Behavior and Spatial Ecology of the Harris' Antelope Ground Squirrel (Ammospermophilus harrisii)
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Authors Burnett, Alexandra D.
Publisher The University of Arizona.
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Link to Item http://hdl.handle.net/10150/636507 BEHAVIOR AND SPATIAL ECOLOGY OF THE HARRIS’ ANTELOPE GROUND
SQUIRREL (Ammospermophilus harrisii)
by
Alexandra Burnett
______
Copyright © Alexandra Burnett 2019
A Thesis Submitted to the Faculty of the
SCHOOL OF NATURAL RESOURCES & THE ENVIRONMENT
In Partial Fulfillment of the Requirements
For the Degree of
MASTER OF SCIENCE
NATURAL RESOURCES – WILDLIFE CONSERVATION & MANAGEMENT
In the Graduate College
THE UNIVERSITY OF ARIZONA
2019 2
THE UNIVERSITY OF ARIZONA GRADUATE COLLEGE
As members of the Master’s Committee, we certify that we have read the thesis prepared by: Alexandra Burnett titled:
and recommend that it be accepted as fulfilling the thesis requirement for the Master’s Degree.
______Date: ______Sep 9, 2019 John L Koprowski
______Date: ______Sep 10, 2019 Michael Bogan
______Date: ______Sep 9, 2019 bret pasch
Final approval and acceptance of this thesis is contingent upon the candidate’s submission of the final copies of the thesis to the Graduate College.
I hereby certify that I have read this thesis prepared under my direction and recommend that it be accepted as fulfilling the Master’s requirement.
______Date: ______Sep 9, 2019 John L Koprowski T hesis Committee Chair
School of Natural Resources and the Environment
3
Acknowledgments
I would like to sincerely thank my graduate advisor, Dr. John Koprowski for providing the opportunity for me to complete my master’s degree at the University of Arizona, as well as his support and guidance throughout my thesis project. I would further like to thank my committee members, Dr. Bret Pasch and Dr. Bill Mannan, for their availability and support along the way.
Special thanks to Sarah Hale, Melissa Merrick, and Vicki Greer for training support and field assistants, Alexis Blair, Sandy Slovikosky, Helena Yomantas, Anne-Laure Blanche, Megan
Bethel, Nicole Bokanowski, Brandon Mayer, and Eduardo Gracia for countless hours of field support and data input. Thanks to M. Merrick and M. Mazzamuto for guidance with software and data analysis, and V. Greer for logistical support with permitting, equipment, and vehicles. I am grateful for the support and guidance provided by the Koprowski Conservation Research
Laboratory throughout my time in Arizona. Finally, I thank my partner, Kevin Wagner, and my parents, friends, and family, for their support and patience throughout my thesis project.
Alexandra D. Burnett
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Table of Contents
List of Figures……………………………………………………………………………………..5
Abstract……………………………………………………………………………………………8
Chapter 1: Introduction…………………………………………………………………………..10
Chapter 2: Present Study…………………………………………………………………………15
Summary of Conclusions…………………………………………………………………………15
Literature Cited……………………………………………………………………………….….17
Appendix A: On using a nonhibernating squirrel to inform models of complexity……..………23
Introduction………………………………………………………………………………………24
Methods…………………………………………………………………………………………..30
Results……………………………………………………………………………………………33
Discussion………………………………………………………………………………………..36
Appendix B: Effects of shrub encroachment on antipredator behavior…………….……………59
Introduction………………………………………………………………………………………60
Methods………………………………………………………………………………………..…62
Results……………………………………………………………………………………………66
Discussion………………………………………………………………………………………..67
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List of Figures
A.1 Figure 1: Average home range size (ha) of Ammospermophilus harrisii in southeastern
Arizona throughout 2017 and 2018. Data are divided by the mating season (Jan-Apr), juvenile season (May-Aug), and nonbreeding season (Sep-Dec). There are no statistical differences of home ranges sizes among season or sex.………………………………………………………54
A.1 Figure 2: 95% and 50% kernel densities of individual antelope squirrels
(Ammospermophilus harrisii) in southeastern Arizona. Home ranges of a) all individuals found within study site 2 and 3 of the Santa Rita Experimental Range in which we collected enough points for a home range. Males are represented by warmer colors (red, orange, yellow) and females are represented by cooler colors (green, blue, purple). Individuals overlapped intra- and intersexually: b) female (green)-male (red) overlap during the months of June-August 2018, b) female-female overlap during the months of June-August 2017, and c) male-male overlap during the months of October and November 2017…………………………………...………………...55
A.1 Figure 3: Average number of antipredator vocalizations given by Harris’ antelope ground squirrels (Ammospermophilus harrisii) detected per hour in each month of 2017 and 2018
(pooled) in southeastern Arizona. Dashed lines represent seasonal boundaries. Both years start with a low hourly rate of antipredator vocalizations until April in the mating season (months 1-
