban’, ‘Native range: urban’ and ‘Australian: non-urban’ were each independently tested for differences with the measurements for ‘Australian: urban’ using a two-tailed t-test.

3.4 Results

3.4.1 Effects of diet on morphology along an urban land use gradient

3.4.1.1 Body mass

There was no significant difference in body mass for red foxes containing mammals, birds, insects or plants in their stomach (p > 0.05; Fig 3.4a-d). Red foxes with rubbish in their stomach were significantly heavier than foxes that had no rubbish

(F1,97 = 4.76, p = 0.032; Fig. 3.4e).

(a) (b)

5.8 5.8

5.6 5.6

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k (

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(e)

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Figure 3.4. Mean body mass for red foxes that have different prey categories present or absent in their stomachs (± se; n = 99): (a) mammals, (b) birds, (c) insects, d) plants, (e) rubbish.

3.4.1.2 Skeletal size Skeletal size did not vary significantly with the presence of any food item in a red foxes’ stomach (all F1,98 < 2.56, p > 0.113; Fig. 3.5).

(a) (b)

1.0 1.0

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1.0 1.0

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t 0.0

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1.0

0.5

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S -0.5

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Absent Present Presence of prey item in stomach

Figure 3.5. Mean skeletal size index values for red foxes that have different prey categories present or absent in their stomachs (± se; n = 100): (a) mammals, (b) birds, (c) insects, d) plants, (e) rubbish.

3.4.1.3 Body condition index There was no significant difference in body condition index for red foxes containing mammals, birds, insects or plants in their stomach (p > 0.05; Fig. 3.6a-d). Red foxes with rubbish in their stomach were significantly heavier than foxes that had no rubbish (F1,97 = 4.76, p = 0.032; Fig. 3.6e).

(a) (b)

0.4 0.4

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0.4 0.4

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i 0.0 0.0 d

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Figure 3.6. Mean body condition index for red foxes that have different prey categories present or absent in their stomachs (± se; n = 99): (a) mammals, (b) birds, (c) insects, d) plants, (e) rubbish.

3.4.2 Morphology among and along land use categories

Body mass varied significantly among the land use categories (F4,109 = 2.72, p = 0.033), as did body mass between male and female red foxes (F1,109 = 38.01, p < 0.001) (Fig. 3.7a). The body mass of all red foxes increased significantly towards the more urbanised land use categories (F1,112 = 9.73, p = 0.002) and males were significantly heavier than females across land use categories (F1,112 = 39.42, p < 0.001) (Fig. 3.7a).

The variation in skeletal size among the land use categories was significant

(F4,111 = 2.58, p = 0.041), as was the difference in skeletal size between male and female red foxes (F1,111 = 59.5, p < 0.001) (Fig. 3.7b). Males consistently had a larger average skeletal size than females along the land use gradient (F1,114 = 61.41, p < 0.001) and for both sexes there was a significant increase in mean skeletal size towards higher human population density (F1,114 = 10.32, p = 0.002) (Fig. 3.7b).

There were no significant differences in mean body condition index in red foxes among land use categories (F4,108 = 1.76, p = 0.142), however males and females varied significantly among land use categories (F1,108 = 4.04, p = 0.047) (Fig. 3.7c). There was no significant difference in mean body condition index along the land use gradient (F1,111 = 3.05, p = 0.084; Fig. 3.7c). However, there was a significant difference in mean body condition index between sexes (F1,111 = 4.540, p = 0.035) (Fig. 3.7c), with the males generally in better condition than females in natural and urbanised areas, with the exception of peri-urban red foxes.

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Figure 3.7. Mean morphological measurements of male (M) and female (F) red foxes against land use categories (± se; n = 116): (a) mass (n: M = 72, F = 42) (b) skeletal size index (n: M = 72, F = 45), (c) body condition (n: M = 71, F = 43). (a) (b) 6.5 720

700 6.0 3.4.3 Comparisons of morphology between global fox populations 680 5.5 660 There were no significant differences in body mass in male foxes from native range 640 non-urban environments and urban foxes from Sydney (t460 = 1.37, p = 0.17; 5.0 620 Fig. 3.8a). Male foxes from native range non-urban environments were significantly 4.5

Mean ody mass (kg) mass Meanody 600 F M F M F M F M Mean NTB length (mm) F M F M F M longer than male urban foxes from Sydney in terms of mean NTB length (t403 = 5.74, Native Australian: Australian: p < 0.001; Fig. 3.8b). Females from native range non-urban environments were range: non-urban urban Class non-urban significantly heavier (t59 = 2.23, p = 0.03; Fig 3.8a) and longer in terms of NTB Class length (t403 = 5.74, p < 0.001; Fig. 3.8b) than urban foxes from Sydney.

Male foxes from Bristol were significantly heavier than male urban foxes from

Sydney (t100 = 2.05, p = 0.04); however, there was no significant difference in body mass between female foxes from Bristol and Sydney (t61 = 0.97, p = 0.33; Fig. 3.8a).

There was no significant difference between male morphometrics (body mass, NTB length) for non-urban and urban foxes in Australia (t < 1.51, p > 0.13; Fig. 3.8). There was no significant difference in body mass between female foxes in urban and non-urban environments within Australia (t190 = 0.34, p = 0.73; Fig. 3.8a). Female

foxes from non-urban Australian environments were significantly longer in terms of

NTB length (t59 = 2.09, p = 0.041; Fig. 3.8b) than female foxes in Sydney.

