Parental Care in Urban San Joaquin Kit Foxes (Vulpes Macrotis Mutica): Relative Roles of Parents and Helpers

PARENTAL CARE IN URBAN SAN JOAQUIN KIT FOXES (VULPES MACROTIS MUTICA): RELATIVE ROLES OF PARENTS AND HELPERS

Tory Lynn Westall

A Thesis Submitted to the Department of Biology California State University, Bakersfield In partial fulfillment of the Degree of Master of Science

Spring 2015

Tory Lynn Westall

2015

Parental Care in Urban San Joaquin Kit Foxes (Vulpes macrotis mutica): Relative Roles of Parents and Helpers

Tory L. Westall

This thesis has been accepted on behalf of the Department of Biology by their supervisory committee:

Parental Care in Urban San Joaquin Kit Foxes (Vulpes macrotis mutica): Relative Roles of Parents and Helpers

Tory L. Westall

Department of Biology, California State University, Bakersfield

ABSTRACT

The San Joaquin kit fox (Vulpes macrotis mutica) is an endangered species endemic to the San Joaquin Desert in the Central Valley of California. Much of the habitat in the San

Joaquin Desert has been converted for agricultural, industrial, and urban development. The remaining San Joaquin kit foxes exist as a meta-population in several satellite populations and three core areas, the Panoche Valley, the Carrizo Plain, and western Kern County.

Another substantial population that could be considered a core area is the urban population that is living in the City of Bakersfield. This population is fairly large and critical in contributing to the conservation of the species as a whole. The urban population of San

Joaquin kit foxes has higher survival rates, lower dispersal potential, and higher reproductive success as well as increased incidence of philopatric young and larger family groups when compared to populations living in natural areas. The San Joaquin kit fox is a socially monogamous species, but philopatric young have been classified as Helpers because they assist in rearing future litters. Understanding how the altered ecosystem in the urban environment can affect reproductive traits of an endangered species is important for conservation. In this study I investigated the relative contributions of adult group members to pup rearing in urban San Joaquin kit foxes. My objectives were to quantify the relative time contributions of each individual, the different tasks performed by each individual, and the changes in time contributions and tasks performed by each individual as the pups aged.

To quantify den attendance and behavior, I used proximity logging collars and base stations at each natal den, performed direct observations of behaviors, and set up remote camera stations at dens. I also compared these methods for efficiency in detecting behaviors. To determine role, I used behaviors and genetic analyses to classify each individual to one of three categories: Mother, Father, or Helper. To monitor changes in behavior as pups aged, I split the breeding season into three periods: Preparturition, Nursing, and Weaned. I monitored six groups at four locations in Bakersfield, California and had four groups that successfully reproduced and were consistently monitored. I found that proximity logging collars were unreliable in measuring den attendance of kit foxes. Cameras were an effective method for documenting behaviors, but they significantly underestimated the amount of time that foxes spent at the den. Direct observations were the most accurate method of gathering behavioral data and were used for analyses of parental care. I found that Mothers play a critical role in pup rearing. Mothers spend significantly more time at the den than either

Fathers or Helpers. While Fathers spend most of their time away from the den, they provision the same amount of food as Mothers, whereas Helpers provisioned significantly less than either Mothers or Fathers. Mothers primarily groomed young, provisioned, guarded while young played, and performed den defense. Fathers primarily provisioned and provided den defense. Helpers mostly interacted with the pups through play, which may teach the pups the social hierarchy and establish dominance. While Helpers do not provide direct care to young, they may provide a form of insurance of parental care of young should something happen to either of the parents. Helpers are likely tolerated within their natal range because there is an increased abundance of food within the urban environment and their presence is not detrimental to the success of the current litter. I also documented two incidences of

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social polygyny and genetic polyandry over the course of my study. This is likely tied to the super abundance of resources because more plentiful resources result in a decreased need for paternal care and so one male can split his time between multiple litters. My results indicate that there is a decreased need for assistance in pup rearing in the urban environment due to the increased resources available. Helpers do not actually help in rearing pups and Fathers are not as necessary to successful pup rearing. Mothers play an essential role in pup rearing and are necessary for successful reproduction in the urban environment.

ACKNOWLEDGEMENTS

I would like to thank my advisors Dr. David Germano and Dr. Brian Cypher for all the encouragement and support they have provided over the years. It was Dr. Germano’s passion in ecology that made me want to pursue this career and academic path and I will always be grateful. Dr. Cypher has been an amazing mentor and given me so many opportunities to expand my knowledge and experience in ecology. I also thank my advisor

Dr. Carl Kloock for his input, advice, and review of my thesis research. I sincerely thank Dr.

Katherine Ralls for supporting my project with ideas, equipment, lab work, and references.

I would like to thank all the individuals who made the work for this project possible.

First, I would like to thank my husband, Scott Westall for his assistance in field work as well as all the love and moral support he has provided over the years. I would also like to thank my grandparents, Stuart and Sandy Soles, for always pushing me to be better and instilling the work ethic and values that have allowed me to get to this point. I would like to thank all the Endangered Species Recovery Program staff who assisted in trapping and data analyses, as well as providing equipment, maps, pictures, and support: Christine Van Horn Job, Erica

Kelly, Allie Madrid, and Scott Phillips. I also couldn’t have done this without the help of all the individuals who volunteered their time and provided moral support, Christopher Reedy,

Katherine Reedy, Rainey Reedy, Erin Tennant, and Elizabeth de la Rosa.

Finally, this project would not have been possible without the financial support provided by the Bureau of Land Management for refurbishment of collars, the Smithsonian

Institution for purchasing cameras, and The Western Section and The San Joaquin Chapter of

The Wildlife Society and the Student Research Scholars Program of California State

University, Bakersfield, for student grants.

TABLE OF CONTENTS

CHAPTER 1. INTRODUCTION ...... 1

LITERATURE CITED ...... 12

CHAPTER 2. A COMPARISON OF METHODS FOR MONITORING BEHAVIOR OF URBAN SAN JOAQUIN KIT FOXES (VULPES MACROTIS MUTICA) ...... 16

INTRODUCTION ...... 17

METHODS ...... 18

RESULTS ...... 21

ACKNOWLEDGEMENTS ...... 25

LITERATURE CITED ...... 25

CHAPTER 3. PARENTAL CARE IN URBAN SAN JOAQUIN KIT FOXES (VULPES MACROTIS MUTICA): RELATIVE ROLES OF ADULT GROUP MEMBERS IN PUP REARING ...... 28

METHODS ...... 33 Study Area...... 34 Field Methods ...... 34 Statistical Analysis ...... 37

RESULTS ...... 38

DISCUSSION ...... 44

ACKNOWLEDGEMENTS ...... 49

LITERATURE CITED ...... 49

CHAPTER 4. OBSERVATIONS OF COMMUNAL LITTERS IN URBAN SAN JOAQUIN KIT FOXES (VULPES MACROTIS MUTICA) ...... 67

ABSTRACT...... 68

METHODS ...... 71

RESULTS ...... 73

DISCUSSION ...... 75

ACKNOWLEDGEMENTS ...... 79

LITERATURE CITED ...... 79

CHAPTER 5. SUMMARY OF RESEARCH AND CONSERVATION IMPLICATIONS...... 91 Behavioral Survey Methods ...... 91 Relative Roles of Adult Group Members to Pup Rearing ...... 92

Communal Litters ...... 94 Conservation Implications...... 95

LITERATURE CITED ...... 96

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LIST OF TABLES

CHAPTER 3

Table 1. Number of nights observations that were conducted on each San Joaquin kit fox (Vulpes macrotis mutica) family group during each period of the breeding season in Bakersfield, California during 2011 and 2012...... 55 Table 2. Number of group members observed in each San Joaquin kit fox (Vulpes macrotis mutica) family group in Bakersfield, California during 2011 and 2012...... 56 Table 3. Post-hoc tests analyzing differences in proportion of time spent performing specific behaviors within roles of San Joaquin kit foxes (Vulpes macrotis mutica) in Bakersfield, California, during the 2011 and 2012 breeding seasons. P values in bold are significant...... 57 Table 4. Primary roles that were observed most often performing different care behaviors in urban San Joaquin kit fox (Vulpes macrotis mutica) family groups during the 2011 and 2012 breeding seasons...... 59

CHAPTER 4

Table 1. Individuals in each socially polygynous San Joaquin kit fox (Vulpes macrotis mutica) group during the 2012 breeding season in Bakersfield, California...... 83 Table 2. CERVUS likelihood of maternity and paternity of San Joaquin kit fox (Vulpes macrotis mutica) pups from the CSUBS group at California State University, Bakersfield, during the 2012 breeding season...... 84 Table 3. CERVUS likelihood of maternity and paternity of San Joaquin kit fox (Vulpes macrotis mutica) pups from the BC2012 group at Bakersfield College during the 2012 breeding season...... 85

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LIST OF FIGURES

CHAPTER 1

Figure 1. San Joaquin kit fox on the Carrizo Plain, San Luis Obispo County, California. (Photograph taken by T. Westall, California State University, Stanislaus, Endangered Species)...... 5 Figure 2. Historic range of the San Joaquin kit fox (Vulpes macrotis mutica) in the San Joaquin Valley, California. Locations from the California Natural Diversity Database (CNDDB). (Map prepared by Scott Phillips, California State University, Stanislaus, of the Endangered Species Recovery Program)...... 6 Figure 3. Existing natural habitat that supports populations of San Joaquin kit fox (Vulpes macrotis mutica). A) Western Kern County; B) Bena Landfill; C) Northern Semitropic Ridge Ecological Reserve; D) Carrizo Plain. (Photographs taken by C. Van Horn Job, California State University, Stanislaus, Endangered Species Recovery Program)...... 7 Figure 4. Existing urban habitats that support family groups of San Joaquin kit foxes (Vulpes macrotis mutica). A) Undeveloped lot; B) Bakersfield City sump; C) Bakersfield College; D) Industrial lot. (Photos taken by T. Westall, California State University, Stanislaus, Endangered Species Recovery Program)...... 9

CHAPTER 3

Figure 1. Site locations for urban San Joaquin kit fox (Vulpes macrotis mutica) families monitored during 2011 and 2012 in Bakersfield, California...... 60 Figure 2. Mean and standard error for time spent at the den by San Joaquin kit foxes (Vulpes macrotis mutica) during the 2011 and 2012 breeding seasons...... 60 Figure 3. Average proportion of time spent by San Joaquin kit foxes (Vulpes macrotis mutica) in the den, at the den providing care, or at the den not providing care by role in Bakersfield, California during the 2011 and 2012 breeding seasons...... 60 Figure 4. Average proportion of time spent by San Joaquin kit foxes (Vulpes macrotis mutica) in the den, at the den providing care, or at the den not providing care by period during the 2011 and 2012 breeding seasons in Bakersfield, California...... 60 Figure 5. Provisioning counts during each period of the breeding season and the total number of provisioning events by role for San Joaquin kit foxes (Vulpes macrotis mutica) in Bakersfield, California during 2011 and 2012...... 60 Figure 6. A series of remote camera photos showing a non-native red fox (Vulpes velox) visiting a San Joaquin kit fox (V. macrotis mutica) natal den (upper left), a kit fox Father aggressively defending the natal den ( upper right and lower left), and the red fox leaving the den area (lower right)...... 60

CHAPTER 4

Figure 1. Size difference in two age classes of San Joaquin kit fox (Vulpes macrotis mutica) pups representing two litters at the same den taken from a camera station at California State University, Bakersfield during the 2012 breeding season. The kit fox in the background is a dye marked and collared adult male fox...... 86 Figure 2. Pictures of both mothers from the San Joaquin kit fox (Vulpes macrotis mutica) family group at California State University, Bakersfield during the 2012 breeding season. A) Female 6309 showing enlarged teats and hair loss from nursing; B) Female 6700 showing enlarged teats and rufus belly fur from nursing; C) Female 6700 nursing the younger litter of pups on the night of April 1, 2012 (pups are standing on their back feet); D) Female 6700 nursing pups from the older litter on the night of April 1, 2012 (pups are sitting fully on the ground and leaning to nurse)...... 86 Figure 3. A picture captured on a remote camera of both San Joaquin kit fox (Vulpes macrotis mutica) mothers showing signs of nursing at Bakersfield College during the 2012 breeding season. . 86 Figure 4. A picture captured by remote camera showing nine out of 10 San Joaquin kit fox (Vulpes macrotis mutica) pups at Bakersfield College during the 2012 breeding season...... 90

CHAPTER 1

INTRODUCTION

Group living and cooperative breeding are common themes in canid ecology

(Macdonald and Sillero-Zubiri 2004). Family groups of North American foxes typically consist of a mated pair and their current offspring, as well as any delayed dispersers that have remained in their natal range (Moehlman 1989, Ralls and White 2003, Kitchen et al. 2005,

Cypher 2010). In kit foxes (Vulpes macrotis), mated pairs are not often closely related (Ralls et al. 2001), though female members of adjacent groups typically are, indicating an extended social network (Ralls and White 2001, Ralls and White 2003, Wayne et al. 2004). Kit fox delayed dispersers, or helpers, tend to be female (Ralls et al. 2001, Cypher 2003, Macdonald and Sillero-Zubiri 2004), though they can be both sexes (Macdonald et al. 2004). A tendency toward female helpers is also common in red foxes (V. vulpes; Cypher 2003, Soulsbuy et al.

2010), swift foxes (V. velox; Cypher 2003, Poessel and Gese 2013), and arctic foxes (Alopex lagopus; Moehlman 1989, Cypher 2003) and is thought to be related to body size (Moehlman

1989, Macdonald and Sillero-Zubiri 2004).