4), remain at a moderate level through the juvenile season (months 5-8), and peak in the nonbreeding season after juvenile dispersal (months 9-12) …………………………………...56
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A.1 Figure 4: Spectrogram of an adult Harris’ antelope squirrel (Ammospermophilus harrisii) call given in southeastern Arizona, looking at frequency (kHz) over time(s). Color represents amplitude; warmer colors represent higher amplitudes. Calls feature a trill with high-frequency overtones that descends in amplitude over time. Squirrels frequently give calls repeatedly, in bouts……………………………………………………………………………………………...57
A.1 Figure 5: Spectrogram of a juvenile Harris’ antelope squirrel (Ammospermophilus harrisii) call in the presence of a Western diamondback rattlesnake (Crotalus atrox) in southeastern
Arizona. Frequency (kHz) is represented on the y-axis and time (s) is represented on the x-axis.
Chirps consist of a short, broadband syllable that is repeated.…………………………………..58
A.2 Figure 1: Selection indices of burrow locations of Ammospermophilus harrisii in southeastern Arizona within each vegetation class based on direct observations compared to average availability across study sites. We included all burrow locations that were used by marked individuals at least once (n=22 animals, 192 total burrow locations). Negative values indicate selection against, positive values indicate selection for the vegetation class. Burrows beneath Opuntia were used most commonly. Prosopis and Celtis were the next most frequent genera for burrowing beneath, though at a significantly lower frequency. Individuals also used burrows beneath Senegalia and Cylindropuntia, as well as Ferocactus, Ephedra, and
Heteropogon……………………………………………………………………………………78
A.2 Figure 2: Selection indices of foraging items within each vegetation class based on direct observations of feeding compared to average availability across study sites (n=47 direct
7 observations of feeding). Negative values indicate selection against, positive values indicate selection for the vegetation class. We observed Ammospermophilus harrisii feeding on flowers and fruits of Opuntia the vast majority of the time in southeastern Arizona. The next most frequently observed food source was grass seeds (Poaceae)…………………………………...79
A.2 Figure 3: Selection indices of alarm calling locations within each vegetation class compared to average availability of each vegetation class across study sites. Only observations in which the plant the individual was calling from was positively identified were included in the analyses
(n=18 observations). Negative values indicate selection against, positive values indicate selection for the vegetation class. Ammospermophilus harrisii called from mesquite trees (Prosopis) in
38.8% of known alarm call locations in southeastern Arizona. Prickly pear (Opuntia) were the next most common observed alarm call locations (33.3%), and then cholla (Cylindropuntia,
11.1%) and hackberry (Celtis, 11.1%)
…………………………………………………………...80
A.2 Figure 4: Selection indices of active individuals within each vegetation class compared to average availability across study sites (n=22 individuals, 257 observations). Negative values indicate selection against, positive values indicate selection for the vegetation class.
Ammospermophilus harrisii in southeastern Arizona selected for bare ground slightly avoided shrub and cacti………………………………………………………..…………………81
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Abstract
Ground squirrels provide a valuable model system for studying both theoretical and applied questions in behavioral ecology. High variability among species ecology imposes selective forces that result in vast differences in social and communication systems. Resource distribution, body size, and kin selection drive social evolution, leading to hypotheses linking larger body size and shorter active periods to greater sociality, which in turn has implications for strategies that may have interesting implications for models of social and communicative complexity. We conducted a two-year study of a nonhibernating squirrel, Ammospermophilus harrisii, examining social and antipredator behavior to test models of complexity. If nonhibernating squirrels comply with predictions of social hypotheses, A. harrisii should be nonsocial and solitary during the winter due to low body size and long active period. We further tested predictions of communicative complexity relating to call function and variability. Our results suggest that antipredator vocalizations may serve multiple functions and vocalizations contain graded variation that may hold additional layers of information. We found that squirrels were not always solitary during winter months, which could explain evidence of kin selection in calling behavior. Nonhibernating squirrels therefore offer insight into potential mechanisms driving variation in communicative complexity.