There was no significant difference in sexual dimorphism, as indicated by the difference in mean male and female measurements, between any of the classes for any of the morphological measurements (p > 0.05, Appendix 3.1).

Figure 3.8. Comparison of mean morphological measurements reported for male (M) and female (F) foxes in native and introduced populations in urban and non-urban environments across the globe. (a) body mass, (b) nose to tail base length (NTB). Mean measurements reported and their associated sample sizes and standard deviations are listed in Appendix 3.1.

3.5 Discussion Within the Greater Sydney region, the skeletal size and body mass of red foxes increased along the land use gradient, supporting my hypotheses. However, the hypothesis that body condition would increase along the land use gradient towards urban areas was not supported. As expected, red foxes with anthropogenic foods in their stomachs were heavier and in better condition than foxes that did not have provide evidence of consumption of such foods; yet, no effect of the consumption of anthropogenic foods on skeletal size could be demonstrated. The meta-analysis of red fox morphology supported my hypotheses that red foxes in urban areas of Sydney would exhibit similar degrees of sexual dimorphism to global red fox populations. However, urban foxes in this study were not significantly heavier or longer than non-urban foxes reported elsewhere in Australia, or urban foxes within their natural distribution.

3.5.1 Morphology versus diet along an urban land use gradient

Few studies have directly examined the effects of diet on the morphology of red foxes (Fairley 1970; Harris 1981b; Lindström 1983; Soulsbury et al. 2008). As predicted, red foxes that had access to anthropogenic food sources were heavier and in better condition than foxes that had not consumed rubbish. However, contrary to my hypotheses, there was no effect on the consumption of rubbish on skeletal size in red foxes in this study.

Although not all anthropogenic items identified in fox stomachs had an energetic benefit, such as fishing lures or food packaging, it can be inferred that the presence of these items in their diet indicated that they were frequently foraging from anthropogenic food sources, for example, rubbish bins and landfill. Similar findings have been reported in other morphometric studies on red foxes (Yom-Tov et al. 2003; Yom-Tov et al. 2007; Yom‐Tov 2003); however, this is the first time in Australia this relationship has been described along an urban land use gradient.

Studies on Mediterranean populations of red foxes have demonstrated that foxes from more productive habitats are larger (Gortazar et al. 2000) and have higher fat deposits (Gortazar 1997; Travaini 1994) than those found in poorer habitats. These studies used the agricultural productivity of these areas as a proxy for food

availability. In urban areas it is difficult to quantify food availability; however, other studies of urban fox diet in Europe have indirectly shown that there is generally a year round abundance of food in urban areas (Contesse et al. 2004; Harris 1981b). Hence it can be inferred that urban areas are more productive habitats than non-urban areas and that red fox body mass and condition increases with habitat productivity.

Red foxes reach their adult body mass during their first year of life (Soulsbury et al. 2008), with some studies suggesting that juveniles can achieve the same mass as adults as early as 6 months of age (Fairley 1970; McIntosh 1963b). Given that only data from foxes older than 6 months is presented here, it is not surprising that the consumption of different prey categories had no effect on adult skeletal size. Thus, rather it would appear that the diet of juvenile red foxes during their period of growth would have a significant effect on their adult body mass, as adult body size is a result of the period of time during growth where juveniles have unrestricted access to high quality food (Geist 1987). Long term research on urban foxes in Bristol, United Kingdom, has shown that the environmental conditions during their period of growth affected their full grown body mass, by virtue of influencing the amount of earthworms and insects available for juvenile foxes to forage on (Soulsbury et al. 2008).

3.5.2 Morphology along a land use gradient

As predicted, red foxes in areas of higher human population density were larger, in terms of body mass and skeletal size, than foxes from areas of lower human population density. Red foxes in urban areas have greater access to food sources as a result of the wide variety of anthropogenic food available for them to exploit, usually in the form of rubbish, crops, road-kill, being deliberately fed by humans, pets and livestock as well as a greater abundance of synanthropic prey species such as rodents, birds (Bateman & Fleming 2012). Similar findings have been reported in other morphometric studies on red foxes. Yom-Tov et al. (2007) reported that red foxes from agricultural areas in Spain were significantly larger than foxes from non- agricultural areas, in terms of skull morphology. Likewise, the skull size of red foxes in Denmark increased during the 20th century as a result of increased access to anthropogenic food sources from intensified and expanded agricultural land use over that period (Yom-Tov et al. 2003). Parallel studies on carnivores commensal with

humans (wolves, golden jackals, striped hyenas and European badgers) have also demonstrated an increase in body size during the 20th century as a result of increased availability of garbage and agricultural crops for these predators (Yom-Tov et al. 2003; Yom‐Tov 2003). Therefore, the effect of urbanisation and access to anthropogenic food on the morphology of red foxes is also evident in urban foxes in the Greater Sydney region.

Body condition did not increase across the land use gradient as the body condition of red foxes at opposite ends of the gradient (natural, suburban and urban areas) were higher than those in agricultural and peri-urban areas. As reported in Chapter 2, red foxes in natural and urban areas foraged on naïve native mammals. The higher body condition in these foxes compared to areas where less native prey were consumed suggests that red foxes that have access to naïve prey can expend less energy on foraging behaviour, a notion that requires further research. Red foxes in urban areas also had access to anthropogenic food sources, resulting in higher body condition than foxes from natural areas without access to anthropogenic food sources (Fig. 3.6c).