In foxes, helpers typically do not breed due to reproductive suppression by the dominant female (Macdonald et al. 2004). Helpers are related to one of the breeding pair and can provide food and care to the breeding female and her offspring (Ralls et al. 2001, Cypher

2003, Wayne et al. 2004, Cypher 2010, Elmhagen 2014). Increased parental care has been associated with helpers in black-backed jackals (Canis mesomelas), Ethiopian wolves (C. simensis), African wild dogs (Lycaon pictus; Macdonald et al 2004), golden jackals (C. aureus), bat-eared foxes (Otocyon megalotis; Moehlman 1989), red foxes (Soulsbury et al.

2010), swift foxes (Poessel and Gese 2013), and arctic foxes (Elmhagen et al. 2014). Helpers are known to increase pup survival (Moehlman 1989) and decrease the parental care investment of the breeding female, which increases her lifetime reproductive success

(Macdonald et al. 2004). Other benefits to the alpha female include more food for her offspring, increased predator surveillance and defense, more time for her to forage while helpers guard offspring, subordinate females to take over care of her pups if she should die, and assurance that her kin will inherit her territory (Moehlman 1989). The subordinate female(s) benefit from staying in a known territory, kin investment, and potentially becoming the breeding female and inheriting their natal range, as well as training in pup rearing

(Moehlman 1989).

The most influential factor in determining group formation and size is prey availability (Moehlman 1989, Spiegel and Tom 1996, Cypher et al. 2000). Kit foxes are opportunistic feeders, though they prefer to eat kangaroo rats (Dipodomys spp.) and pocket mice (Perognathus spp. and Chaetodipus spp.; Morrell 1972, Moehrenschlager et al. 2004).

Natural populations of kit foxes follow the fluctuating prey availability that results from erratic rainfall patterns in a desert habitat (Cypher 2010). Years of low rainfall, and thus low prey availability, have resulted in reduced reproductive success for kit foxes (Cypher et al.

2000). On the other hand, when resources are abundant within a territory, a home range may be able to support additional individuals and groups are formed (Moehlman 1989,

Macdonald et al. 2004). During years of abundant food availability, survival rates and reproductive rates are higher (Warrick et al. 1999). This same pattern can be observed in other fox species as well. In populations of arctic foxes that are reliant on cyclic rodent populations, groups tend to form following increases in the rodent population (Elmhagen et

al. 2014). In contrast, coastal populations of arctic foxes that rely on a stable food source derived from the ocean do not form groups larger than a breeding pair (Elmhagen et al.

2014). Red foxes also are known to form groups when rodent and leporid populations are high (Cypher 2003).

Kit foxes are small tan to gray canids with relatively large ears, long slender legs, and a long, bushy, black-tipped tail (Morrell 1972, USFWS 1998, Cypher 2010). The core population is found in northwestern Mexico and the southwestern United States (Waithman and Roest 1977, Cypher 2010), though they are also found in small numbers as far north as southern Oregon and Idaho (Moehrenschlager et al. 2004). Kit foxes typically inhabit arid and semiarid habitats including desert scrub, chaparral, and native and non-native grasslands

(Macdonald and Sillero-Zubiri 2004, Moehrenschlager et al. 2004, Cypher 2010). Unlike most canids which only use dens for pup rearing, kit foxes are unusual because they use earthen or subterranean dens every day of their life (Koopman et al. 1998, Moehrenschlager et al. 2004, Cypher 2010). Dens are used to escape predators, to avoid temperature extremes and water loss, for diurnal resting, and for pup rearing (Ralls and White 2003,

Moehrenschlager et al. 2004, Cypher 2010). Kit foxes typically have multiple dens within their home range that are maintained by family groups (Morrell 1972, Ralls and White 2003).

Kit foxes are mostly monogamous, with occasional cases of polygyny and they generally mate for life (Spiegel and Tom 1996, Moehrenschlager et al. 2004, Ralls et al.

2007, Cypher 2010). They mate in late November to early December and young are born from late January to early March (Morrell 1972, Moehlman 1989, Macdonald and Sillero-

Zubiri 2004, Moehrenschlager et al. 2004, Cypher 2010). Litters consist of 1-9 pups with an average of four per pair (Moehrenschlager et al. 2004, Ralls et al. 2007). Pups emerge from

the den at four weeks, are weaned at eight weeks, and become independent at 5-6 months

(Morrell 1972, Moehrenschlager et al. 2004, Ralls et al. 2007). At independence, young will disperse or choose to delay dispersal and continue to occupy their natal ranges (Ralls et al.

2001, Ralls et al. 2007, Cypher 2010).

There are two distinct subspecies of kit fox, the desert kit fox (V. m. arsipus) and the

San Joaquin kit fox (V. m. mutica; Waithman and Roest 1977, Moehrenschlager et al. 2004,

Wayne et al. 2004). The San Joaquin kit fox (Fig. 1) is located in the San Joaquin Desert of

California and is topographically and genetically isolated from the kit fox population east of the Sierra Nevada (Moehrenschlager et al. 2004). While desert kit fox populations have been increasing in most of the western states, the population of foxes in the San Joaquin Desert has been in decline (Moehrenschlager et al. 2004).

Figure 1. San Joaquin kit fox on the Carrizo Plain, San Luis Obispo County, California. (Photograph taken by T. Westall, California State University, Stanislaus, Endangered Species).

Historically, the San Joaquin kit fox ranged from the southern San Joaquin Valley in

California north to Tracy and from the Coastal Range on the west to the Sierra Nevada on the east (Fig. 2; USFWS 1998, Wayne et al. 2004). Extensive habitat loss has been occurring within the historic range of San Joaquin kit foxes for decades. By 1958 approximately 50% of the original natural communities in the valley had been lost, degraded, or fragmented due to conversion by agricultural and industrial developments, urbanization, and water flow alterations (USFWS 1998, Smith et al. 2006).

Figure 2. Historic range of the San Joaquin kit fox (Vulpes macrotis mutica) in the San Joaquin Valley, California. Locations from the California Natural Diversity Database (CNDDB). (Map prepared by Scott Phillips, California State University, Stanislaus, of the Endangered Species Recovery Program).

Many existing habitat patches (Fig. 3) are too small and isolated to support a kit fox home range and San Joaquin kit foxes are extremely rare or even absent from parts of their northern range (Smith et al. 2006, Cypher 2013). As a result, the San Joaquin kit fox has been federally listed as Endangered by the U.S. Fish and Wildlife Service (USFWS) and state-listed as Threatened by the California Department of Fish and Wildlife (CDFW) due to habitat loss caused by human impacts (Morrell 1972, USFWS 1998, Cypher et al. 2013).

Figure 3. Existing natural habitat that supports populations of San Joaquin kit fox (Vulpes macrotis mutica). A) Western Kern County; B) Bena Landfill; C) Northern Semitropic Ridge Ecological Reserve; D) Carrizo Plain. (Photographs taken by C. Van Horn Job, California State University, Stanislaus, Endangered Species Recovery Program).

As a result of habitat fragmentation, San Joaquin kit foxes exist in a meta-population consisting of several small satellite populations and three core populations located in Western

Kern County, the Carrizo Plain, and the Panoche Valley (Cypher et al. 2013). A potential fourth core population exists in the form of an urban population of San Joaquin kit foxes. A large number of San Joaquin kit foxes are known to reside in Taft, Coalinga, and Bakersfield

(Cypher and Frost 1999, Cypher 2010). While Taft and Coalinga are small cities that are

surrounded by kit fox habitat, Bakersfield is a large city with only 25-30% of its limits abutting natural habitat (Cypher 2010). As a result, Bakersfield has a substantial population of San Joaquin kit foxes living entirely within the city (Smith et al. 2006, Cypher 2010). The urban environment is an altered environment full of processes that are very different from those of natural habitats (Gehrt 2010). Investigating the differences between urban and nonurban populations of San Joaquin kit foxes is important to developing conservation strategies that protect the species as a whole.

The areas inhabited by kit foxes in an urban setting are very different from the desert habitat in which they are typically found. In an urban landscape, foxes will use undeveloped land, sumps, industrial areas, manicured lawns, and linear rights of way (Fig. 4; Cypher

2010). Many features and land uses in the urban environment prevent movement between habitable patches and result in a smaller home range for urban foxes (Frost 2005, Cypher

2010). For instance, kit foxes will not readily travel through or inhabit heavily residential areas that make up large portions of the city (Frost 2005). Availability of dens can also be a limiting factor; however, kit foxes are known to use atypical or man-made dens (Spiegel and

Tom 1996, Moehrenschlager et al. 2004, Cypher 2010). Natal dens, those used for

Figure 4. Existing urban habitats that support family groups of San Joaquin kit foxes (Vulpes macrotis mutica). A) Undeveloped lot; B) Bakersfield City sump; C) Bakersfield College; D) Industrial lot. (Photos taken by T. Westall, California State University, Stanislaus, Endangered Species Recovery Program).

reproduction, tend to be earthen dens (Spiegel and Tom 1996) and the urban population may be limited by the lack of suitable earthen dens.

In urban areas presence of helpers occurs at a higher frequency as a result of higher survival rate, restricted dispersal potential, and an overabundance of food and water (Cypher

2010). Like natural kit foxes, urban foxes prefer to eat rodents and insects, though they primarily feed on gophers, squirrels, mice, rats, beetles, cockroaches, and grasshoppers

(Cypher 2010). The presence of anthropogenic food sources (trash, pet food, handouts, etc.) allows for a larger carrying capacity in smaller patches (Frost 2005, Cypher 2010). As a result of increased food availability, urban foxes have higher reproductive rates (Cypher and

Frost 1999, Cypher 2010) and lower mortality rates than kit foxes in natural habitats (Frost

2005). Given that prey availability is the most influential factor in determining group formation and size, it is no surprise that there are more cases of delayed dispersal in the urban environment than in natural areas, and even cases of older foxes helping offspring (Cypher

2010). Urban populations of red foxes also show an increase in the number of groups with helper foxes (Soulsbury et al. 2010). In some urban settings, when resources are very abundant, red fox populations switch from monogamy to polygyny and subordinate females will reproduce and raise their pups communally with the litter of the dominant female

(Soulsbury et al. 2010). In natural populations of canids, helpers have been shown to increase reproductive success and pup survival (Moehlman 1989); however, the occurrence of helpers is infrequent. Looking at the role of helpers in parental care in the urban environment leads to a better understanding of kit fox biology and can help to develop management strategies that best conserve the urban population. This is the focus of my research.

There are many detrimental effects on wildlife that come from exposure to an urban environment. Some important effects include habituation to people, loss of natural behaviors, and developing a dependency on anthropogenic food sources (Cypher and Frost

1999). Kit fox conservation would benefit from examining these effects on the Bakersfield population, especially because such a robust population exists in the city. Maintaining the

Bakersfield population of kit foxes would contribute substantially to kit fox conservation

(Cypher 2010). My project examined the roles of parents and helpers in pup rearing in an urban environment. The primary research goals of my project were to determine: 1) the relative time invested by each adult group member to pup rearing; 2) the tasks performed by each adult member in pup rearing (e.g., provisioning, guarding, etc.); and 3) the chronology of participation and tasks performed by adult group members in pup rearing. A secondary goal of my project was to compare research techniques to determine the optimal method for conducting a behavioral study on kit foxes. With a better understanding of how kit fox reproduction and group formation differs in a natural versus urban setting, management practices can be developed to protect urban populations.

The results of my research project are presented in the following three chapters.

Chapter Two, “A comparison of methods for monitoring behavior in urban San Joaquin kit foxes (Vulpes macrotis mutica),” outlines the methods I used to gather my behavioral data and the pros and cons of each method. Chapter Three, “Parental care in urban San Joaquin kit foxes (Vulpes macrotis mutica): relative roles of adult group members to pup rearing,” describes the main results of my thesis research on parental care. Chapter Four,

“Observations of communal litters in urban San Joaquin kit foxes (Vulpes macrotis mutica),” gives an account of two family groups observed raising litters in a single den, which has never been documented in San Joaquin kit foxes. All three chapters are formatted as manuscripts to be submitted as separate journal publications. Chapter Two is formatted for submission to Western Wildlife and Chapters Three and Four are formatted for submission to

Western North American Naturalist.

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Maldonado. 2006. Relative abundance of endangered San Joaquin kit foxes (Vulpes

macrotis mutica) based on scat-detection dog surveys. The Southwestern Naturalist

51:210–219.

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Ecology, Conflict, and Conservation. John Hopkins University Press, Baltimore,

Maryland.

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oil-developed habitat of Kern County, California. Pages 53–70 in Spiegel, L. K.,

editor. Studies of the San Joaquin Kit Fox in Undeveloped and Oil-developed Areas.

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Species of the San Joaquin Valley, California. Region 1, Portland, Oregon.

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of Mammalogy 58:157–164.

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to supplemental feeding. The Southwestern Naturalist 44:367–374.

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Zubiri, editors. The Biology and Conservation of Wild Canids. Oxford University

Press, Oxford, UK.