We also used A. harrisii to answer conservation questions about rapid environmental changes. Habitat degradation and loss is a significant driver of extinction, limiting species resilience to rapid change and resulting in widespread declines. Behavior is often flexible and context-dependent, allowing researchers to gauge wildlife responses to disturbances and determine whether population decline will result. Monitoring whether novel behaviors arise or survival strategies falter can be the first indicator of a potential threat. Further, understanding
9 how animals respond to environmental stimuli is useful for predicting responses to future disturbance. The Harris’ antelope ground squirrel is representative of many species adapted to open, arid environments in that they rely on vigilance and antipredator signals to evade predators. However, desert grasslands on nearly every continent are shifting from open grassland to mesquite, a phenomenon known as shrub encroachment. Shrub encroachment can alter foraging behavior and communication, and a shift in species composition can ultimately ensue.
We conducted a two-year study of A. harrisii in the Santa Rita Mountains, monitoring individuals in areas of high and low velvet mesquite (Prosopis velutina) cover to assess reliance on mesquite as a resource and quantify differences in antipredatory behavior. We found evidence that the presence of mesquites may alter or reduce antipredator behaviors that may affect adult and juvenile survival. A. harrisii were also found to select against woody vegetation and areas of thick vegetation. Thus, shrub encroachment may have adverse effects on antelope squirrel populations and limit future distribution.
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Chapter 1: Introduction
Behavioral research has a rich history in wildlife studies that has led to the discovery of a vast array of diversity in survival and reproductive strategies. Decades of behavioral research have provided a framework that allows researchers to use behavior as a tool to understand how environmental selective pressures evolve behavioral adaptations. Many conventional questions regarding human evolution can be answered by turning to animal systems. For example, the evolution of human society has long been regarded as unique in complexity, however, research into other animal societies has revealed that non-human animals also exhibit a remarkable spectrum in their social relationships and communication. Examining these dynamic characteristics across an array of different ecologies allows evolutionary biologists a means to understand what processes shape these complex behaviors. In an applied setting, behavior is useful as a way of gauging the status of an animal population because it can respond to environmental changes within short time frames but has lasting effects on reproduction and survival. Changes in wildlife behavior that are maladaptive or reduce survival may be indicative of larger issues on the landscape and can serve as a warning system to managers. Behavioral monitoring is becoming increasingly important as climate change brings rapid landscape changes that can decimate populations before multi-year reproductive data can be sufficiently gathered to identify problems. Behavior is therefore an important tool for understanding the underlying principles of animal societies, including that of humans, as well as how anthropogenic actions can put populations at risk.
Of particular interest to many researchers is the evolution of seemingly altruistic or cooperative behaviors, such as sociality and communication. Further study of animal systems has unveiled a large spectrum of social and communication behaviors both within and among taxa
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(Michener 1984, Blumstein 2007, Schel et al. 2010, Bouchet, Blois-Heulin, and Lemasson
2013). Many of the underlying components of complex communication networks, such as referential signaling (‘words’) and ordering (‘syntax’), are most often seen in species with greater social cohesion (Cheney and Seyfarth 1980, Zuberbühler 2000, Blumstein 2007).