Seasonal variation in body condition has been observed in non-urban red foxes in Australia (Winstanley et al. 1999), but never reported before in urban red foxes in Australia. In urban environments where there is an abundance of food throughout the year, body condition of red foxes in their native distribution has been observed to remain constant throughout the year as there are otherwise no seasonal food shortages (Harris 1981b). Due to a lack of even temporal distribution of carcasses collected in this study, these seasonal trends in body condition of urban and non- urban red foxes could not be confirmed. To further examine any variation in body condition along a land use gradient, an even spread of samples across all seasons and all land use categories should be collected. Identifying periods during the year and areas where red foxes are in low body condition and hence in demand for food, could be used to plan effective baiting programs where and when red foxes are more likely to consume poison baits (Winstanley et al. 1999).

3.5.3 Comparisons of morphology between other global red fox populations

Despite being released into an ecosystem where red foxes have the opportunity to hunt naïve prey (Cox & Lima 2006), and the added advantage of access to anthropogenic food sources, urban foxes in the Sydney region were not significantly heavier or longer, on average, than foxes from populations within their native distribution. Furthermore, urban red foxes in this study were significantly lighter, in terms of body mass, than urban foxes from within their native distribution. Urban red foxes in the Sydney region did not consume as much anthropogenic food as urban foxes from European cities (Chapter 2) (Contesse et al. 2004; Doncaster et al. 1990; Harris 1981b; Saunders et al. 1993), suggesting that red foxes in Sydney do not have access to the same amount of anthropogenic food sources as in European cities or are less reliant on anthropogenic resources. Carnivores that exploit anthropogenic food sources are generally larger than those without access to them (Yom-Tov et al. 2003; Yom-Tov et al. 2007; Yom‐Tov 2003). Similarly adult body mass in red foxes is related to the amount and period of time they have access to of high quality food during their formative period of growth (Geist 1987; Soulsbury et al. 2008). Hence, as discussed in Chapter 2 (see section 2.5.1), there may be a lower availability of anthropogenic food resources in Sydney compared to the European cities previously studied. An assessment of availability of food from garbage bins and wildlife feeding by residents in Sydney would be required to confirm this suggestion.

An alternate explanation for the smaller body mass of urban red foxes in Sydney is avoidance of domestic dogs in urban areas. In Australia, there is evidence that red foxes avoid wild dogs in natural environments (Mitchell & Banks 2005) and domestic dogs in semi-urban environments (Coman et al. 1991). Whilst there has been no research on the interactions between dogs and red foxes in urban Australian environments, in Bristol, United Kingdom, there was a negative correlation between the distribution of stray dogs and foxes. Dogs were also the second major cause of mortality in red fox cubs (Harris 1981a). While access to anthropogenic food sources has been shown to increase the size of red foxes (Yom-Tov et al. 2003; Yom-Tov et al. 2007), in the presence of larger carnivores that also had access to the same anthropogenic food sources, the body size of the larger carnivores increased but red foxes did not, as they were possibly excluded from access to these resources (Yom‐

Tov 2003). Thus, although there is not an abundance of free ranging dogs roaming the streets of Sydney, high dog ownership in Australia (Animal Medicines Australia 2016), may result in red foxes avoiding areas of high dog activity, hence limiting access to anthropogenic food in these areas. However, this needs to be confirmed through movement ecology research on foxes in urban environments in Australia.

A third potential reason may be that there is not enough genetic variation in Australian red foxes to exhibit highly variable body mass and size, due to the founder effect of only a relatively small number of foxes being introduced into Australia in the 19th century (Rolls 1969). While there may not be a lot of variation in red foxes in Australia compared to global populations, due to the high fecundity and rapid colonisation of foxes post release, it has been suggested that there would be minimal loss of genetic variation from their British ancestors post-introduction, as a consequence of inbreeding or genetic drift (Lade et al. 1996). However, comparisons in genetic variation between native European and introduced red foxes in Australia are required to confirm this.

It has been previously suggested that morphological variation, or lack thereof, in populations of red foxes is a result of phylogenetic distance rather than geographical variation in environmental conditions (Cavallini 1995). As fox populations in this study were classed by geographic location, the effect of relatedness on variation in morphology was not examined. However it has been noted that the morphology of introduced red foxes in Australia is very similar to the British populations they are descended from (Cavallini & Lovari 1991), based on cluster analysis.

There were no significant differences in size or mass between urban red foxes reported in this study and non-urban foxes reported elsewhere in Australia, except for female non-urban red foxes being significantly longer than female urban foxes. Despite reporting variation in size and mass along a land use gradient, across a broader scale these trends were not apparent. There was also no difference in sexual dimorphism for any of the measurements amongst any of the classes of fox populations, hence similar degrees of sexual dimorphism are displayed in all the fox populations mentioned.