Urban San Joaquin Kit Fox Parental Care

CHAPTER 2

A COMPARISON OF METHODS FOR MONITORING BEHAVIOR OF URBAN SAN JOAQUIN KIT

FOXES (VULPES MACROTIS MUTICA)

1,2,4 2 3 TORY L. WESTALL , BRIAN L. CYPHER , AND KATHERINE RALLS

1Department of Biology, California State University, Bakersfield, California 93309

2Endangered Species Recovery Program, California State University, Stanislaus, P.O. Box

9622, Bakersfield, California 93389

3 Smithsonian Conservation Biology Institute, 3001 Connecticut Avenue NW, Washington,

DC 20008

4Corresponding author, email: [email protected]

Abstract.—Gathering behavioral data for mammalian carnivores is difficult due to their secretive and often nocturnal nature. A wide variety of methods are available for monitoring carnivores, but direct comparisons of the efficacy of these methods have not been conducted. We used proximity logging collars, direct observations, and remote cameras simultaneously to monitor den attendance patterns in San Joaquin kit foxes

(Vulpes macrotis mutica). We compared the effectiveness of each method for determining the total time spent at the den by individual foxes. Proximity logging collars were unsuccessful at recording den attendance during this study and results could not be compared between this and other methods. Remote cameras significantly underestimated the amount of time that foxes spent at the den. This was due to the limited field of view and the complex nature of kit fox den sites. Direct observations

Urban San Joaquin Kit Fox Parental Care were the most accurate method for collecting behavioral data, but there is a risk of influencing the behavior of the fox with human presence and the problem of reduced visibility when monitoring nocturnal species.

Key Words.—camera stations, direct observations, proximity collars, San Joaquin kit fox, survey methods, Vulpes macrotis mutica

INTRODUCTION

Gathering behavioral information about mammalian carnivores is essential to understanding their place in an ecological system (Elbroch and Allen 2013). Often, even small carnivores play significant roles in ecosystem function despite their relatively low abundance (Gompper et al. 2006). Monitoring behavior in terrestrial carnivores is a difficult task because they are often nocturnal and secretive and occur in low densities with relatively large home ranges (Crooks et al. 2008; Balme et al. 2009; Prange et al. 2011; Brawata et al.

2013). In addition to their secretive nature, some species occupy habitats that are not conducive to observation (i.e., fossorial or arboreal species; Prange et al. 2006; Hauver et al.

2010). To overcome these limitations, many researchers have relied on the use of modern technologies to enhance visibility of the study subjects and gather more detailed information

(Brawata et al. 2013).

A wide variety of options are available to conduct surveys for cryptic species. Track stations (Gompper et al. 2006; Balme et al. 2009), scat surveys (Smith et al. 2006; Brawata

2013), and scent stations (Gompper et al. 2006) have been used to document presence of cryptic carnivores, but they do not provide detailed information regarding behavior. The most

Urban San Joaquin Kit Fox Parental Care commonly used methods to document behavior include direct observation (Strand et al.

2000; McGee et al. 2005; Poessel and Gese 2013), night-vision equipment (Murdoch et al.

2002; Brawata et al. 2013), remote cameras (Cutler and Swann 1999; Swann et al. 2004;

Crooks et al. 2008), remote video surveillance (McGee et al. 2005; Brawata et al. 2013), and thermal imaging (Brawata et al. 2013). Recently, proximity logging collars have been used to record social interactions among island foxes (Urocyon littoralis) as well as to determine social structure and mating systems (Ralls et al. 2013). Proximity logging collars have also been used to document den attendance patterns and tolerance of den visitations by conspecifics in northern raccoons (Procyon lotor; Hauver et al. 2010). Each method has advantages and limitations, but there have not been many studies making direct comparisons between methods used simultaneously.

We compared the efficacy of three methods used to collect data on den attendance patterns in adult San Joaquin kit foxes (Vulpes macrotis mutica) during pup rearing. The three methods were proximity logging collars, remote cameras, and direct observations. The methods were used simultaneously at dens so that results could be directly compared among data collection strategies.

METHODS

We trapped foxes during late December 2010 to mid-January 2011 and in early

Urban San Joaquin Kit Fox Parental Care from well trafficked areas and covered the traps with oiled cloth tarps to guard against the elements. We evaluated each fox to determine age, sex, and reproductive condition and we applied a uniquely numbered ear-tag to every individual. Females were ear-tagged on the right and males were ear-tagged on the left to help distinguish fox sex at a glance. We marked each fox with a unique pattern using a permanent non-toxic dye (Nyanzol-D) to allow for the identification of individuals over the course of the project.

Once age and sex were determined, we applied proximity logging collars (Sirtrack,

Model: E2C 162A, Havelock North, New Zealand) to foxes. Due to budget constraints, we had a limited number of collars, and so we only collared adult foxes that were exhibiting signs of breeding (e.g., swollen vulva, enlarged testes). All proximity logging collars transmitted a VHF signal that could be tracked using a receiver (Communications Specialists,

Inc., Model R1000, Orange, California) and 3-element antenna (AF Antronics, Inc., Model

F150-3FB, Urbana, Illinois) or omni-antenna (Teleonics, Model RA-5A, Mesa, Arizona).

Each collar had a mortality sensor that would double the signal pulse rate if the animal remained motionless for more than 8 h. Once we were reasonably sure that most, if not all, individuals from a site were captured, trapping ended and observation at each site began.

The objective during the observation period was to record times when adult foxes were present and absent from the den, as well as to observe behaviors performed at the den.

Proximity logging collars served two functions, they allowed us to track the foxes directly to the natal den and they recorded when foxes were present or absent from the den. At each den where we had collared foxes, we placed a proximity base station (Sirtrack, Model: E2C

162A, Havelock North, New Zealand; Sirtrack, Model E2S 181A, Havelock North, New

Zealand) near the den entrance. To secure the base station at the den, we attached the base

Urban San Joaquin Kit Fox Parental Care station to a 0.6-m (2-ft) wooden stake and hammered the stake into the ground until the base station was buried just below the surface (approximately 0.1-m). The proximity logging collars and the base station would log the date, time, and collar ID of any collared animal that came within 10 m of it. The den base stations were attached to a stake and buried just below the surface at the den entrance. This was done in an effort to discourage foxes from moving collars or base stations away from dens. Use of base stations allowed for continuous collection of presence and absence data around the den.

We performed direct observations at each den for a period of 2 h one to two times a week between January and May. We would arrive at the den 0.5 h prior to sunset and track foxes to the proper den for observation. After tracking foxes, we would find a location a suitable distance from the fox den and begin our 2-h observation window when fox activity started. Foxes were monitored for the first 2 h of their activity and the amount of time spent present and absent was recorded for each fox each night. To gather additional observation data, we set up remote motion sensing cameras (Bushnell Trophey XLT, Model 119456C,

Hartford, Connecticut) at natal dens. Cameras were attached to a 0.9-m (3-ft) u-post placed approximately 8–10 m from the den and pointed at the den entrance. Cameras were powered by eight AA batteries and images were recorded on an 8GB SD card. We programmed cameras to take three 8-MP pictures for each trigger and to wait 1 s between triggers.

Cameras documented behavior continuously while deployed. To avoid disruption to the study subject, we only used cameras that used an infrared flash at night. To measure differences between methods, we conducted observations using multiple methods simultaneously. We totaled the amount of time present at the den for each fox using the different methods and used a Wilcoxon sign rank test (α = 0.05) to determine if there were

Urban San Joaquin Kit Fox Parental Care significant differences in the times spent by foxes at the den based on camera data and direct observations.

RESULTS

We deployed proximity collars on five foxes belonging to two family groups. We installed base stations at the natal dens associated with each family group. Unfortunately, the data collected from the base stations were unreliable. The base stations did not register any fox activity within the 2-h window used to collect simultaneous data using the other observation methods. As a result, proximity logging collars could not be compared to other field methods for monitoring den attendance patterns during our study.

We monitored three groups using both direct observation and camera stations. There were 13 nights during the breeding season when we used both methods simultaneously to collect behavioral data. We compared time spent at the den for 50 samples using both methods. The mean (± SE) number of minutes spent at the den by each fox was 7.52 ± 1.34 for direct observations and 4.40 ± 1.85 for camera station observations. The amount of time that foxes were present at the den was significantly higher for direct observations than for observations made by camera station (t = 145.5, df = 12, P = 0.005).

DISCUSSION

Proximity logging collars were an unreliable source of den attendance information for urban San Joaquin kit foxes. The collars did not log kit fox presence at times when an

Urban San Joaquin Kit Fox Parental Care observer was monitoring the den and kit foxes were known to be moving in and out of the area. Proximity logging collars have been successfully used to determine den attendance patterns in arboreal species (Hauver et al. 2010). However, controlled studies suggest that the closer the collars are to the ground the less reliable they are in recording contacts because the ground absorbs power from the signal (Prange et al. 2011). In our study base stations were buried at dens to prevent removal by kit foxes or humans. Ground interference likely prevented the collar signal from reaching the base station. Future studies on den attendance using proximity loggers on fossorial species probably would be more effective if base stations are located above ground (e.g., attached to a post). However, in urban settings this could increase the risk of theft or vandalism.

Another factor that may have limited the efficacy of using proximity loggers to monitor den attendance is the structure of kit fox dens. Kit foxes tend to use large natal dens with multiple entrances. Installing multiple base stations around the den complex may be necessary to ensure detection of foxes. Kit fox dens can also be deep and complex (Morrell

1972) and it may not be possible to determine kit fox presence if a collared individual is too far underground. With proximity loggers, den attendance information for fossorial species may be limited to time spent above ground at the den because time in the den and away from the den may be indistinguishable.

Monitoring the den directly provides a more extensive view, which allows for documentation of behaviors occurring both at the den and in the surrounding area (Brawata et al. 2013). However, direct observations are limited by the amount of time a person can spend vigilantly watching a den (Weller and Derksen 1972). Direct observations are also limited by the distance from the point of interest. The ability of an observer to identify

Urban San Joaquin Kit Fox Parental Care individuals and collect accurate behavioral information may decrease with distance, particularly if there are objects or vegetation obstructing the view (Sundell et al. 2006;

Brawata et al. 2013). Conversely, if the observer is too close to a den, they could alter the natural behavior of the animal under observation (Brawata et al. 2013). In this study, observations were performed in an urban setting where animals were habituated to the presence of humans. A study conducted in natural lands would be more difficult due to increased wariness by foxes.

Camera stations are an effective method to collect behavioral information continuously over long periods of time (Cutler and Swann 1999). Because cameras can be left out for extended periods (e.g., several days), they can collect continuous data without the limitation of decreasing vigilance due to observer fatigue. Another advantage to using remote cameras is that they can be placed directly in front of the natal den without affecting the behavior of the animals under observation due to rapid habituation (Cutler and Swann

1999; Brawata et al. 2013). Also, cameras capable of taking infrared images, such as the ones we used, can record data under light conditions that would preclude direct observations.

While there are several advantages to using cameras, the method does have some associated disadvantages. The biggest limitation when using cameras to monitor a den is the restricted field of view. Cameras will only detect activity in a cone directly in front of the infrared sensor (Cutler and Swann 1999), but as previously stated, kit foxes use large dens with multiple entrances, some of which may be outside the field of view. Also, adult foxes often patrol around the area when guarding young and may not be detected by the camera.

Unless a camera can be installed at multiple den entrances and in the surrounding area, there is a risk of missing some behaviors. Another concern when using remote cameras is that

Urban San Joaquin Kit Fox Parental Care human activity when deploying cameras or human scent on cameras or on the route into cameras will attract other species to den sites (Cutler and Swann 1999). This could be detrimental to the study animals if potential predators are attracted to a den area, particularly when vulnerable young are present. Finally, while deployment and operation of cameras is less labor intensive than direct observations, analysis of the resulting photos can be a tedious and time consuming process (Weller and Derksen 1972).

Based on our results, camera stations significantly underestimated the amount of time kit foxes spent at the den compared to direct observations. This is likely due to the limited field of view of cameras and possible failed triggering. During direct observations, foxes guarding pups would patrol the den area, moving in circles around the den and stopping at regular stations to keep watch. Without multiple cameras in place, it could appear that a fox on patrol had left the den area when in fact it was still present but simply outside the camera field of view. Camera stations also may have missed rapidly occurring events, like provisioning, which can occur in less time than the camera trigger speed.

Direct observations seem to provide the most accurate information on kit fox den attendance and behavior, but may be limited to relatively short observation periods. Camera stations can provide information over longer periods of time, but results generally are not as accurate as direct observations. When conducting a study monitoring behavior over time, either method could be used to gather valuable information, depending upon the study objectives, subject animals, and observation conditions. Direct observations may be used to focus on behaviors that are difficult to detect on camera (e.g., patrolling) and camera observations can be used to continuously document a wide variety of behaviors, but the two methods are not comparable when analyzing den attendance. Proximity logging collars were

Urban San Joaquin Kit Fox Parental Care unreliable in our den attendance study. However, proximity loggers could be used on urban

San Joaquin kit foxes to obtain valuable information on social interactions, mating systems, and the potential for disease transmission.

Acknowledgements—We would like to thank The Smithsonian Institution for

purchasing cameras, The Western Section and San Joaquin Chapter of The Wildlife

Society and the Student Research Scholar Program of California State University,

Bakersfield for student grants for funding supplies for camera stations. The Bureau of

Land Management provided funding for refurbishing our collars. We also thank David

Germano and Carl Kloock for reading an earlier draft of the manuscript, Scott Westall and

Sandra Soles for assisting with camera deployment, and Erica Kelly and Marilyn

Naderhoff for assistance with analysis of photos from camera stations.

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comparison of noninvasive techniques to survey carnivore communities in

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comparison of survey techniques for swift fox pups. Wildlife Society Bulletin

33:1169–1173.

Morrell, S. 1972. Life history of the San Joaquin kit fox. California Fish and Game 58:162–

174.

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Smith, D.A., K. Ralls, B.L. Cypher, H.O. Clark, P.A. Kelly, D.F. Williams, and J.E.