However, hints of network structure are apparent across a variety of social and nonsocial contexts as researchers begin to uncover how interactions between selective pressures can shape communication systems overall. Signal meaning or function can vary based on the presence or absence of additional signals and one signal can have multiple functions directed toward multiple receivers (Hebets et al. 2016). Social and communication behaviors are constantly under selection of physiological, phylogenetic, genetic, and both abiotic and biotic environmental interactions. Thus, a more holistic, systems approach is needed when answering proximate and ultimate questions. The antipredator communication system of ground squirrels has been used to model social (Armitage 1981, Rayor and Armitage 1981, Blumstein and Armitage 1998) and communicative complexity (Blumstein and Armitage 1997b, Pollard and Blumstein 2012) and is frequently cited as evidence for the social complexity hypothesis, in which greater sociality is hypothesized to lead to greater communicative complexity (Freeberg, Dunbar, and Ord 2012,
Sewall 2015). Antipredator vocalizations used by squirrels likely function as both a predator deterrent and a warning to offspring (Blumstein and Armitage 1997a, Digweed and Rendall
2009, Fuong, Maldonado-Chaparro, and Blumstein 2015) and phylogenetic studies show that predator deterrence likely evolved first in Rodentia (Shelley and Blumstein 2005). However, kin selection plays a large role in calling behavior and call structure in a number of species (Sherman
1977, Dunford 1977, Blumstein et al. 1997), resulting in a majority of research focus devoted toward the social implications of antipredator vocalizations in hibernating squirrels that live in
12 large family groups (Ackers and Slobodchikoff 1999, McCowan and Hooper 2002, Blumstein,
Verneyre, and Daniel 2004, Matrosova et al. 2010, Pollard 2011). Nonhibernating squirrel exhibit sociality that may vary throughout the year (Karasov 1983, Williams et al. 2009) and can be readily observed in both social and nonsocial contexts. Antipredator communication systems in nonsocial, nonhibernating rodents could provide insight into how selective pressures other than sociality may shape communication structure due to minimized effects of kin selection.
Behavior not only offers researchers a glimpse into the evolutionary process, but also provides a useful gage for studying the effects of rapid environmental change. Animals rely on communication to find food and mates, minimize predation, and reinforce social bonds.
Disruption in communication systems can therefore lead to a breakdown in reproduction and survival. Successful transmission of signals between signalers and recipients depends on the surrounding environment, however, vast landscape changes over very short time intervals affect the transmission of visual, acoustic, and olfactory signals and alter the context in which individuals may communicate. Antipredator signals typically depend on specific environmental qualities in order for both parties to benefit from the signal (Wiley and Richards 1978, Forrest
1994, Briefer et al. 2009). Stotting is an antipredator behavior in Artiodactyla that signals to predators when they’ve been spotted and communicates their fitness to the predator, deterring further pursuit (Caro 2004). Perceived predation risk can influence habitat use and may prompt herbivores to use open environments preferentially (Valeix et al. 2009). Rodents living in open habitats that experienced environmental changes resulting in less visibility increased perceived predation risk and altered foraging behavior (Arenz and Leger 1997, Wheeler and Hik 2014).
Thus, prey may rely on open visual environments to detect and display to the predator as well as for the predator to detect and assess such signals (Lima 1988). Rodents are unlikely to signal
13 unless they are able to track the predator before betraying their location with attention-grabbing behavior such as tail flicking or alarm calling (Blumstein and Armitage 1997a, Shelley and
Blumstein 2005, Owings 2010). Rodents in grasslands or desert scrub that have evolved antipredator cues for open environments may therefore experience detrimental effects when environmental change prevents normal antipredator behavior from occurring (Arenz and Leger
1997, Wheeler and Hik 2014, Akunke and O’Connell 2017). Shrub encroachment is an ongoing problem in arid grasslands worldwide (Archer 1995, Van Auken et al. 2010), and many areas, including Southwest North America, are already experiencing biodiversity losses due to shrub encroached habitat (Ratajczak et al. 2012, Smit and Prins 2015). Examining the effects of shrub encroachment on antipredator behavior and habitat selection may shed light onto the mechanism of population decline and possible management strategies that may help mitigate or minimize species decline before local extirpation.