3.5.4 Implications for red fox management in urban areas of Australia

The results presented above have demonstrated that the body size and mass of red foxes in Australia increased along a land use gradient, towards urban areas. Increased body size in male red foxes in Bristol, United Kingdom, has been shown to increase territory sizes and numbers of litters sired, hence leading to increased reproductive success (Iossa et al. 2008). While similar effects were not demonstrated in females, increased body size of male red foxes in urban areas found in this study, by virtue of access to anthropogenic food sources, could lead to increased reproductive output of male foxes in urban environments. Increased body size in red foxes has also been shown to facilitate movement in and out of fragmented habitats in urban environments (Bateman & Fleming 2012; Gehring & Swihart 2003). Therefore, anthropogenic modifications to environments may be benefiting survival and reproductive success in introduced red foxes in Australia. This has not been directly examined yet in urban environments in Australia, and warrants further research.

If urban Australian environments are increasing the fitness of red foxes, this could possibly result in increased pressure on any naïve native prey species living in urban refugia. This reinforces the need to reduce the availability of anthropogenic food sources to introduced red foxes in urban environments of Australia, such as by sealing garbage bins and reducing access to food stores. However, further research is required on urban red foxes in Australia to determine whether morphology has the same effect on life history traits as in native populations of red foxes.

3.6 Conclusion This is the first time in Australia that the morphology of red foxes has been described across an urban land use gradient. Urban red foxes from this study were neither larger nor heavier than their conspecifics from populations within their natural distribution. Urban red foxes in this study were longer in some aspects of skeletal size than non-urban foxes reported in Australia. Within the Greater Sydney region, these trends were more apparent, as the skeletal size and body mass of red foxes increased along the land use gradient, however body condition did not vary across the gradient. This is also the first time in Australia where diet has been directly related to red fox morphology across an urban land use gradient. Red foxes that had consumed, and hence had access to, anthropogenic food were heavier and in better condition than foxes without access.

Here I have presented results that red foxes in areas of higher human population densities are larger than foxes from lower population densities. However, the skeletal size of red foxes did not vary with diet and I have attributed this to the sample of full grown adult foxes used for diet analysis in this chapter. Nutrition has a significant effect on the body size of animals, especially during periods of growth (Geist 1987). Thus, to confirm that diet composition during juvenile growth stages of red foxes in urban areas of Sydney is causing increased skeletal size, future analysis of juvenile fox diet is required, similar to Soulsbury et al. (2008).

Body mass and condition have a significant bearing on life history components in red foxes. Therefore, these findings reinforce the importance of restricting access by red foxes to anthropogenic food sources in urban areas of Australia, to reduce any benefits to the fitness of these introduced predators.

CHAPTER 4

CONCLUSION

4.1 Summary of main findings From the results presented in the previous chapters, it would appear that urban foxes in Australia consume less native species than non-urban foxes however there is still a considerable presence of native species in the diet of urban foxes. Foxes in urban areas in Sydney are supported by a wide range of food types available to them and hence are not limited by the availability of one prey source. No threatened species were reported in the diet of foxes in this study however, where locally present, threatened species in Sydney are subject to fox predation.

Foxes in urban areas consume more anthropogenic food than in non-urban areas and this potentially explains the trend of larger foxes in urban areas when compared to non-urban areas in the Greater Sydney region. Whilst urban foxes in Australia may not grow to the extent of native foxes in their natural distribution, they are still larger in some respects to non-urban foxes from elsewhere in Australia.

4.2 Implications for fox management in urban environments in Australia Whilst this study has revealed insights into the diet composition of urban foxes in Australia, as well as the effects of urbanisation on fox morphology, more research is required to determine if this has significant implications for the management of foxes in urban Australian environments. The potential implications discussed below are purely speculative at this point.

Whether the current level of predation on native species urban environments has the potential to impact them at the population level warrants further investigation. The predation paradox hypotheses proposed by Fischer et al. (2012) serve as a potential framework to analyse the impacts of fox predation on populations of native prey species in urban Australian environments.

Not only could anthropogenic food sources in urban Australian environments be supporting high densities of foxes, which in turn could result in increased predation rates on native prey, but access to anthropogenic food could be increasing the fitness of urban fox populations. It is yet to be determined whether the increased body mass and skeletal size of urban foxes in this study has effects on the life history and fitness of foxes, as seen in British populations (Iossa et al. 2008). Increased reproductive success and survival of urban foxes, as a consequence of access to anthropogenic food sources, could limit the effectiveness of fox control in urban areas if their abundance is resistant to lethal control.

Despite the absence of threatened species recorded in the diet of foxes this study, it is crucial that sites in Sydney containing isolated populations of endangered species continue to be listed as priority sites for fox management by government authorities. Even with high densities of foxes in urban environments, the impact one fox can have on a dwindling, isolated population of a threatened species can be disastrous.

Based on the considerable proportion of native species, such as ringtail possums, consumed in urban areas, access should be reduced to anthropogenic foods that are supporting populations of foxes in urban Australian environments. However, the effects of significantly reducing access to these subsidises needs to be tested, in case it results in prey switching to consuming more wildlife in urban areas.

4.3 Suggestions for future research There are still some questions that need to be answered to further increase our knowledge of urban foxes in Australia, in relation to their impact on native species as well as potential effects of urbanisation on fitness. Areas that require further investigation are highlighted below.