Maldonado. 2006. Relative abundance of endangered San Joaquin kit foxes (Vulpes

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Urban San Joaquin Kit Fox Parental Care

CHAPTER 3

PARENTAL CARE IN URBAN SAN JOAQUIN KIT FOXES (VULPES MACROTIS MUTICA): RELATIVE

ROLES OF ADULT GROUP MEMBERS IN PUP REARING

TORY L. WESTALL

Department of Biology, California State University, Bakersfield, California 93309 Endangered Species Recoery Program, California State University, Stanislaus, California 95382 Present Address of TLW: California State University, Stanislaus – Endangered Species Recovery Program, P.O. Box 9622, Bakersfield, CA 93389 [email protected]

BRIAN L. CYPHER

Endangered Species Recovery Program, California State University, Stanislaus, CA 95382 [email protected]

KATHERINE RALLS

Smithsonian Conservation Biology Institute, Washington, DC 20008 [email protected]

DAVID J. GERMANO

Department of Biology, California State University, Bakersfield, CA 93311 [email protected]

Urban San Joaquin Kit Fox Parental Care

ABSTRACT.—Because of extensive habitat degradation and loss, the San Joaquin kit fox

(Vulpes macrotis mutica; SJKF) is federally listed as Endangered and listed by California as

Threatened. A substantial population of San Joaquin kit foxes is known to reside in

Bakersfield, California. Kit fox family groups typically consist of a mated pair, the young- of-the-year, and occasionally older offspring from previous years. The relative contributions of the parents and older offspring to the rearing of young are unknown in the urban environment. We determined the relative time investment by each adult group member to pup rearing (den attendance), the tasks performed by each adult group member in pup rearing

(e.g., provisioning, guarding, etc.), and the chronology of participation and tasks performed by adult group members in pup rearing. We classified group members into three categories

(Mother, Father, and Helper) and monitored for three periods of the breeding season

(Preparturition, Nursing, and Weaned). Our results indicated no significant difference in den attendance between periods, but there was a significant difference in den attendance by role.

Mothers spent significantly more time at the den than either Fathers or Helpers. Mothers and

Fathers had no significant difference in the number of provisioning events, but both provisioned significantly more than Helpers. Not surprisingly, Mothers played a critical role in pup rearing and provided the most direct care to young, while Fathers searched for food to provision Mothers and pups. Helpers in the urban setting did not contribute significantly to pup care and were only tolerated in their natal range because of a super-abundance of food.

Further research should investigate the role of Helpers in a natural setting to determine the benefit they may have to pups.

Urban San Joaquin Kit Fox Parental Care

Group living and cooperative breeding are common themes in canid ecology

(Macdonald and Sillero-Zubiri 2004). Canid pups typically have a prolonged period of dependence following birth and rely on care from both parents to survive (Macdonald et al.

2004). Occasionally, young of the year will remain in their natal range and assist parents with pup rearing of future litters (Moehlman 1989, Ralls et al. 2001, Macdonald et al. 2004,

Cypher 2010). Helpers are known to increase pup survival (Moehlman 1989) and decrease the parental care investment of the breeding (alpha) female, which increases her lifetime reproductive success (Macdonald et al. 2004). Other benefits to the alpha female include more food for her offspring, increased predator surveillance and defense, more time for her to forage while helpers guard offspring, having subordinate females to take over care of her pups if she should die, and assurance that her kin will inherit her territory (Moehlman 1989).

The subordinate females benefit by staying in a known territory, kin investment, and potentially becoming the breeding female and inheriting their natal range, as well as training in pup rearing (Moehlman 1989).

San Joaquin kit foxes (Vulpes macrotis mutica) are small canids of California that typically inhabit arid and semiarid habitats including desert scrub, chaparral, and native and non-native grasslands (Macdonald and Sillero-Zubiri 2004, Moehrenschlager et al. 2004,

Cypher 2010). Kit foxes (all subspecies) and the closely related swift foxes (V. velox) are unique among canids in that they use earthen or subterranean dens every day of their life

(Koopman et al. 1998, Moehrenschlager et al. 2004, Cypher 2010). Dens are used to escape predators, avoid temperature extremes and excessive water loss, diurnal resting, and for pup rearing (Ralls and White 2003, Moehrenschlager et al. 2004, Cypher 2010). Kit foxes typically have multiple dens within their home range that are maintained by family groups

Urban San Joaquin Kit Fox Parental Care

(Morrell 1972, Koopman et al. 1998, Ralls and White 2003). A kit fox family group consists of a mated pair and their current offspring as well as any delayed dispersers that have remained in their natal range (Ralls and White 2003, Cypher 2010). In kit foxes delayed dispersers, or helpers, tend to be female, though they can be either sex (Koopman et al. 1998,

Ralls et al. 2001). Helper foxes are always related to one of the breeding pair and typically provide food and care to the breeding female and her offspring (Ralls et al. 2001, Wayne et al. 2004, Cypher 2010). Mated pairs are not often closely related (Ralls et al. 2001), though female members of adjacent groups typically are, indicating an extended social network

(Ralls and White 2001, Ralls and White 2003, Wayne et al. 2004).

Kit foxes are mostly monogamous, with occasional cases of polygyny and they generally mate for life (Spiegel and Tom 1996, Moehrenschlager et al. 2004, Ralls et al.

2007, Cypher 2010). They mate in late November to early December and young are born from late January to early March (Morrell 1972, Moehrenschlager et al. 2004, Cypher 2010).

Litters consist of 1–7 pups with an average of four per pair (Moehrenschlager et al. 2004,

Ralls et al. 2007). Pups emerge from the den at four weeks, are weaned at eight weeks, and become independent at 5–6 months (Morrell 1972, Moehrenschlager et al. 2004, Ralls et al.

2007). At that time, young will disperse or choose to delay dispersal and continue to occupy their natal ranges (Ralls et al. 2001, Ralls et al. 2007, Cypher 2010).

The San Joaquin kit fox, which occurs in central California, is federally listed as

Endangered by the U.S. Fish and Wildlife Service (USFWS) and state-listed as Threatened by the California Department of Fish and Wildlife (CDFW) due to habitat loss caused by human impacts (Morrell 1972, USFWS 1998, Cypher et al. 2013). San Joaquin kit foxes are genetically distinct and topographically isolated from desert kit foxes (V. m. arsipus)

Urban San Joaquin Kit Fox Parental Care populations to the east (Waithman and Roest 1977). Currently, San Joaquin kit foxes exist in a meta-population consisting of several small satellite populations and three core populations located in Western Kern County, the Carrizo Plain, and the Panoche Valley (Cypher et al.

2013). A potential fourth core population exists in the form of an urban population of San

Joaquin kit foxes. A large number of San Joaquin kit foxes are known to reside in Taft,

Coalinga, and Bakersfield (Cypher and Frost 1999, Cypher 2010). While Taft and Coalinga are small cities and surrounded by kit fox habitat, Bakersfield is a large city with only 25-

30% of its limits abutting natural habitat (Cypher 2010). As a result, Bakersfield has a substantial population of San Joaquin kit foxes living within the city (Smith et al. 2006,

Cypher 2010). In the smaller cities, kit foxes may be splitting some of their time between urban and natural habitats, but in Bakersfield many foxes will spend their entire lives within the urban environment. The urban environment is an altered environment full of processes that are very different from that of natural habitats (Gehrt 2010). Investigating the differences between urban and nonurban populations of San Joaquin kit foxes is important to developing conservation strategies that protect the species as a whole.

In urban areas, the presence of helpers occurs at a higher frequency as a result of higher survival rates, restricted dispersal potential, and consistently abundant food and water

(Cypher 2010). Like natural kit foxes, urban foxes prefer to eat rodents and insects, primarily feeding on gophers, squirrels, mice and rats, and beetles, cockroaches, and grasshoppers (Cypher 2010). The presence of anthropogenic food sources (e.g., trash, pet food, handouts) results in a higher carrying capacity in smaller patches (Frost 2005, Cypher

2010). As a result of increased food availability, urban foxes have higher reproductive rates and lower mortality rates than kit foxes in natural habitats (Cypher and Frost 1999, Warrick

Urban San Joaquin Kit Fox Parental Care et al. 1999, Frost 2005, Cypher 2010). Given that food availability is the most influential factor in determining group formation and size (Cypher et al. 2000), it is no surprise that there are more cases of delayed dispersal, and even older foxes helping their offspring, in the urban environment (Cypher 2010). Presence of helpers in other canid species has been shown to increase reproductive success and pup survival (Moehlman 1989), but little is known about the effects of extra helpers in an urban setting.

1999). Kit fox conservation would benefit from examining these effects in the Bakersfield population, especially because such a robust population exists in the city, and maintaining this population could contribute substantially to kit fox conservation (Cypher 2010). We examined the roles of parents and helpers in pup rearing in an urban environment. The primary research goals of our project were to determine: 1) the relative time invested by each adult group member to pup rearing; 2) the tasks performed by each adult member in pup rearing (e.g. provisioning, guarding, etc.); and 3) the chronology of participation and tasks performed by adult group members in pup rearing. With a better understanding of how kit fox reproduction and group formation differs in a natural versus urban setting, management practices can be developed to protect urban populations.

METHODS

Urban San Joaquin Kit Fox Parental Care

Study Area

We conducted our study at various school campuses in Bakersfield, California. These sites were chosen based on knowledge of historical natal dens, provided by the California

State University, Stanislaus, Endangered Species Recovery Program (ESRP). We chose school sites because they were secure locations for direct observation as well as places where ambient lighting increased visibility of fox behavior. The sites we monitored were

Bakersfield College, Stockdale High School, North High School, and California State

University, Bakersfield (Fig. 1).

Field Methods

We trapped foxes during late December 2010 to mid-January 2011 and in early

January 2012 to apply collars, mark foxes, and gather relevant biological information. We captured foxes with wire-mesh box traps (38 x 38 x 107 cm) that were baited with cat food, hot dogs, and sardines. For the animals’ protection, we placed traps in secure locations away from well trafficked areas and covered the traps with oiled cloth tarps to guard against the elements. We evaluated each fox to determine age, sex, and reproductive condition and applied a uniquely numbered ear-tag to every individual. Females were ear-tagged on the right and males were ear-tagged on the left to help distinguish fox sex at a glance. Hair samples were collected from all foxes and tissue samples were collected from some individuals for genetic analysis. Tissue samples were collected from one ear using a 2-mm disposable biopsy punch (Inegra® Miltex®, Model 33-31,York, Pennsylvania). We marked each fox with a unique pattern using a permanent non-toxic dye (Nyanzol-D) to allow for the identification of individuals over the course of the project.

Urban San Joaquin Kit Fox Parental Care

Once age and sex were determined, we applied proximity logging collars (Sirtrack,

Model: E2C 162A, Havelock North, New Zealand) to foxes with breeding potential. Due to budget constraints, a limited number of foxes could be collared, so we only collared older foxes that were showing signs of breeding. All proximity logging collars transmitted VHF signal that could be tracked using a receiver (Communications Specialists, Inc., Model

R1000, Orange, California) and 3-element antennae (AF Antronics, Inc., Model F150-3FB,

Urbana, Illinois) or omni-antennae (Teleonics, Model RA-5A, Mesa, Arizona). Each collar had a mortality sensor that would double the signal pulse rate if the animal remained motionless for more than 8 h. Once we were reasonably sure that most, if not all, individuals from a site were captured, trapping ended and observations at each site began. The objective during the observation period was to record times when adult foxes were in the natal den, at the den, and away from the den, as well as to observe activities performed at the den. We used three methods to meet these objectives: proximity logging collars, direct observations, and camera stations set up at the natal den.

Proximity logging collars served two functions: they allowed us to track the foxes directly to the natal den and they recorded when foxes were present or absent from the den.

At each den used by collared foxes, we placed a proximity base station (Sirtrack, Model:

E2C 162A, Havelock North, New Zealand; Sirtrack, Model E2S 181A, Havelock North,

New Zealand) near the den entrance. The proximity logging collars and the base station would log the date, time, and collar ID of any collared animal that came within 10 m of it.

This allowed for continuous collection of presence and absence data around the den. It did not, however, provide information on activities performed by adult foxes while they were present at the den.

Urban San Joaquin Kit Fox Parental Care

We performed direct observations at each den for a period of 2 hr one to two times a week between January and May. We would arrive at the den 0.5 hr prior to sunset and track foxes to the proper den for observation. After tracking foxes, we would find a location at a suitable distance from the fox den and begin our 2-hr observation window when fox activity started. Foxes were monitored for the first 2 hr of their activity because kit foxes and closely related swift foxes are most active at the den early in the night (Poessel and Gese 2013; pers. obsv.). The amount of time spent present and absent was recorded for each fox each night.

Of the time spent present, behavior was split into three categories: in the den, providing care

(guarding, playing, provisioning, etc.), or non-care behaviors (resting, foraging, digging, etc.). The distance from the den and the start time of fox activity varied between family groups. To gather additional observation data, we set up remote motion sensing cameras

(Bushnell Trophey XLT, Model 119456C, Hartford, Connecticut) at natal dens. We placed cameras approximately 8–10 m from the den and pointed them at the den entrance. Cameras were attached to a 0.91-m (3-ft) u-post and set up with eight AA batteries and an 8GB SD card. We programmed cameras to take three 8MP pictures for each trigger and to wait 1 s between triggers. To avoid disruption to the study subject, we only used cameras that used an infrared flash at night.

We categorized foxes into three roles: Mother, Father, or Helper. The role of a fox was determined based on observations and, in one case, genetic analysis. Mothers were easily identifiable because they showed signs of nursing. Most groups only had one male who was classified as the Father, but in one case two males were associated with one group and paternity was unknown. Genetic analysis was used to determine paternity and one male was classified as a Father and the other a Helper (Westall 2015).

Urban San Joaquin Kit Fox Parental Care

To determine changes in behavior over time, we split the breeding season into three periods based on pup development: Preparturition, Nursing, and Weaned. We estimated the date of birth of the pups by counting back four weeks from the date of emergence because

San Joaquin kit fox pups typically emerge from the den at four weeks of age

(Moehrenschlager et al. 2004, Ralls et al. 2007). Preparturition lasted from the start of observations to the birth of the pups. The Nursing period began at the estimated date of birth and ended at eight weeks of age, when the pups are fully weaned (Moehrenschlager et al.