Ammospermophilus harrisii offers an excellent model to answer the theoretical and conservation questions outlined above. Ammospermophilus harrisii is a desert-dwelling sciurid that emits variable alarm calls but is thought to be solitary, providing a good system to fill gaps in current models of sociality and communication. Individuals are active year-round, providing an opportunity to study antipredator vocalizations in both social contexts, in which juveniles are present, as well as nonsocial contexts. By observing calling behavior with and without juvenile presence, we can identify signal receivers and call function, offering insight into selective forces other than sociality could shape communication systems. A. harrisii is also endemic to the
Sonoran Desert but is generally associated with more upland desert scrub, which is currently facing shrub encroachment of velvet mesquite (Prosopis velutina) (Archer 1995, Bahre and
Shelton 1993). In the Santa Rita Experimental Range, A. harrisii occur across an elevational
14 gradient that exhibits variable levels of shrub encroachment. This provides a natural experiment allowing us to compare calling behavior between shrub encroached and areas that remain open.
If antipredator behavior is reduced in shrub encroached areas, predation may increase and population numbers may decline. These findings would have broader implications for other desert and grassland species that have evolved antipredator strategies that rely on open environments, many of which threatened or endangered.
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Chapter 2: Present Study
This thesis is a compilation of two manuscripts prepared for publication, located in
Appendices A and B. Appendix A: On using a nonhibernating squirrel to inform models of complexity, formatted for Animal Behaviour, discusses the sociality and communication of
Harris’ antelope squirrel (Ammospermophilus harrisii) in relation to the study of complexity. We focus on the function of antipredator vocalizations and subsequent implications for the current structure of the antipredator communication system. Appendix B: Effects of shrub encroachment on antipredator behavior, formatted for Conservation Biology, describes avoidance of shrub cover by squirrels and shows how shrub encroachment can reduce predator-deterring behavior, which could indicate higher foraging costs and altered predator-prey interactions in dense areas.
Below is a summary of the conclusions of these studies.
Summary of Conclusions
We used the Harris’ antelope ground squirrel (Ammospermophilus harrisii) to inform models of social and communicative complexity as well as management decisions relating to shrub encroachment. In our first study, we found that A. harrisii vocalizes year-round but that callers are female-biased. We also found that A. harrisii emits at least two different vocalizations in antipredator contexts and that trill vocalizations contained a large amount of variation within and between call bouts. Our findings coincide with other research that suggests that antipredator vocalizations are likely used for both a predator deterrent and a warning to offspring, and vocalizations may therefore be shaped by kin selection. Further, species that are typically classified as solitary may still benefit from neighbors and maintain social bonds throughout their lifetime. Thus, social or kin selection may explain some of the graded variation observed. In a separate study, we found that antipredator behavior in a low-density stud site differed from our
16 shrub encroached study site. We also found that squirrels preferred desert vegetation and bare ground, avoiding woody patches. Shrub encroachment may therefore reduce antipredator behavior adapted to open environments, potentially decreasing survival. This could further imperil grassland species that are already threatened or endangered. Additionally, avoidance of woody patches could indicate that shrub encroachment may further alter population distribution if squirrels select against such areas when dispersing. Other open-habitat species may also exhibit similar avoidance, potentially due to increased costs of vigilance (Arenz and Leger 1997) or decreased likelihood of survival (Akunke and O’Connell 2017) due to reduced visibility.
Managers should employ a variety of tactics to maintain open habitat for grassland and upland desert species (Thomas and Goodson 1992, Twidwell et al. 2013). Further, travel corridors between areas of high biodiversity should be created and maintained to encourage gene flow and increase resilience to climate change.
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Appendix A: Use of a nonhibernating squirrel (Ammospermophilus harrisii) to inform models of complexity
Burnett, Alexandra D.*, Koprowski, John L.*
*School of Natural Resources and the Environment, University of Arizona, Tucson, AZ, USA
Ground squirrels offer a fascinating model for studying the evolution of sociality and communication. High variability among species ecology imposes selective forces that result in vast differences in social and communication systems. Resource distribution, body size, and kin selection as main drivers of social evolution, which in turn has implications for the evolution of communication. Conspecifics in many ground squirrel species respond to antipredator vocalizations and sociality functions as a strong selective force favoring more informative antipredator vocalizations. However, comparatively little research exists on identifying other selective forces acting on call structure and function, particularly on communication systems with multiple potential receivers. If predators are the intended receiver of antipredator vocalizations, sociality may not account for all observed variation in antipredator communication systems. We conducted a two-year study to determine the potential function of antipredator vocalizations in a non-hibernating squirrel, Ammospermophilus harrisii. If non-hibernating squirrels comply with predictions of sociality models, A. harrisii should remain solitary throughout the year, exhibit non-overlapping home ranges, and display neutral or avoidant behavior toward other individuals. We further hypothesized that if calls function as a predator- deterrent and are only given when predators are present, callers should be of equal sex ratio and vocalize year-round. If calls function primarily as a warning to offspring, callers should be predominantly female and vocalize only when juveniles are above ground. Additionally,
24 vocalizations should exhibit little variation due to low sociality. We found that callers were predominantly female but vocalized throughout the year. We also found that call bouts varied considerably in duration, amplitude, rate, and call type, which could hold additional layers of information. Our results suggest that antipredator vocalizations may function as a predator deterrent, however, calling behavior may still be shaped by kin selection in solitary species. If antipredator vocalizations have multiple functions and multiple receivers, a number of drivers are likely affecting the evolution of complexity in antipredator vocalizations in ground squirrels.