4.3.1 Diet analysis during growth

An analysis of the diet of cubs and juveniles could reveal implications for larger prey species in urban areas of Australia. Vixens in London have been recorded selectively eating smaller food items and taking back larger prey to their dens to feed their cubs (Harris 1981b). This has also been reported for foxes in parts of Sweden (Englund 1969). Thus the stomach analysis of any vixens in this study that were rearing cubs may have failed to highlight prey species that were killed by vixens but eaten by their cubs. The carcasses of two cubs from urban areas were provided for this study but their stomach contents not reported in the above analyses. One cub had an empty stomach and hence was probably still being weaned. However, the stomach of the other cub contained the remains of T. vulpecula and some herbaceous plant material. The possum remains were in the form of ingested tissue and hair, likely to have been from the carcass brought back to the den by the vixen, but also an ingested fox scat containing possum hair, likely to have been from the vixen as well. Hence further research is required to determine what prey items vixens are bringing back for their cubs to determine any further impacts on native species in urban areas. This could also be complemented by a camera collar study (see below).

4.3.2 Camera collars

It is also difficult to distinguish through analysis of stomach or scat contents whether prey items were hunted or scavenged as carrion. Likewise the prevalence of prey items may be underestimated if they are scavenging from open carcasses and not ingesting hair, for example deer (Davis et al. 2015). Future studies deploying animal- borne video and environmental data collection systems (AVEDs) (Moll et al. 2007) could overcome some of these limitations and reveal more fine scale data about fox predation in urban environments. AVEDs can also reveal information about surplus killing in carnivores or prey items eaten that may not show up in scat or gut content

analyses. For example, footage obtained by AVEDs on feral cats in northern Australia recorded high rates of predation on frogs (McGregor et al. 2015); however, the cats rarely ate frogs whole and often discarded the hard parts. Hence previous gut content analyses would underestimate predation on frogs and could explain the absence of amphibian remains found in this study if foxes predated upon frogs in a similar way. Other applications of AVED deployment on urban foxes could include examining how habitat structure affects hunting success, similar to McGregor et al. (2015); quantifying the number of animals each fox kills per night; as well as identifying prey items that vixens are bringing back for their cubs.

Initial research into developing a suitable camera collar design for foxes was undertaken during this project however further research is required to develop a model that can be deployed on foxes and capture sufficient data per deployment, whilst not affecting the behaviour of collared foxes (Moll et al. 2007; Moll et al. 2009a; Moll et al. 2009b). Limitations to overcome for a suitable design include minimising the weight of the device whilst also maximising battery life and enabling night vision on the camera. As the device is likely to be deployed on a fox in the morning after it has been trapped, a scheduling device is required to activate the camera at night time, as the battery is likely not to last more than a few hours. The scheduler could also be wired to a motion detector so the device is only able to be turned on when the fox is active.

4.3.3 Genetic studies

Genetic samples (hair and ear tissue) were also collected from all carcasses analysed in this study and stored in ethanol for future genetic analysis. Analysing the population genetics of foxes in the Greater Sydney region could reveal implications for fox management, such as the location of source and sink populations. Since urban areas support high densities of foxes (Harris & Rayner 1986; Marks & Bloomfield 1999) with an abundance of food sources, urban areas could be acting as source populations for foxes dispersing to non-urban areas surrounding Sydney. The converse could also be true, as demonstrated in Zurich with rural foxes immigrating into urban areas (Wandeler et al. 2003).

Gene flow appears to be limited between urban populations of foxes within Melbourne, Australia, due to a lack of corridors of suitable fox habitat (Robinson &

Marks 2001). It is yet to be determined where there are similar barriers to gene flow within Sydney. If this does not hold true, the lack of uniform fox management within Sydney could be creating source and sink populations within this region. For example, intensive fox management on the northern beaches of Sydney, where a large proportion of national parks, coastal heath and hence native species occur, could be encouraging foxes from surrounding less intensely managed areas to move in to new territories, vacated by the active removal of foxes through pest management.

4.3.4 Cats

The possibility exists that any potential impact of fox predation in urban environments is far outweighed by predation from feral and pet cats. In this study, it did not appear that foxes were frequently consuming more than one vertebrate per night. Cat predation in non-urban areas of Australia have been recorded as high as seven animals per night (McGregor et al. 2015). Comprehensive studies quantifying predation by free-ranging domestic cats in urban areas of Australia are lacking, but they estimate less than one native animal per night, on average (Barratt 1998). As cats are arboreal predators, they have access to a greater range of prey than foxes in urban environments. Hence it needs to be confirmed whether predation by cats in urban areas outweighs any potential impacts of foxes on native species.

APPENDICES

Appendix 2.1. Justification of land use categories

A land use gradient measurement was initially created using extracted population density values alone. However, in some cases the value returned did not accurately reflect the environment around those carcasses being considered as urban. For example, carcasses collected in golf courses, large urban parklands or even national parks adjacent to high density development returned low human population density values (sometimes even zero) as there were no humans recorded living within 1km2. Consequently, the sample of foxes appeared skewed towards low density areas (Fig. A1) although the majority of carcasses were collected in urban areas of Sydney (Fig. A2). Thus, land use categories were constructed to create the gradient, incorporating the extracted human population density values.

9000

)

2 8000

7000

6000

5000

4000

3000

2000

1000 Human population density (per km (per density population Human

0 20 40 60 80 100 120 140

nth red fox carcass

Figure A1. Distribution of 130 red fox carcasses in relation to human population density (1 km2).