2004, Ralls et al. 2007). The final period, Weaned, began when the pups reached eight weeks of age and lasted until the pups began to leave the den with their parents, typically mid-May. Splitting the breeding season into these three periods allowed us to monitor changes in adult kit fox contributions to pup rearing as the pups’ needs changed.

Statistical Analysis

To determine relative parental care contributions, we calculated the average number of minutes each fox spent at the den per period of the breeding season. Observation nights were standardized to 2 h so counts of minutes were used instead of frequencies. We ran a two-way ANOVA to determine if there were differences in the amount of time Mothers,

Fathers, and Helpers spent at the den and if the amount of time at the den changed between periods of the breeding season. We tested for interactions between role and period. We used

Tukey’s pairwise comparisons to determine differences between roles and periods. The time spent at the den was also analyzed to determine if Mothers, Fathers, and Helpers spent significantly different amounts of time in the den, providing care, or displaying non care related behaviors. To analyze the differences in behaviors at the den we transformed the

Urban San Joaquin Kit Fox Parental Care proportion of time each fox spent performing a behavior using the arcsin transformation to normalize the data and then we used a two-way ANOVA. We tested for interactions between role and behavior, periods and behavior, and role, period, and behavior. We used Tukey’s pairwise comparisons to determine difference between roles and periods. To determine differences in provisioning events we used a chi-square goodness of fit test for observed counts. Provisioning events were compared between the Nursing and the Weaned periods only because there was only one provisioning event during the Preparturition period. For all tests, α = 0.05.

RESULTS

We began monitoring in mid-January to capture behavior prior to pup birth, but after a natal den had been chosen. We continued to monitor until pups began leaving the den with their parents at night, around mid-May. We monitored six family groups in Bakersfield, although only four groups were used in the parental care analyses. In 2011, we monitored one family group from Bakersfield College (BC 2011) and one from Stockdale High School

(SHS). We monitored the BC 2011 group for 33 nights and the SHS group for 29 nights

(Table 1). The BC 2011 group consisted of six adult foxes (two males and four females) and four pups (two male, one female, and one unknown; Table 2). One pup did not survive the breeding season; however, the other three pups survived and were present the following year as active group members. The SHS group consisted of three adult foxes (two females and a male). Unfortunately, the SHS group did not produce pups; as a result, the group was not included in the parental care analyses.

Urban San Joaquin Kit Fox Parental Care

During the 2012 breeding season, we monitored a group at Bakersfield College (BC

2012), two groups from California State University, Bakersfield, central (CSUB C) and south

(CSUB S), and a group from North High School (NHS). We monitored BC 2012 directly for

12 nights and indirectly via remote camera for 23 nights (Table 1). This group consisted of four adults and 10 pups, the adults were two females and two males who had been present the year before, but had not reproduced (Table 2). We monitored CSUB C for 14 nights directly and 26 nights via trail camera (Table 1). This group consisted of a mated pair and four pups

(Table 2). This was the only group that did not have any Helpers. We monitored CSUB S for 21 nights directly and 25 nights via trail camera. This group consisted of four adults and six pups; the adults were one male and three females (Table 2). We were only able to monitor NHS indirectly through remote cameras due to insufficient lighting at the den location. Unfortunately, the results from trail cameras were significantly different from the results acquired through direct observation (Westall 2015) and so NHS was not included in our analyses for parental care. Proximity logging collars and trail cameras were unreliable in detecting presence of foxes at the den (Westall 2015), so the results from these methods were not used for our statistical analyses. We have only presented den attendance patterns and behaviors based on direct observations.

The range for the proportion of time spent at the den was 9.5–14.5% for Fathers,

20.0–32.4% for Helpers and 43.2–67.4% for Mothers. Kit foxes spent significantly different amounts of time at the den based on role (F2,33 = 11.06, P < 0.001), but no difference based on period (F2,33 = 1.46, P = 0.247). The interaction between role and period was not significant (F4,33 = 0.24, P = 0.913). On average, Mothers spent 64.2% of the observation period at the den, Fathers spent 13.4%, and Helpers spent 36.5% (Fig. 2). Mothers spent

Urban San Joaquin Kit Fox Parental Care significantly more time at the den than Helpers (t = 2.54, d.f. = 8, P = 0.042) and Fathers (t =

4.64, d.f. = 8, P < 0.001). The amount of time that Helpers and Fathers spent at the den was not significantly different (t = 1.92, d.f. = 6, P = 0.148; Fig. 2). Time spent on specific behaviors differed by role (F4,66 = 7.97, P < 0.001) and by period (F2,66 = 11.42, P < 0.001), but the interaction between role and period was not significant (F4,66 = 1.37, P = 0.254). All foxes spent signifcantly less time performing non-care behaviors than they did in the den (t =

-3.17, df = 54, P = 0.006) or providing care (t = -5.15, df = 54, P < 0.001).

The amount of time foxes spent in the den and providing care did not differ (t = -1.98, df = 54, P = 0.124). Of the time Fathers spent at the den, the average proportion of time spent in the den was 13.9%, 76.5% was spent providing care, and 9.6% of their time present was spent performing non care behaviors (Fig. 3). Fathers spent significantly more of their time present at the den providing care than in the den or not providing care (Table 3).

Fathers also spent significantly more of their time present providing care than Helpers (Table

4). Of the time Helpers spent at the den, the average proportion of time spent in the den was

46.0%, 26.7% was spent providing care, and 27.3% of their time present was spent performing non care behaviors (Fig. 3). The amount of time helpers spent providing care did not differ from time in the den or time performing non-care behaviors (Table 3). Of the time

Mothers spent at the den, the average proportion of time spent in the den was 48.0%, 44.4% was spent providing care, and 7.6% of their time present was spent performing non care behaviors (Fig. 3). The amount of time mothers spent in the den and providing care at the den did not differ, but mothers spent significantly less time performing non-care behaviors than in the den or providing care (Table 3).

Urban San Joaquin Kit Fox Parental Care

Of the time adult foxes spent at the den during the Nursing period, the average proportion of time spent in the den was 48.3%, 31.4% was spent providing care, and 20.3% of their time present was spent performing non care behaviors (Fig. 4). The amount of time all foxes spent providing care in the nursing period did not differ from time in the den or providing care (Table 3). Of the time adult foxes spent at the den during the Weaned period, the average proportion of time spent in the den was 23.7%, 66.9% was spent providing care, and 9.4% of their time present was spent performing non care behaviors (Fig. 4). Foxes spent significantly more of their time present providing care during the Weaned period than during the Nursing period (Table 3). During the Weaned period, foxes spent more of their time present providing care than time in the den or performing non-care behaviors (Table 3).

For all observation periods combined, we observed 80 provisioning events. Of the 80 events, 42 (52.5%) were performed by Mothers, 29 (36.3%) were performed by Fathers, and

9 (11.3%) were performed by Helpers (Fig. 5). Only a single provisioning event occurred during Preparturition, so data were only compared between the Nursing and Weaned periods.

The number of provisioning events did not differ between these two periods for Mothers (χ2

= 3.43, df = 1, P = 0.064), Fathers (χ2 = 0.57, df = 1, P = 0.450), or Helpers (χ2 = 1.00, df = 1,

P = 0.317). Total provisioning counts for both periods did not differ between Mothers and

Fathers (χ2 = 2.38, df = 1, P = 0.123), but counts for Helpers were less than for Mothers (χ2 =

21.35, df = 1, P < 0.001) or Fathers (χ2 = 10.53, df = 1, P = 0.001). We documented kit foxes provisioning many anthropogenic items including pizza, potato chips, fast food, and various trash that had no nutritional value. Kit foxes also provided natural food items including desert cottontail (Sylvilagus audubonii), California ground squirrel

Urban San Joaquin Kit Fox Parental Care

(Otospermophilus beecheyi), rat (Rattus sp.), bird, and American bullfrog (Lithobates catesbeianus).

We observed a variety of behaviors over the course of the breeding season, including provisioning, guarding, defense, and play (Table 4). While all behaviors may have been performed by all roles over the course of the study, each behavior was frequently associated with a specific role (Table 4). A common behavior observed throughout the breeding season was guarding. Adult foxes were typically present at the den when pups were above ground, though the frequency of periods where the pups were unattended increased as they grew older. Foxes on guard duty were typically vigilant in watching pups and the surrounding area. The fox or foxes guarding would patrol the area in wide circles, stopping at regular intervals to scan the area. Whenever there was a perceived threat the guarding fox would vocalize a warning and the pups would immediately return to the den. The vocalization used to warn pups was a high pitched bark. Once the threat was over, the guarding fox would go to the den entrance and presumably signal to the pups that it was safe to come out. While no sound was audible from the observer’s vantage point, shortly after the adult returned to the den entrance the pups would reemerge. Most often warning sounds were given when humans came too close to the den, though on occasion, it occurred when cats approached as well.

Den defense was documented on multiple occasions. In some cases foxes took defensive postures at dens and at other times they were more aggressive. Den defense was always performed by Fathers and Mothers. Helpers were never documented defending the den from other wildlife or humans. A Father defended the natal den from a red fox in a series of pictures captured on a remote camera. The kit fox was sitting at the entrance

Urban San Joaquin Kit Fox Parental Care lunging and snapping and a few minutes later a red fox was seen in the background leaving the area (Fig. 6). This male was also observed chasing a person walking passed the den and teaming up with a Mother to flank someone walking through the den area. At one point he circled the observer and growled when the pups started venturing towards the location where the observer was monitoring. We also documented on camera other foxes defending their dens when cats or dogs approached the area.

Play typically involved just pups. Generally, the play observed was group play in the form of chase and retreat, though there was some solitary play as well. In one instance, a

Helper brought a golf ball to the den, which was located on a slope, and a pup would carry the golf ball to the top of the hill, drop it, chase it down the slope, then repeat the process.

Helpers spent more time playing with pups than either parent except in the one group that did not have any Helpers. In this group, the Father occasionally played with the pups.

Kit foxes rarely roamed into adjacent family territories during the breeding season.

Three family groups in this study had natal den locations within 500 m of each other and yet adjacent family members were never documented within sight of another group’s natal den.

Towards the end of the study, a Mother was observed with a pup outside of their core home range within 50 m of a den used by an adjacent family group. This suggests that as the pups age and begin to leave the natal den, the adjacent groups may begin to mingle in shared foraging areas.

Mortality rates were low during the observation periods. Five pups from three litters died while groups were being monitored. One pup died shortly after the pups emerged from the den, but the cause was unknown and the carcass was never recovered. Another pup died late in the breeding season. The carcass was recovered at the den and, based on the location

Urban San Joaquin Kit Fox Parental Care and condition, was likely killed by a great horned owl. The other three pups that died were all from the same litter. They all died the same night when they were caught up and strangled in a batting cage net at a high school. Only two adults died during the project, but both died outside of the breeding season. A male and female from Bakersfield College were killed in 2011 by vehicle strikes. The foxes were hit about three weeks apart in the fall of

2011 and were a mated pair from the previous spring. Their home range was inherited by philopatric young.

DISCUSSION

Role was the most significant factor in predicting the amount of parental care provided to pups by San Joaquin kit foxes. Mothers spent significantly more time at the den then Helpers or Fathers. Mothers provided the most direct parental care while Fathers and

Helpers spent most of their time away from the den and occasionally provided food to the

Mother and pups. This is common among non-urban kit foxes where the males are known to forage and provision lactating females, as well as the pups, while the females remain at the den to guard and nurse the young (Cypher 2003). These results are consistent with a similar study on den attendance patterns in closely related swift foxes where breeding females spent more time providing direct parental care and male parents provisioned infrequently (Poessel and Gese 2013). Similar trends have been recorded for arctic foxes (V. lagopus; Strand et al.

2000) and red foxes (V. vulpes; Soulsbury et al. 2010) as well. In swift foxes, it has been suggested that males may be spending their time away from the den maintaining their territories (Kitchen et al. 2005) and searching for extra-pair copulations while females dedicate their efforts to caring for the young (Poessel and Gese 2013). In our study, Fathers

Urban San Joaquin Kit Fox Parental Care did provide some level of defense when present at the den, we even had one Father defend the den from a red fox. Red foxes are known to limit reproductive success in arctic foxes due to predation on pups (Frafjord et al. 1989), and red foxes have also been documented killing kit foxes (White and Ralls 1995, Clark et al. 2005). There may be more indirect paternal care in the form of territory maintenance that we were not able to document in this study.

The amount of time kit foxes spent at the den was similar among breeding periods.

Similar results were reported for males in a den attendance study on swift foxes, but not for females (Poessel and Gese 2013). In that study, females spent more time with the pups early in the breeding season, but their time at the den decreased as the pups got older. This was attributed to the high use of insects by the adults later in the breeding season (Poessel and

Gese 2013). Adult foxes would be required to forage for longer amounts of time to collect enough insects to meet their dietary needs and insects are difficult to bring back to pups at the den (Poessel and Gese 2013). In our study, the amount of time kit fox Mothers spent at the den did not change as the pups aged, but this could be related to the abundance of food in the urban environment. The super abundance of food in the urban environment (Cypher and

Frost 1999) may have allowed Mothers to maintain consistent habits throughout the breeding season.