Organisms exhibit a rich diversity of strategies and behaviors to maximize fitness and ensure survival. In many animal taxa, developing effective, evolutionarily stable strategies depends on coping with tradeoffs that result in the evolution of complex behaviors (Alexander
1974, Arnold 1992). A recent surge of interest in the evolution of complexity and the resulting emergent interactions between system components (Fischer, Wadewitz, and Hammerschmidt
2017, Kappeler et al. 2019, Patricelli and Hebets 2016) has resulted in a systems approach to the study of complex behaviors (Bradbury and Vehrencamp 2014, Fischer et al. 2017, Hebets et al.
2016). Complexity is composed of nonlinear, dynamic systems with interacting emergent properties (Bradbury and Vehrencamp 2014). Comparative analyses within and across phylogenetic clades have uncovered common patterns underlying complexity, focusing on behaviors related to cognition (Seyfarth and Cheney 2015), sociality (Armitage 1981, Benson-
Amram et al. 2016, Blumstein and Armitage 1998, Rayor and Armitage 1991), as well as communication (Bouchet, Blois-Heulin, and Lemasson 2013, Blumstein and Armitage 1997b,
Freeberg, Dunbar, and Ord 2012, Pollard and Blumstein 2012). Though some debate exists over the definition (Kappeler et al. 2019), quantification (Bergman and Beehner 2015, Fischer et al.
25
2017, Kappeler 2019, Peckre, Kappeler, and Fichtel 2019) and comparison of complexity across clades (Kappeler et al. 2019), communication systems that exhibit larger, more graded repertoires or vocalizations that serve multiple functions are generally considered more complex
(Blumstein 2007, Freeberg et al. 2012, Fischer et al. 2017, Hebets et al. 2016).
Complex behaviors, including social group formation, may form due to phylogenetics
(Shelley and Blumstein 2005), physiological and environmental constraints (Armitage 1981,
Blumstein and Armitage 1998, Jarman 1974, Michener 1984), and genetic influences (Alexander
1974, Hamilton 1964, Maynard Smith 1965, Sherman 1977). Because steep trade-offs must be overcome for sociality to be evolutionarily stable (Alexander 1974), predicting the circumstances under which complex social systems evolve is challenging. Sociality can evolve as a strategy to secure resources and ensure survival through times of scarcity, and resource distribution and availability have significant influences on reproductive ecology and social structure in ground squirrels. Mammalian species exhibit larger and more complex groups in geographic locations with patchy resources (Clutton-Brock 1989, Travis and Slobodchikoff 1993, Verdolin and
Slobodchikoff 2009) or short seasonal availability of resources (Armitage 1981, Michener 1984).
Armitage (1981) and Michener (1984) looked comparatively across species, finding that larger bodied species or species with shorter active periods delay dispersal, developing multi-year relationships with parents and siblings. These models focused predominantly on northern latitude species that use hibernation as a strategy to endure resource constraints. Species in arid environments with more variable resource distribution and availability, in turn, exhibit more variable behavioral strategies among species that may result in different social structures
(Dunford 1975, Karasov 1983, Munroe and Koprowski 2014, Waterman 1996). Sympatric species in arid environments can display alternative strategies to cope with seasonal resource
26 depletion, exhibiting both hibernating (i.e. Xerospermophilus tereticaudus; Neal 1965) or nonhibernating behaviors (i.e. Ammospermophilus harrisii; Neal 1965). Nonhibernating squirrels often still experience seasonal energetic constraints but remain active throughout the year, evolving unique social behaviors. Tree squirrels, which do not hibernate, face resource depletion and thermoregulatory constraints during winter months, that prompt solitary species to nest with neighboring squirrels during winter months (Edelman and Koprowski, 2007, Halloran and
Bekoff, 1994; Koprowski, 1996; Ramos-Lara and Koprowski 2012, Williams et al. 2013).