Figure A2. Location of all carcasses (n = 130) collected in the Greater Sydney region used for diet analysis. Image created using Google Earth. It is important to note that during the period since the 2011 census, Sydney has undergone rapid growth and its population has increased accordingly (Australian Bureau of Statistics 2016). If the same analysis was repeated with 2016 census data, it would likely result in a shift of carcasses towards the high-density end of the gradient, in reflection of the recent population and housing growth across Sydney.

There has been a wide variety of methods employed by various studies to construct land use gradients (Theobald 2004). Other studies on the diet of urban foxes have examined their diet composition in relation to proximity from the city centre, for example London (Harris 1981b) and Zurich (Contesse et al. 2004). In these studies, the central location of the ‘city centre’ in relation to the surrounding landscape has enabled the collection of carcasses along an urban gradient in nearly all directions from the city centre (Fig. A3). However, Sydney is a coastal city and its central business district (CBD) is located next to Sydney Harbour and as such, the gradient is not present in all directions surrounding the city centre. Likewise, the gradient from urban to rural to natural areas only exists running east to west from the CBD to the Blue Mountains National Park (Fig. A3). To supplement the sample of foxes from natural areas, foxes were collected from national parks to the north and south of the CBD and from natural areas outlying the boundary of the Greater Sydney region. The national parks to the north and south of the CBD (such as the Royal National

Park, Garigal National Park and Ku-ring-gai Chase National Park) lie adjacent to human development; hence foxes collected from these natural areas did not fall on the ideal urban to natural land use gradient (running through rural areas).

Figure A3. Comparison of different cities used for urban land use gradient studies on red foxes. ● denotes the city centre in each figure. (a) London study area from Harris (1981) (image modified)- the outer line denotes the Greater London Council (GLC) boundary; ● denotes carcasses from inner zone (more than 5km within GLC boundary); ▪ denotes carcasses from outer zone (less than 5km within GLC boundary). 10km grid squares shown. (b) Zurich study area from (Gloor 2002)- white: rural area; light grey: urban area; blue: lakes and rivers; black line: border of municipality. (c) Greater Sydney region study area from this thesis, black line: border. Image: ArcGIS.

Appendix 2.2. List of vertebrates consumed by red foxes, according to location and Local Government Area (LGA). Councils listed include new amalgamated councils, formed in 2016 by the NSW State Government. n = number of individuals consumed; *no further description of location given; **collected on council borders; ***likely to have been killed by vixen.

LGA Location Fox Vertebrate n Bayside Council Eastlakes Golf Course F080 Eastern Snake-necked turtle eggs 2 Unidentified mammal 1 Bonnie Doon Golf Course F068 Unidentified bird 1 F069 Common ringtail possum 1 Bexley Golf Course F112 Unidentified vertebrate 1 Blue Mountains Blackheath catchment F120 Common ringtail possum 1 City Council Katoomba catchment F122 Unidentified bird 1 Blackheath F123 Bush rat 1 Camden Council Australian Botanic Gardens, F033 Eastern Snake-necked turtle 1 Mount Annan Canterbury Bankstown* F001 European hare 1 Bankstown Council F013 Black rat 1 Unidentified bird 1 F023 Unidentified bird 1 House mouse 1 F061 Unidentified bird 1 F076 Black rat 1 Bankstown Airport F082 Unidentified bird 1 Bankstown Golf Course F071 Unidentified fish 1 F073 Black rat 1 Chullora Resource Recovery Park F066 Unidentified bird 1 (Bankstown tip) Kelso Park, Bankstown F012 Pacific Black Duck 1 House mouse 1 City of Lithgow Hartley F086 Unidentified bird 1 Council City of Parramatta Sydney Olympic Park F040 Common ringtail possum 1 Council F078 Magpie lark 1 F041 Unidentified bird 1 Toongabie Creek F114 Unidentified bird 1 House mouse 1 F116 Brown quail 1 House mouse 1 Cumberland Auburn Botanic Gardens F030 Unidentified bird 1 Council Auburn F009 Unidentified vertebrate 1 F077 House mouse 1 Fairfield City Calmsley Hill City Farm F011 Unidentified vertebrate 1 Council

Liverpool City Warwick Farm F059 Unidentified bird 1 Council F057 Red whiskered bulbul 1 North Sydney Berry Island Reserve, F020 Black rat 1 Council Wollstonecraft Northern Beaches Allambie F014 European rabbit 1 Council Cromer Golf Course F067 European rabbit 1 F074 European rabbit 1 F084 Common brushtail possum 1 F085 Common ringtail possum 1 Unidentified bird 1 Elanora Golf Course F055 Black rat 1 Brown thornbill 1 Elanora Heights F060 Unidentified bird 1 Terrey Hills F034 Swamp wallaby 1 Warriewood F102 Unidentified bird 1 West Head, Ku-ring-gai Chase F128 Swamp wallaby 1 National Park Randwick Council Latham Park, Maroubra F005 Black rat 1 Malabar F007 Common brushtail possum 1 F006 Dusky Moorhen 1 Randwick Council/ Centennial Parklands, Moore Park F088 Common brushtail possum*** 1 Waverley (cub) Scat- Common brushtail possum*** 1 Council** Sutherland Shire Bundeena F104 Unidentified vertebrate 1 Council Lucas Heights Tip F064 House mouse 1 Menai F031 Unidentified bird 1 F032 House mouse 1 The Council of the Royal Botanic Gardens, Sydney F046 Common ringtail possum 1 City of Sydney The Hills Shire Baulkham Hills F054 Domestic chicken 1 Council Common ringtail possum 1 Castle Hill GC F038 Dusky Moorhen 1 Black rat 1 Willoughby Council Willoughby F024 Unidentified bird 1 Wingecarribee Upper Nepean catchment F134 Unidentified mammal 1 Shire F137 Common ringtail possum 1 F139 Unidentified bird 1 F140 Common ringtail possum 1 Bush rat 1 House mouse 1 Wollondilly Shire Elizabeth Macarthur Agricultural F093 Brown rat 1 Council Institute (EMAI), Menangle Mulgoa F090 Unidentified vertebrate 1