Of the four groups monitored, three groups had philopatric young that were classified as Helpers. Helpers were mostly female (66.7%), which is consistent with findings for populations of kit foxes living in natural areas (Koopman et al. 2000, Ralls et al 2001,

Moehrenschlager et al. 2004). One of the three Helpers was very attentive to the pups, but the other two Helpers came to the den infrequently and did not provide much care while present. Occasionally, the Helpers would bring food or play with pups, but they rarely

Urban San Joaquin Kit Fox Parental Care guarded or spent long periods of time at the den. In the wild, when resources are high, the presence of helpers can increase pup survival (Moehlman 1989), but in town the presence of helpers may be solely related to low dispersal potential and high concentration of food in a small area. Kit fox spacing systems are directly related to the type and abundance of prey that is available (White and Ralls 1993). Because food is abundant in the urban environment, enough food is likely available within a home range that a mated pair can share their dens with one or more adult offspring at no cost to themselves or their future litters. If this is the case, then Helpers may not necessarily be contributing to pup care, but are tolerated because they do not impose a negative effect on the parents or future siblings. A similar trend was documented in arctic foxes where additional family members were only accepted in years of high prey availability (Strand et al. 2000). Helpers have been shown to adopt and raise pups following the death of the parents (Spiegel and Tom 1996). While Helpers, did not provide parental care to the pups in most cases, they could potentially care for the pups if something happened to either or both of the parents.

Adult foxes were observed provisioning at the den on numerous occasions throughout the breeding season. Various food items were provided to the pups with many being anthropogenic in origin. On one occasion a pup was caught in a trap and was provisioned with half of a cottontail rabbit. Provisioning of pups caught in traps has been observed previously in non-urban kit foxes (unpubl. data) and also has been documented in island foxes (Garcelon et al. 1999). Pups were provisioned by all adult group members, although

Helpers provisioned pups significantly less than Mothers or Fathers. This is consistent with an arctic fox study where Helpers provided minimal amounts of food to pups and therefore must be present for reasons other than assisting with parental care (Strand et al. 2000).

Urban San Joaquin Kit Fox Parental Care

Arctic foxes have also been shown to live in groups more frequently when food availability increases, either naturally or with supplemental feeding (Elmhagen et al. 2014). This suggests that Helpers in the urban environment may simply be tolerated in their natal range where resources are abundant because there is no negative impact on the mated pair and their future offspring.

Helpers may have an active role in teaching pups the social structure of the group.

Helpers frequently played with pups and possibly used play to establish dominance in the hierarchy of the group. Play between individuals is often a method to test an opponent for weaknesses in preparation for a time when philopatric young may have the opportunity to take over the breeding territory of the dominant pair (Cordoni 2009). By returning to the den periodically and initiating play with the pups, the Helper may be communicating to its younger siblings that it is stronger and higher up in the social hierarchy off the group.

Mothers almost never played and frequently avoided or ran away from pups while they were playing. On occasion, Mothers would aggressively bite at the heads of persistent pups to signal that play was not acceptable. Canids often use signals to indicate when behaviors are meant as play and not as antagonism. The Bow is a classic signal that canids will perform before or after aggressive behaviors to indicate that what they are about to do is play or that play is still continuing despite an aggressive behavior (Beckoff 1995). While Helpers were frequently observed using the Bow to signal play, Mothers and Fathers were rarely witnessed attempting to initiate or continue play with the pups.

Not surprisingly, our findings confirm that Mothers play a critical role in pup rearing for urban San Joaquin kit foxes. Until the pups can be weaned, Mothers are essential in providing nourishment to the young via lactation. After the pups are weaned, it is possible

Urban San Joaquin Kit Fox Parental Care for other family members to assist in the care of the pups, but Mothers still play a large role in pup care. Mothers spend more time at the den than either Fathers or Helpers and are the primary care giver. While Fathers do not provide as much direct care as Mothers, they still contribute the same amount of provisioning throughout the breeding period. Fathers also provision Mothers during lactation and early weaning which allows Mothers to spend more time at the den with the pups that depend on her care. As a result, Mothers are less exposed to the risk of death by predators or, in the case of the urban environment, vehicle strikes.

Fathers also seem to play a large role in den defense and spend the majority of their time at the den guarding pups.

Helpers seem to play a variety of roles in the urban environment. Most groups included Helpers, but they seem to remain in their natal range as a result of the increased food availability in an urban environment. The role of Helpers appears to be supplemental as parents are clearly capable of raising litters on their own. Helpers spent significantly less time at the den than Mothers and they provisioned significantly less than Mothers or Fathers.

Even though Helpers in the urban environment provide little to pup rearing, any assistance they do contribute will reduce the energy, time, and risk investment of the parents. Helpers may not contribute parental care while both parents are present, but it is possible that they may increase their contribution should one of the parents die or become incapacitated.

Parents may allow Helpers to remain in their natal range as a form of insurance in the event that the parents are unable to care for the pups. Helpers may also benefit from remaining in their natal range and interacting with pups to ensure their place in the social hierarchy in the event that their natal territory becomes available.

Urban San Joaquin Kit Fox Parental Care

This is the first study to document parental care behaviors in urban San Joaquin kit fox. The altered processes in the urban environment provide a unique opportunity to define the roles of parents and helpers. The increased frequency of occurrence of groups with philopatric young allows researchers to examine and refine our understanding of the roles of each adult group member in pup rearing. Further research into the demographics and ecology of urban kit foxes will aid efforts to conserve this important population.

ACKNOWLEDGEMENTS

We would like to thank the Endangered Species Recovery Program of California

State University, Stanislaus for supplying equipment for trapping and handling as well as supplies for camera stations. We also thank the Bureau of Land Management for financial support to refurbish collars, The Smithsonian Institution for purchasing cameras, and The

Western Section and San Joaquin Chapter of The Wildlife Society and the Student Research

Scholar Program of California State University, Bakersfield for providing student grants to purchase materials and equipment for camera stations. We thank Carl Kloock for reading an earlier draft of the manuscript and all the individuals who assisted in data collection and analyses for this project: S. Westall, S. E. Soles, S. W. Soles, C. Reedy, K. Reedy, R. Reedy,

C. Van Horn Job, E. Kelly, M. Naderhoff, E. de la Rosa, E. Tennant, and A. Madrid.

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Urban San Joaquin Kit Fox Parental Care

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Ecology, Conflict, and Conservation. John Hopkins University Press, Baltimore,

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oil-developed habitat of Kern County, California. Pages 53–70 in Spiegel, L.K.,

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Urban San Joaquin Kit Fox Parental Care

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Urban San Joaquin Kit Fox Parental Care

Table 1. Number of nights observations that were conducted on each San Joaquin kit fox

(Vulpes macrotis mutica) family group during each period of the breeding season in

Bakersfield, California during 2011 and 2012.

Direct Observation Camera Observation

Family Group Preparturition Nursing Weaned Preparturition Nursing Weaned

BC 2011 6 14 13 0 0 0

BC 2012 1 7 4 0 23 0

CSUB C 3 7 4 6 12 8

CSUB S 8 8 5 0 18 7

Urban San Joaquin Kit Fox Parental Care

Table 2. Number of group members observed in each San Joaquin kit fox (Vulpes macrotis mutica) family group in Bakersfield, California during 2011 and 2012.

Family Group Mothers Fathers Helpers Pups

BC 2011 1 1 4 4

BC 2012 2 1 1 10

CSUB C 1 1 0 4

CSUB S 2 1 1 6

Urban San Joaquin Kit Fox Parental Care

Table 3. Post-hoc tests analyzing differences in proportion of time spent performing specific behaviors within roles of San Joaquin kit foxes (Vulpes macrotis mutica) in Bakersfield,

California, during the 2011 and 2012 breeding seasons. P values in bold are significant.

Comparison df t P

Behavior within Role

Father in the den vs. Father care 4 -5.17 < 0.001

Father care vs. Father non care 4 -5.52 < 0.001

Father non care vs. Father in the den 4 -0.35 1.000

Mother in the den vs. Mother care 4 0.36 1.000

Mother care vs. Mother non care 4 -3.72 0.012

Mother non care vs. Mother in the den 4 -4.09 0.004

Helper in the den vs. Helper care 4 1.60 0.801

Helper care vs. Helper non care 4 0.05 1.000

Helper non care vs. Helper in the den 4 -1.55 0.829

Behavior across Role

Father in the den vs. Mother in the den 4 3.09 0.068

Father in the den vs. Helper in the den 4 2.66 0.184

Mother in the den vs. Helper in the den 4 0.18 1.000

Father care vs. Mother care 4 -2.90 0.107

Father care vs. Helper care 4 -4.11 0.003

Mother care vs. Helper care 4 1.60 0.799

Father non care vs. Mother non care 4 -0.19 1.000

Father non care vs. Helper non care 4 1.46 0.871

Urban San Joaquin Kit Fox Parental Care

Mother non care vs. Helper non care 4 -1.78 0.693

Behavior within Period

Nursing in the den vs. Nursing care 2 1.81 0.467

Nursing care vs. Nursing non care 2 -1.91 0.839

Nursing non care vs. Nursing in the den 2 -3.00 0.042

Weaned in the den vs. Weaned care 2 -4.64 < 0.001

Weaned care vs. Weaned non care 2 -6.17 < 0.001

Weaned non care vs. Weaned in the den 2 -1.53 0.648

Behavior across Period

Nursing in the den vs. Weaned in the den 2 -2.64 0.102

Nursing care vs. Weaned care 2 3.81 0.004

Nursing non care vs. Weaned non care 2 -1.17 0.850

Urban San Joaquin Kit Fox Parental Care

Table 4. Primary roles that were observed most often performing different care behaviors in urban San Joaquin kit fox (Vulpes macrotis mutica) family groups during the 2011 and 2012 breeding seasons.

Behaviors Mother Father Helper

Provisioning X X

Play X

Den Defense X X

Guarding X

Urban San Joaquin Kit Fox Parental Care

Figure 1. Site locations for urban San Joaquin kit fox (Vulpes macrotis mutica) families monitored during 2011 and 2012 in Bakersfield, California.

Figure 2. Mean and standard error for time spent at the den by San Joaquin kit foxes (Vulpes macrotis mutica) during the 2011 and 2012 breeding seasons.

Figure 3. Average proportion of time spent by San Joaquin kit foxes (Vulpes macrotis mutica) in the den, at the den providing care, or at the den not providing care by role in

Bakersfield, California during the 2011 and 2012 breeding seasons.

Figure 4. Average proportion of time spent by San Joaquin kit foxes (Vulpes macrotis mutica) in the den, at the den providing care, or at the den not providing care by period during the 2011 and 2012 breeding seasons in Bakersfield, California.

Figure 5. Provisioning counts during each period of the breeding season and the total number of provisioning events by role for San Joaquin kit foxes (Vulpes macrotis mutica) in

Bakersfield, California during 2011 and 2012.

Figure 6. A series of remote camera photos showing a non-native red fox (Vulpes velox) visiting a San Joaquin kit fox (V. macrotis mutica) natal den (upper left), a kit fox Father aggressively defending the natal den ( upper right and lower left), and the red fox leaving the den area (lower right).

Urban San Joaquin Kit Fox Parental Care

Figure 1

Urban San Joaquin Kit Fox Parental Care

Figure 2 90

40 Time Present (min) Present Time 30

0 Father Helper Mother Role

Urban San Joaquin Kit Fox Parental Care

Figure 3

100% 90% 80% 70% 60% 50% 40% 30%

20% Father Proportion ofPresent Minutes Proportion 10% Mother 0% Helper in the den care non care

Behavior

Urban San Joaquin Kit Fox Parental Care

Figure 4

100%

80%

60%

40%

20% Proportion ofPresent Minutes Proportion Weaned 0% in the den Nursing care non care

Behavior

Urban San Joaquin Kit Fox Parental Care

Figure 5

40 35 30 25 Mother 20 Father 15 Helper 10

5 No. of Provisioning Events Provisioning of No. 0 Preparturition Nursing Weaned Total

Breeding Period

Urban San Joaquin Kit Fox Parental Care

Figure 6

Polygyny in Urban San Joaquin Kit Fox

CHAPTER 4

OBSERVATIONS OF COMMUNAL LITTERS IN URBAN SAN JOAQUIN KIT FOXES (VULPES

MACROTIS MUTICA)

TORY L. WESTALL

Department of Biology, California State University, Bakersfield, CA 93309 Present Address of TLW: California State University, Stanislaus – Endangered Species Recovery Program, P.O. Box 9622, Bakersfield, CA 93389 [email protected]

BRIAN L. CYPHER

Endangered Species Recovery Program, California State University, Stanislaus, CA 95382 [email protected]

KATHERINE RALLS

Smithsonian Conservation Biology Institute, Washington, DC 20008 [email protected]

TAMMY WILBERT

Smithsonian Conservation Biology Institute, Washington, DC 20008 [email protected]

Polygyny in Urban San Joaquin Kit Fox

ABSTRACT.—San Joaquin kit foxes (Vulpes macrotis mutica) are a small desert adapted species endemic to the San Joaquin Desert in California. These foxes are monestrous, typically monogamous, and live in social groups consisting of a breeding pair, their current offspring and occasionally philopatric young that delay dispersal. There is a substantial population of San Joaquin kit foxes living in the city of Bakersfield where resources are abundant, dispersal potential is low, and population density is high. We monitored family groups during the 2012 breeding season and documented two cases of social polygyny and genetic polygamy in urban San Joaquin kit foxes. One family group at Bakersfield College consisted of two mothers, a father, a helper, and two litters of three pups each. The other family group at California State University, Bakersfield, had two mothers, a father, a helper, and two litters totaling 10 pups. While the group at CSUB was socially polygynous, genetically it was only polyandrous, with a minimum of two fathers being associated with the group genetically. The group at Bakersfield College was both socially and genetically polygynous, while also genetically polyandrous. In this group there was a minimum of four fathers genetically, but only one father socially. The increased availability of resources in the urban environment likely has decreased intraspecific competition for resources and so females can tolerate another breeding female within their range. Further investigation into the frequency of occurrence of social polygyny in the urban population could be important to understanding the level of inbreeding and the reproductive success of this endangered species.