Ammospermophilus leucurus, a nonhibernating ground squirrel found as far north as Idaho, likewise share burrows with neighbors during winter months, likely to defray the cost of thermoregulation (Karasov 1983). Nonhibernating ground squirrels living in arid regions of
Africa and North America may live in small groups with isolated burrows (Xerus rutilus, O’Shea
1976; Ammospermophilus harrisii, Chew and Chew 1930, Neal 1965; Xerospermophilus tereticaudus, Neal 1965, Bradley 1967) or large family groups (Cynomys ludovicianus,
Hoogland 1983; Xerus inauris, Waterman 1995). Though fewer studies are available, nonhibernating species offer an opportunity to inform models of sociality using species that lack obligatory constraints due to hibernation but must still cope with energetic constraints during wintertime.
The antipredator vocalizations of ground squirrels can similarly serve as a model system for the evolution of communication (Blumstein and Armitage 1997b, Krams et al. 2012,
Pollard and Blumstein 2012). Comparative analyses show support for the social complexity hypothesis, which predicts vocal complexity to increase with greater sociality (Bouchet, Blois-
Heulin, and Lemasson 2013, Blumstein and Armitage 1997b, Krams et al. 2012, Pollard and
Blumstein 2012). Conspecifics glean information such as the type, direction, or urgency of threat
27 from variability in antipredator vocalizations (Rodentia: Leger and Owings 1978, Ackers and
Slobodchikoff 1999, Blumstein and Armitage 1997a, Blumstein and Daniel 2004, Weary and
Kramer 1995; Primate: Schel, Candiotti, and Zuberbühler 2010, Zuberbühler 2001). Many squirrel species further exhibit a female-biased ratio of callers, and reproductive females or females with relatives nearby are more likely to call (Dunford 1977, Hoogland 1983, Leger and
Owings 1978, Schwagmeyer 1980, Sherman 1977). These findings provide evidence that calls function as a warning to kin and kin selection is the principal mechanism driving call structure.
Though there is strong support for the social complexity hypothesis, communication structure and variability are constrained by physiological characteristics of both the caller and the receiver(s) (Guilford and Dawkins 1991), as well as the surrounding environment (Marten and
Marler 1977, Wiley and Richard 1978), which must be considered when evaluating proximate and ultimate drivers of vocalization structure (Patricelli and Hebets 2016, Peckre et al. 2019).
Signals must be detectable by receivers (Guilford and Dawkins 1991, Rowe 2013) and depending on the function or audience of signals, signal structure may be subject to opposing or coinciding evolutionary forces (Arnold 1992, Hunt et al. 2009, Krebs and Dawkins 1984).
Animal communication systems often include signals that have multiple functions (pluripotency:
Guindre-Parker et al. 2012, Manno et al, 2007), increasing the number of selective pressures shaping signal structure (Hebets et al. 2016, Hunt et al. 2009). In particular, signals directed toward both conspecific and heterospecific receivers would impose complex selection pressures that may constrain or select for variation. Thus, studying the signal of interest in a variety of contexts is imperative for understanding the structure and evolution of communication systems and evaluating complexity.