Appendix 3.1. Morphological measurements of different red fox populations as reported by different studies with summary of combined sample size, mean and standard deviation for each class: (a) body mass, (b) nose to tail base length, (c) body length, (d) hind foot length. Classes: Native range = natural distribution, Australian = non-native distribution; NU = non-urban, U =

Urban. Values: n = sample size, x̅ = reported mean, SD = reported standard deviation, ncomb = combined sample size, x̅comb = combined mean, σcomb = combined standard deviation. Study number - Reference: 1. (Hattingh 1956), 2. (Kolb & Hewson 1974), 3. (Kolb 1978), 4. (Fairley 1970), 5. (Travaini & Delibes 1995), 6. (Gortazar et al. 2000), 7. (Gomes & Valente 2016), 8. (Cavallini 1995), 9. (Hoffman & Kirkpatrick 1954), 10. (Storm et al. 1976), 11. (Takeuchi 2010), 12. (Iossa et al. 2008), 13. (Winstanley et al. 1998), 14. (McIntosh 1963b), 15. (Read & Bowen 2001), 16. (Meek & Saunders 2000), 17. (Berghout 2000), 18. This study.

Appendix 3.1 continued…

(a) Population Class (Study no.) Body mass (kg) Male Female Sexual dimorphism

n x̅ SD n x̅ SD n x̅푑푖푓푓 SD England (1) Native range: NU 40 6.6 0.6 34 5.4 0.7 74 1.3 0.9

Scotland (2) Native range: NU 39 7.3 0.9 30 6.2 0.9 69 1.1 1.1

Scotland (3) Native range: NU ------

Ireland (4) Native range: NU 207 6.9 1.6 281 5.8 1.3 488 1.1 0.4

Spain (5) Native range: NU 64 6.3 1.0 60 5.1 0.9 124 1.2 0.7

Spain (6) Native range: NU 160 6.2 1.0 175 5.2 0.9 335 1.0 0.4

Portugal (7) Native range: NU 181 6.7 1.1 155 5.7 0.9 336 1.0 0.5

Italy (8) Native range: NU 204 5.8 13.6 123 4.9 7.5 327 0.8 1.1

Indiana (US) (9) Native range: NU 47 5.3 0.5 52 4.2 0.5 99 1.0 0.6

Illinois (US) (10) Native range: NU 46 5.0 0.9 37 4.1 0.5 83 1.0 0.7

Iowa (US) (10) Native range: NU 106 4.7 0.7 90 3.8 0.6 196 0.9 0.4

Tochigi (JAP) (11) Native range: NU 17 5.1 0.8 17 4.4 1.0 34 0.7 1.1

Bristol, UK (12) Native range: U 69 6.4 1.9 58 5.5 5.1 127 0.8 0.8

Orange, NSW (AUS) (13) Australian: NU 86 5.9 0.8 84 4.9 0.7 170 1.0 0.5

Canberra district, ACT/NSW Australian: NU 84 6.3 0.8 60 5.5 5.6 144 0.8 0.7 (AUS) (14) Roxby Downs, SA (AUS) (15) Australian: NU 57 4.9 1.1 26 4.3 0.6 83 0.6 0.9

Jervis Bay, NSW (AUS) (16) Australian: NU 9 5.4 0.7 5 4.5 0.9 14 0.9 2.0

Murringo, NSW (AUS) (17) Australian: NU 12 5.4 0.7 24 4.9 0.5 36 0.5 1.0

Greater Sydney region (excl. Australian: NU 19 5.3 0.8 12 4.5 0.4 31 0.8 1.3 Sydney), NSW (AUS) (18) Sydney, NSW (AUS) (18) Australian: U 53 5.9 0.9 31 4.9 0.8 84 1.0 0.9

SUMMARY 푛 x̅ 휎 푛 x̅ 휎 푛 x̅ 휎 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏

Native range: Non-urban 1111 6.1 6.0 1054 5.2 2.8 2165 1.0 0.7

Native range: Urban 69 6.4 1.9 58 5.5 5.1 127 0.8 0.8

Australian: Non-urban 267 5.7 1.0 211 4.9 3.0 478 0.8 0.9

Australian: Urban 53 5.9 0.9 31 4.9 0.8 84 1.0 0.9

Appendix 3.1 continued…

(b) Population Class NTB (mm) (Study no.) Male Female Sexual dimorphism

n x̅ x̅푑푖푓푓 x̅푑푖푓푓 x̅ SD n x̅푑푖푓푓 SD

Scotland (2) Native range: NU 39 712.0 22.0 30 679.0 30.0 69 33.0 124.0

Scotland (3) Native range: NU 329 726.9 25.2 391 680.4 24.5 720 46.5 34.4

Ireland (4) Native range: NU 42 723.0 25.9 42 677.0 25.9 84 46.0 104.5

Spain (5) Native range: NU 65 712.0 36.0 57 659.0 29.0 122 53.0 87.4

Spain (6) Native range: NU 186 687.2 44.4 201 647.2 38.4 387 40.0 45.8

Portugal (7) Native range: NU 181 722.3 45.7 155 683.7 34.9 336 38.6 55.0

Italy (8) Native range: NU 193 657.0 541.8 116 620.0 387.7 309 37.0 69.5

Tochigi (JAP) (11) Native range: NU 60 648.0 36.0 46 614.0 32.0 106 34.0 90.6

Orange, NSW (AUS) (13) Australian: NU 86 667.0 36.2 84 633.0 33.0 170 34.0 69.2

Murringo, NSW (AUS) (17) Australian: NU 12 679.0 55.4 24 656.0 44.1 36 23.0 134.9

Greater Sydney region (excl. Australian: NU 19 622.5 33.0 13 582.5 36.4 32 40.0 161.7 Sydney), NSW (AUS) (18)

Sydney, NSW (AUS) (18) Australian: U 60 651.3 39.9 35 616.9 37.2 95 34.4 104.4

SUMMARY 푛 x̅ 휎 푛 x̅ 휎 푛 x̅ 휎 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 Native range: Non-urban 1095 701.2 231.6 1038 663.4 134.9 2133 42.0 61.3

Australian: Non-urban 117 661.0 41.9 121 632.1 40.8 238 33.1 98.5 Australian: Urban 60 651.3 39.9 35 616.9 37.2 95 34.4 104.4

Appendix 3.1 continued…

n x̅ x̅푑푖푓푓 x̅푑푖푓푓 x̅ SD n x̅푑푖푓푓 SD

England (1) Native range: NU 33 1027.3 241.3 31 983.2 168.4 64 44.1 181.5

Illinois (US) (10) Native range: NU 46 1028.5 59.7 37 966.0 47.4 83 62.5 159.1

Iowa (US) (10) Native range: NU 106 999.0 49.9 90 946.0 65.9 196 53.0 99.8

Tochigi (JAP) (11) Native range: NU 57 1022.0 52.0 44 971.0 48.0 101 51.0 146.5

Canberra district, ACT/NSW Australian: NU 84 1046.7 43.0 60 1001.7 38.5 144 45.0 129.4 (AUS) (14)

Greater Sydney region (excl. Australian: NU 19 1019.0 50.7 13 958.2 61.3 32 60.8 266.0 Sydney), NSW (AUS) (18)

Sydney, NSW (AUS) (18) Australian: U 55 1039.6 56.1 32 987.3 57.5 87 52.2 174.7

SUMMARY 푛 x̅ 휎 푛 x̅ 휎 푛 x̅ 휎 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏

Native range: Non-urban 242 1013.9 102.6 202 960.8 86.1 444 53.0 137.1

Australian: Non-urban 103 1041.6 45.8 73 994.0 46.5 176 47.9 163.1 Australian: Urban 55 1039.6 56.1 32 987.3 57.5 87 52.2 174.7

Appendix 3.1 continued…

(d) Population Class Hind foot length (mm) (Study no.) Male Female Sexual dimorphism

n x̅ SD n x̅ SD n x̅푑푖푓푓 SD

England (1) Native range: NU 41 136.0 46.4 35 133.1 30.1 76 2.8 23.6 Scotland (2) Native range: NU 39 167.0 7.0 30 159.0 6.0 69 8.0 29.1

Ireland (4) Native range: NU 42 161.0 13.0 42 151.0 6.5 84 10.0 23.4

Spain (5) Native range: NU 65 157.0 7.0 61 145.0 6.0 126 12.0 18.6

Portugal (7) Native range: NU 181 154.0 9.4 155 143.9 7.5 336 10.1 11.6

Illinois (US) (10) Native range: NU 46 166.0 11.9 37 157.5 13.4 83 8.5 26.0

Iowa (US) (10) Native range: NU 106 158.5 12.9 90 146.0 12.3 196 12.5 15.4

Tochigi (JAP) (11) Native range: NU 23 14.9 7.0 16 14.1 7.0 39 0.8 3.8

Orange, NSW (AUS) (13) Australian: NU 86 148.0 7.4 84 138.0 6.4 170 10.0 15.1 Canberra district, ACT/NSW Australian: NU 84 153.3 6.0 60 146.4 6.7 144 6.9 18.9 (AUS) (14) Greater Sydney region (excl. Australian: NU 21 152.6 6.0 13 142.4 6.1 34 10.2 39.5 Sydney), NSW (AUS) (18) Sydney, NSW (AUS) (18) Australian: U 60 152.7 6.2 35 144.7 6.3 95 8.0 24.5

SUMMARY 푛 x̅ 휎 푛 x̅ 휎 푛 x̅ 휎 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏 푐표푚푏

Native range: Non-urban 543 150.5 33.5 466 141.9 27.6 1009 9.6 18.6

Australian: Non-urban 191 150.8 7.2 157 141.6 7.6 348 8.7 20.3

Australian: Urban 60 152.7 6.2 35 144.7 6.3 95 8.0 24.5

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