Monogamy in mammals is recognized as the continual close proximity of a mated pair whose members express a preference for reproducing exclusively with one another and

Polygyny in Urban San Joaquin Kit Fox remain together outside of and during the breeding season (Kleiman 1977). In mammals, monogamous pairs often remain together over several breeding seasons and the relationship may persist for a large portion of their lifespan (Kleiman 1977). Monogamy can be further categorized as social monogamy or genetic monogamy. Social monogamy occurs when a mated pair has the appearance of being monogamous, but this social system can be combined with an underlying genetic mating strategy (monogamy, polygyny, or polyandry; Baker et al.

2004). Monogamy typically evolves as the result of a need for paternal care when rearing offspring (Moehlman 1989). Canids are thought to be an unusual group because most species exhibit paternal care and have been reported as monogamous (Asa and Valdespino

1998).

Canid breeding systems strongly correlate to body size (Moehlman 1989). Smaller canids, like vulpine foxes, tend to be monogamous (Moehlman 1989). Populations of small canids typically have female biased sex ratios and male dispersal (Moehlman 1989). Due to their size, they are solitary hunters that forage and hunt for small prey (Moehlman 1989).

While monogamy is typical in small canids, the breeding system can be altered under different ecological conditions (Kleiman 1977). The breeding system in small canid populations is often dependent on the cyclic pattern of prey populations (Asa and Valdespino

1998). When resources are scarce, monogamy is a more successful breeding system because paternal care is more critical to pup rearing (Zabel and Taggart 1989, Lemons et al. 2003,

Kamler et al. 2004). When resources are plentiful, extrapair copulations and shifts in breeding strategy are expected to occur more frequently (Cameron et al. 2011). In smaller canids, when resources are abundant, there tends to be a shift towards polygyny (Malcolm

1985, Moehlman 1989).

Polygyny in Urban San Joaquin Kit Fox

The San Joaquin kit fox (Vulpes macrotis mutica) is a small desert adapted canid that is endemic to the San Joaquin Desert located at the south end of the Central Valley in

California (Morrell 1972, Germano et al. 2011). The San Joaquin kit fox is monestrous and socially monogamous (Spiegel and Tom 1996). A social group is typically made up of a breeding pair and their current offspring, though occasionally offspring will delay dispersal and remain in the natal range (Ralls et al. 2001, Ralls and White 2003). Due to habitat loss, the San Joaquin kit fox has been federally listed as Endangered and listed by California as

Threatened (USFWS 1998). As a result of agricultural, industrial, and urban development, the San Joaquin kit fox exists in a meta-population consisting of several small satellite populations and three core areas, the Panoche Valley, the Carrizo Plain, and western Kern

County (Cypher et al. 2013). A fourth substantial population has adapted to living in the urban environment and persists in Bakersfield, California (Cypher and Frost 1999, Cypher

2010).

In the urban environment, there is an increased occurrence of philopatric young due to an increase in the abundance of food (Cypher and Frost 1999). Increased resource availability and a fragmented landscape have resulted in low dispersal potential and increased population density (Cypher and Frost 1999). Alterations to the demographic and ecological traits of the urban San Joaquin kit fox population have affected the breeding system of some groups within this environment. In this paper, we documented an altered breeding system in two family groups in an urban population of San Joaquin kit fox based on direct observation of behavior and genetic analyses.

Polygyny in Urban San Joaquin Kit Fox

METHODS

We trapped kit foxes in early January 2012 to apply collars, mark foxes, and gather relevant biological information and samples. We captured foxes with wire-mesh box traps

(38 x 38 x 107 cm) that were baited with cat food, hot dogs, and sardines. For the animals’ protection, we placed traps in secure locations away from well trafficked areas and covered the traps with oiled cloth tarps to guard against the elements. We evaluated each fox to determine age, sex, and reproductive condition and we applied a uniquely numbered ear-tag to every individual. Females were ear-tagged on the right and males were ear-tagged on the left to help visually distinguish sex of individuals. We collected hair samples and tissue samples from all foxes for genetic analysis. We collected tissue samples from the ear using a

2-mm biopsy punch (Inegra® Miltex®, Model 33-31, York, Pennsylvania) and we stored samples in 95% ethanol. We marked each fox with a unique pattern using a permanent non- toxic dye (Nyanzol-D) to allow for the identification of individuals over the course of the project.

Once age and sex were determined, we applied collars (Sirtrack, Model: E2C 162A,

Havelock North, New Zealand) to foxes with breeding potential. Due to budget constraints, a limited number of foxes could be collared, so we only collared older foxes that were showing signs of breeding (e.g., vulvar swelling, testicular enlargement). All collars emitted a very high frequency (VHF) signal that could be tracked using a receiver (Communications

Specialists, Inc., Model R1000, Orange, California) and 3-element antennae (AF Antronics,

Inc., Model F150-3FB, Urbana, Illinois) or omni-antennae (Teleonics, Model RA-5A, Mesa,

Polygyny in Urban San Joaquin Kit Fox

Arizona). Each collar had a mortality sensor that would double the signal pulse rate if the animal remained motionless for more than 8 h.

We performed direct observations at each den for a period of 2 h one to two times a week, between January and May. To gather additional observation data, we set up remote motion sensing cameras (Bushnell Trophey XLT, Model 119456C, Hartford, Connecticut) at natal dens. We placed cameras approximately 8–10 m from the den and pointed them at the den entrance. We attached cameras to a 0.91-m (3-ft) u-post and the cameras held eight AA batteries and an 8GB SD card. We programmed cameras to take three 8 MP pictures for each trigger and to wait 1 s between triggers. To avoid disruption to the study subject, we only used cameras that used an infrared flash at night. We categorized foxes into three roles: mother, father, or helper. The role of a fox was determined based on observations and genetic analysis.

We investigated relatedness using the molecular methods described in Wilbert et al.

2015. Briefly, we extracted DNA using QIAamp DNA stool mini kit (QIAGEN®). We genotyped each sample at 11 microsatellite tetranucleotide repeat loci (FH2137, FH2140,

FH2226, FH2535, FH2561, Pez19, AHTh171, FH2054, FH2328, and Ren162) that had previously been proven to be reliable for kit fox (Smith et al. 2006). For each DNA extract, we performed two to three PCR replicates of each microsatellite to obtain reproducible genotypes. We used fluorescently labeled forward primers (TET, HEX or FAM) to visualize the products on an ABI PRISM 3130 Genetic Analyzer (Applied Biosystems). We scored the size of each fragment using Genemapper® software. We genotyped 342 individuals captured in Bakersfield from 2000 to 2011. Parentage was determined by a likelihood–based method using the program CERVUS (Kalinowski et al. 2007), which uses the allelic frequencies

Polygyny in Urban San Joaquin Kit Fox from all individuals to calculate the likelihood of parentage for each individual. We used the genotypes from all 342 individuals to calculate allele frequencies and perform simulations in

CERVUS. We simulated maternity, paternity, and parental pair data using the following parameters: 10,000 offspring; eight candidate mothers, fathers, and pairs; 85% mothers, fathers, and pairs sampled; 90% loci typed; 1% missing data; and a minimum of six loci genotyped. We then calculated the likelihood that the adults in each social group were the parents of the pups sampled from that group.

We used a two-step procedure to assign parentage with CERVUS following Dugdale et al. (2007). If CERVUS identified a male-female pair as the parents of a pup with a likelihood of > 80%, we considered that both parents had been identified. If CERVUS did not assign a pair with this level of probability, we examined the likelihood that individual foxes were parents and accepted a female as the mother if her likelihood of maternity was

>95% and a male as the father if his likelihood of paternity was >95%. While a relaxed likelihood of 80% is acceptable for defining pairs (Dugdale et al. 2007), the online manual for CERVUS recommends a minimum likelihood of 95% when defining individual parents

(http://www.fieldgenetics.com/pages/aboutCervus_Method.jsp).

RESULTS

We determined that two groups monitored during the 2012 breeding season were socially polygynous; a group at California State University, Bakersfield (CSUBS) and a group at Bakersfield College (BC2012). Each group consisted of two mothers, one father, and one helper (Table 1). We investigated the relatedness of eight of the 10 individuals

Polygyny in Urban San Joaquin Kit Fox associated with the CSUBS social group and the relatedness of 10 of 14 individuals associated with the BC2012 social group. With the exception of one individual from

BC2012 (male 6584), we were able to genotype these individuals at least eight of 11 microsatellite loci. Most individuals in these two groups were genotyped at all 11 loci.

Overall, we had a low level of dropout (estimated null allele frequencies ranged from 0 –

-9 -4 0.06) and sufficient data for identification of parentage (PID = 1.44 x 10 ; PSIB = 2.47 x 10 ).

CSUBS had two litters with three pups in each litter. The second litter emerged three weeks after the first, and the size and development differences between the litters were obvious (Fig. 1). Allosuckling did occur because both mothers (#6309 and #6700) were documented nursing pups from each litter (Fig. 2). BC2012 had two litters that totaled 10 pups, the total number of pups in each litter was unknown because all pups emerged simultaneously and appeared to be about the same age. There were two mothers present and both showed signs of actively nursing pups (Fig. 3). It is unclear whether or not allosuckling took place in this group because we could not visually distinguish the pups in the two litters.

We sampled four of six pups from the CSUBS group for genetic analysis. We captured three pups and we collected one dead from outside the den. The four pups that we sampled were offspring of the two females associated with the group (#6700 and #6309;

Table 2). The helper associated with this group was a female and none of the pups were her offspring. The male associated with the group (#6065) was the father of two of the four pups, but the paternity of the remaining two pups was unknown and was likely the result of an extra-pair copulation (Table 2). Both pups that male #6065 fathered were also offspring of female #6700, but the offspring of #6309 and the third offspring of #6700 had unknown fathers who were not associated with the group.

Polygyny in Urban San Joaquin Kit Fox

We captured six of 10 pups from BC2012 and we sampled them for genetic analysis.

All pups were offspring of the two females observed with the pups (#6566 and #6525; Table

3). Two of the six pups (#6596 and #6606) were offspring of the dominant male associated with the group (#6524), but #6596 was the offspring of mother #6656 and #6606 was the offspring of mother #6525 (Table 3). Another pup (#6677) was the offspring of a male

(#6523) who lived in the group in 2011, but was no longer present in 2012. Male #6523 may have dispersed over the summer, but returned during mating in search of extra-pair copulations. Pup #6607 was the offspring of male #6547 who died during pairing in

November. The pups in this group were born a month early and #6607 was likely the result of an extra-pair copulation that occurred prior to the death of male #6547. Pups #6595 and

#6678 were not the offspring of any male associated with this group, indicating another extra-pair copulation. The male helper associated with this group (#6584) could not have been the unknown father because he had conflicting alleles at three out of four loci that amplified. There were two incidences of incest involving female #6525. We believe she was a pup from 2010 based on capture information in 2011. Her father was likely #6547 and male #6524 was a pup from 2011 that was likely her brother, she reproduced with both individuals in 2012.

DISCUSSION

Our results are the first documentation of social and genetic polygyny in San Joaquin kit foxes. While social polygyny has been documented in desert kit foxes (V. m. arsipus;

Egoscue 1962), there are no recent documentations of polygyny in desert or San Joaquin kit foxes. The likely primary cause of this shift from social monogamy to social polygyny is an

Polygyny in Urban San Joaquin Kit Fox increase in the availability of resources in the urban environment. The Resource Dispersion

Hypothesis (RDH) suggests that a pair of carnivores may tolerate additional group members when resources are abundant as long as the pair has sufficient resources throughout periods of limited availability (von Schantz 1984, Zabel and Taggart 1989, Baker et al. 2004). Urban environments tend to have more consistent and abundant food and cover for small canids compared to natural lands (Cypher and Frost 1999, Gosselink et al. 2010). As a result, dominant females may be more tolerant of conspecifics and even allow subordinate females to reproduce within their home range, assuming there is no detriment to the reproductive success of the dominant female (Zabel and Taggart 1989). In urban red foxes (V. vulpes), dominant females and subordinate females reproduced in 100% and 56% of breeding opportunities, respectively, indicating no effect on dominant female reproduction (Baker et al. 2004). With plentiful food and no decrease in dominant female reproductive success, the shift from monogamy to polygyny is not unexpected.

Density may be another factor influencing a shift in breeding system. In the urban environment, there is low dispersal potential because patches of suitable habitat may be fragmented and are often already occupied (Gosselink et al. 2010). Low dispersal potential results in a higher incidence of philopatric young (Elmhagen et al. 2014) and an increase in the number of social interactions between individuals (Murdoch 2008). High interaction rates and high population density can lead to an increase in the frequency of polygynous groups (Kitchen et al 2006). In swift fox (V. velox) populations, all groups in a low density population were made up of monogamous pairs, while 30% of groups in a high density population were polygynous trios (Kamler et al. 2002). The disadvantage to this strategy is that members of a breeding pair are not often closely related, but philopatric young are

Polygyny in Urban San Joaquin Kit Fox typically the offspring of the pair (Ralls et al. 2007). We did document incestuous reproduction between a father and a daughter and between potential siblings at Bakersfield

College. There could be an increased incidence of inbreeding under urban circumstances. It may be that foxes who are unable to find a breeding territory of their own or an unrelated mate are choosing to reproduce with related individuals as a preferred alternative to not reproducing.

Extra-pair paternity occurs frequently in canids and is a safeguard against inbreeding because offspring are not as closely related to one another as offspring of genetically monogamous pairs (Baker et al. 2004, Cameron et al. 2011). We documented extra-pair copulations in both polygynous groups. One group had a minimum of four fathers genetically and the other had a minimum of two. Our documentation of extra-pair paternity in San Joaquin kit foxes was consistent with recent studies that have detected genetic polygamy in other small vulpine canids that are thought to be mostly monogamous (e.g., red foxes, Baker et al. 2004; swift foxes, Kitchen et al. 2006; arctic foxes, V. lagopus, Cameron et al. 2011). A reproducing female engaging in extra-pair copulations may risk paternal care by the cuckolded male (Baker et al. 2004, Kitchen et al. 2006), but based on our observations male San Joaquin kit foxes may not be able to detect which offspring are unrelated. This is consistent with results indicating that swift fox males are unable detect nonparentage as well

(Kitchen et al. 2006). Without a risk of losing paternal care, promotion of outbreeding is strictly beneficial to the female because it helps control the frequency of inbreeding by introducing new genes from members of other family groups (Cameron et al. 2011). Extra- pair copulations are detrimental to the cuckolded male, who spends his time and energy raising offspring for which he receives no inclusive fitness benefit.

Polygyny in Urban San Joaquin Kit Fox

A substantial advantage to a polygynous breeding system is the opportunity for communal litters and alloparental care (Elmhagen et al. 2014). The Polygyny Threshold model predicts that the polygyny threshold is reached when the cost of sharing a male with another female is exceeded by the benefit of raising offspring cooperatively (Zabel and

Taggart 1989). The process of nursing and providing food to weaned pups puts an immense burden on mothers (Kleiman 1977). In our study, we documented at least one case of allosuckling, which would reduce the burden on any one female. Communally raising litters may also allow one mother to remain at the den while the father and the second mother forage and provision food to pups. In swift foxes, more adult group members resulted in an increase in the amount of time an adult was present at the den (Elmhagen et al. 2014). This provides greater den defense, as well as reduces the amount of time each mother must remain away from the den where she is more exposed to danger. Also, because additional group members tend to be offspring of the breeding pair, a mother allowing her offspring to reproduce within her range also increases the ultimate reproductive success of the mother

(Cameron et al. 2011).

Our results showed the occurrence of polygyny in two family groups of urban San

Joaquin kit foxes. However, the extent of a breeding system shift is unknown for the urban population overall. Further research into the frequency of occurrence of polygynous groups, as well as the extent of inbreeding could benefit conservation efforts for the species as a whole. Understanding the limitations for dispersal and the level of inbreeding could be informative for planning urban landscapes in a manner that could benefit kit foxes. Urban development could provide corridors that are more permeable to kit foxes to increase genetic flow across the population and increase the fitness of the population as a whole.

Polygyny in Urban San Joaquin Kit Fox

ACKNOWLEDGEMENTS

We would like to thank the Endangered Species Recovery Program of California

Western Section and San Joaquin Chapter of The Wildlife Society and the Student Research

Scholar Program of California State University, Bakersfield for providing student grants to purchase materials and equipment for camera stations, and the Smithsonian Conservation

Biology Institute for general support. We also thank David Germano and Carl Kloock for reading an earlier draft of the manuscript.

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Polygyny in Urban San Joaquin Kit Fox

Table 1. Individuals in each socially polygynous San Joaquin kit fox (Vulpes macrotis mutica) group during the 2012 breeding season in Bakersfield, California.

Group ID Mother Father Helper # Pups Pups Sampled

CSUBS 6700♀ 6065♂ 6585 6 6593♀

6309♀ 6594♀

6676♂

U177

BC2012 6566♀ 6524♂ 6584♂ 10 6595♂

6525♀ 6596♀

6606♀

6607♂

6677♀

6678♂

Polygyny in Urban San Joaquin Kit Fox

Table 2. CERVUS likelihood of maternity and paternity of San Joaquin kit fox (Vulpes macrotis mutica) pups from the CSUBS group at California State University, Bakersfield, during the 2012 breeding season.

Pup ID Mother Criterion Father Criterion

6593 6700 Pair Likelihood >80% 6065 Pair Likelihood >80%

6594 6309 Mother Likelihood >95% Unknown

6676 6700 Mother Likelihood >95% Unknown

U177 6700 Pair Likelihood >80% 6065 Pair Likelihood >80%

Polygyny in Urban San Joaquin Kit Fox

Table 3. CERVUS likelihood of maternity and paternity of San Joaquin kit fox (Vulpes macrotis mutica) pups from the BC2012 group at Bakersfield College during the 2012 breeding season.

Pup ID Mother Criterion Father Criterion

6595 6566 Mother Likelihood >95% Unknown

6596 6566 Mother Likelihood >95% 6524 Father Likelihood >95%

6606 6525 Mother Likelihood >95% 6524 Father Likelihood >95%

6607 6525 Mother Likelihood >95% 6547 Pair Likelihood >80%

6677 6566 Pair Likelihood >80% 6523 Pair Likelihood >80%

6678 6566 Mother Likelihood >95% Unknown

Polygyny in Urban San Joaquin Kit Fox

Figure 1. Size difference in two age classes of San Joaquin kit fox (Vulpes macrotis mutica) pups representing two litters at the same den taken from a camera station at California State

University, Bakersfield during the 2012 breeding season. The kit fox in the background is a dye marked and collared adult male fox.

Figure 2. Pictures of both mothers from the San Joaquin kit fox (Vulpes macrotis mutica) family group at California State University, Bakersfield during the 2012 breeding season. A)

Female 6309 showing enlarged teats and hair loss from nursing; B) Female 6700 showing enlarged teats and rufus belly fur from nursing; C) Female 6700 nursing the younger litter of pups on the night of April 1, 2012 (pups are standing on their back feet); D) Female 6700 nursing pups from the older litter on the night of April 1, 2012 (pups are sitting fully on the ground and leaning to nurse).

Figure 3. A picture captured on a remote camera of both San Joaquin kit fox (Vulpes macrotis mutica) mothers showing signs of nursing at Bakersfield College during the 2012 breeding season.

Figure 4. A picture captured by remote camera showing nine out of 10 San Joaquin kit fox

(Vulpes macrotis mutica) pups at Bakersfield College during the 2012 breeding season.

Polygyny in Urban San Joaquin Kit Fox

Figure 1

Polygyny in Urban San Joaquin Kit Fox

Figure 2

Polygyny in Urban San Joaquin Kit Fox

Figure 3

Polygyny in Urban San Joaquin Kit Fox

Figure 4

CHAPTER 5

SUMMARY OF RESEARCH AND CONSERVATION IMPLICATIONS

Urban environments offer both challenges and opportunities for certain wildlife species. Challenges include unique hazards and threats (e.g., toxic substances, vehicular traffic, high densities of domestic dogs and cats, etc.) not typically encountered in non-urban environments (Cypher 2010). Opportunities can include fewer natural predators and an abundance of food due to anthropogenic resources (Cypher and Frost 1999, Cypher 2010).

Despite being endangered, the San Joaquin kit fox apparently has some capacity to adapt to urban environments, and consequently, a large and robust population occurs in Bakersfield

(Cypher 2010). The altered ecological conditions of an urban habitat can affect social ecology, and this provided me an opportunity to examine the response of a species to such conditions. In this study, I investigated parental care among urban kit foxes, and also gathered information on mating system and research techniques.

Behavioral Survey Methods

I found that direct observations provide the most accurate information on San Joaquin kit fox (Vulpes macrotis mutica) den attendance and behavior. The greatest limitation when using this survey method is the decreased observer vigilance that comes with increased observation periods. Camera stations can provide information over longer periods of time and under conditions that are not conducive to direct observation, but cameras significantly underestimate the amount of time each fox spends at the den. The underestimation in den attendance time is likely due to the limited field of view and failure to trigger. Cameras are

also likely to underestimate relative parental care contributions when rapidly occurring events, such as provisioning, fail to trigger the camera. While cameras do not provide the most accurate den attendance and care information, they can be very useful in providing permanent documentation of behaviors that are not typically observed. When conducting a study monitoring behavior over time, either method could be used to gather valuable information, depending upon the study objectives, subject animals, and observation conditions.

I found that proximity logging collars were unreliable in the den attendance study. In controlled studies on northern raccoons (Procyon lotor), proximity collars lost transmission power the closer they were to the ground (Prange et al. 2011). While proximity logging collars may not be useful for den attendance in fossorial species, they could be used on urban

San Joaquin kit foxes to obtain valuable information on social interactions, mating systems, and the potential for disease transmission.

Relative Roles of Adult Group Members to Pup Rearing

My results confirm that mothers play a critical role in pup rearing for urban San

Joaquin kit foxes. Until the pups can be weaned, mothers are essential in providing nourishment to the young via lactation. After the pups are weaned, mothers still play a large role in pup care. Mothers spend more time at the den than either fathers or helpers and are the primary care giver. While fathers do not provide as much direct care as mothers, they still contribute the same amount of provisioning throughout the breeding period. Fathers also provision mothers during lactation and early weaning which allows mothers to spend more time at the den with the pups that depend on her care. As a result, mothers are less exposed

to the risk of death by predators or, in the case of the urban environment, vehicle strikes.

Fathers also seem to play a larger role in den defense than mothers and while they spend very little time at the den compared to mothers, the majority of their time at the den is spent guarding pups.

Helpers seem to play a variety of roles in the urban environment. Most groups included helpers, but they seem to remain in their natal range as a result of the increased food availability in an urban environment. The role of helpers appears to be supplemental as parents are clearly capable of raising litters on their own. Helpers spent significantly less time at the den than mothers and they provisioned significantly less than mothers or fathers.

Even though helpers in the urban environment provide little to pup rearing, any assistance they do contribute will reduce the energy, time, and risk investment of the parents. Helpers may not contribute parental care while both parents are present, but it is possible that they may increase their contribution should one of the parents die or become incapacitated.

Parents may allow helpers to remain in their natal range as a form of insurance in the event that the parents are unable to care for the pups. Helpers may also benefit from remaining in their natal range and interacting with pups to ensure their place in the social hierarchy in the event that their natal territory becomes available.

Abundant resources, high survival rate, and high reproductive rates combined with low dispersal potential contribute to more individuals in each family group (Cypher 2010).

More individuals per group means higher density and more interactions within groups, as well as between adjacent groups (Murdoch et al. 2008). Understanding how group formation and social interactions occur can help determine the likelihood of disease transmission and spread, as well as the best intervention procedure to respond to outbreaks. Demographic and

behavioral information contribute to our understanding of population size, reproductive rates, mortality, and survival. Understanding the roles of adult group members can also inform decisions regarding prospective individuals for reintroduction to suitable unoccupied areas.

Further behavioral research on the urban population, particularly in direct comparison to natural populations, would contribute to understanding the viability and sustainability of the urban population.

Communal Litters

I observed social polygyny in two family groups of urban San Joaquin kit foxes. One of these groups constituted the first documented case of two females reproducing with one male in San Joaquin kit foxes. While both groups in my study were socially polygynous, one group was genetically polygynous and both groups were genetically polyandrous. Fathers can increase their reproductive success by reproducing with multiple females whenever possible. Multiple cases of extra-pair copulations were demonstrated in my genetic results, indicating that Mothers are not concerned with losing paternal care from cuckolded males.

Mothers increase the genetic diversity of their litters through extra-pair copulations. Extra- pair copulations serve as a form of protection from inbreeding by introducing genetic material into the family group. While extra-pair copulations were common, relatedness between all individuals was very high and breeding occurred between some parents and offspring. The urban population could suffer from inbreeding depression, but further research is needed to determine the magnitude of this threat. Urban planning could potentially develop corridors to encourage the spread of genes through extra-pair copulations to insure genetic diversity and increase the fitness of this important population.

Conservation Implications

The principal challenge to the conservation of the San Joaquin kit fox is protecting suitable habitat for the remaining population. The majority of existing kit fox habitat is privately owned and currently unprotected (Cypher et al. 2013). Furthermore, the remaining undeveloped land with suitable habitat is in high demand for agricultural, industrial, and urban development, as well as for conservation efforts (Cypher et al. 2013). The increase in demand for undeveloped land has led to a higher cost per acre, which further limits the ability to protect habitat for kit foxes in the San Joaquin Desert (Cypher et al. 2013).

Amazingly, the San Joaquin kit fox has been successful in adapting to life in an urban environment and there is a robust and viable population living in the city of Bakersfield

(Cypher 2010, Cypher et al. 2013). With the difficulties that exist in protecting habitat for kit foxes, it is even more crucial to protect the stable urban population.

Studying populations in an altered ecosystem can serve as a natural experiment when comparing behavioral, ecological and demographic traits to populations living in unaltered habitat. There is also a value to conserving populations in altered environments because they may be less affected by environmental stressors (e.g., prolonged drought conditions) that can severely hinder, and even cause local extirpations, in natural populations. Understanding differences between these populations is crucial to determine the best conservation efforts to address unique stressors for each area. Further behavioral, ecological, and demographic research on natural and urban populations of San Joaquin kit foxes could help us develop better management practices to protect the species as a whole.

LITERATURE CITED

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John Hopkins University Press, Baltimore, Maryland.

Cypher, B. L., and N. Frost. 1999. Condition of San Joaquin kit foxes in urban and exurban

habitats. The Journal of Wildlife Management 63:930–938.

Cypher, B. L., S. E. Phillips, and P. A. Kelly. 2013. Quantity and distribution of suitable

habitat for endangered San Joaquin kit foxes: conservation implications. Canid

Biology & Conservation 16:25–31.

Murdoch, J. D., K. Ralls, B. Cypher, and R. Reading. 2008. Social interactions among San

Joaquin kit foxes before, during, and after the mating season. Journal of Mammalogy

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