28
Research on antipredator vocalizations has largely focused on conspecific receivers, however, visual and acoustic antipredator signals across taxa are capable of altering predator behavior, prompting movement of the predator to a new location (Artiodactyla: Caro 2004;
Anseriformes: Woodland 1980; Columbiformes: Amorim and Dias 2019; Primate: Adams and
Kitchen 2018, Isbell and Binder 2016, Zuberbühler, Jenny, and Bshary 1999; Rodentia: Barbour and Clark 2012, Clark 2005). An additional hypothesis explaining alarm calling behavior is that prey can decrease the chances of a costly chase by signaling when the predator has been detected
(Hasson 1991, Sherman 1977, Woodland 1980). Phylogenetic studies that map antipredator vocalization behavior in Rodentia found that alarm calling was largely explained by the evolution of diurnality rather than sociality, further supporting the predator-deterrent hypothesis
(Shelley and Blumstein 2005). Antipredator vocalizations may accomplish both functions
(Blumstein and Armitage 1997a, Caro 2004, Digweed and Rendall 2009, Fuong, Maldonado-
Chaparro, and Blumstein 2015, Shelley and Blumstein 2005, Zuberbühler, Jenny, and Bshary
1999). Unfortunately, antipredator behavior in ground squirrels is rarely evaluated to assess how vocalizations affect predator behavior, and studies are largely conducted on social, hibernating species in which juveniles and conspecifics are always present. Teasing apart whether antipredator vocalizations are given regardless of conspecific presence and identifying other potential receivers is therefore extremely difficult. To evaluate antipredator vocalizations in
Sciuridae, development of a systems approach to study antipredator vocalizations in different contexts is necessary. Examining antipredator behavior in a nonsocial context may provide insight into how intraspecific receivers may shape signal structure (Rowe 2013) as well as other possible drivers of complexity (Patricelli and Hebets 2016).
29
Nonhibernating species in desert environments exhibit more variable reproduction and sociality (Waterman 1996), offering an opportunity to examine whether antipredator vocalizations exhibit pluripotency and explore other selective forces imposed by multiple receivers or the environment. Ammospermophilus harrisii occupy the Sonoran Desert, a semidesert in southwest North America (Audubon and Bachman 1854). A. harrisii is a non- hibernating species of small body size (~120g) that lives at low densities (Chew and Chew 1930) in simple family groups composed of mother and offspring of the year (Neal 1965). Juveniles disperse within their first year and relatedness of neighboring individuals is not known. Sociality models (Armitage 1981, Michener 1984) classify squirrels that obtain sexual maturity and disperse within one year as nonsocial if they live solitarily in the breeding season. Few studies have characterized the social relationships and antipredator vocalizations of Ammospermophilus
(but see Bolles 1988 and Neal 1965) and the genus was not considered in previous studies modeling complexity, offering an opportunity to test hypotheses in sociality and communication.
If A. harrisii are nonsocial, individuals should remain solitary throughout the year, maintain non- overlapping home ranges, and individuals should exhibit neutral or avoidant behavior toward neighbors.
A. harrisii are active year-round but occur at low densities during the winter season after offspring dispersal (Chew and Chew 1930), allowing researchers to gain insight into the structure and function of antipredator vocalizations in this species. Nonsocial squirrels are predicted by models of communicative complexity to exhibit low variability in antipredator vocalization systems (Pollard and Blumstein 2012). Under the assumption that adults are largely solitary during the nonbreeding season, individuals should call only during the breeding season and caller ratio should be female biased if the primary function of antipredator vocalizations is a
30 warning to offspring. We restrict our hypotheses to offspring and do not include relatives as potential beneficiaries because dispersal patterns and relatedness between neighbors is unknown.
Further, direct fitness likely acts as a stronger driver than indirect fitness (Blumstein et al. 1997), particularly in solitary species. If antipredator vocalizations function to communicate with predators, animals should continue to give antipredator vocalizations throughout the year and caller ratio should be equal to the sex ratio of males and females in the population. Antipredator vocalizations may therefore be shaped by multiple receivers, shedding light on how complexity may arise.
Methods
Study Area
We conducted a two-year study from January 2017 to January 2019 in the Santa Rita
Experimental Range (SRER), a 21,000-ha area in Pima County, Arizona about 32 km south of
Tucson. Located at the western edge of the Sonoran Desert, the SRER boundary lies at ~900m elevation and receives ~300mm of rainfall yearly in a bimodal pattern, driving seasonal vegetation blooms and spikes in wildlife activity (McClaran 2003). This ecotone is largely dominated by cacti and woody shrubs, including prickly pear (Opuntia spp.), mesquite (Prosopis spp.), and desert hackberry (Celtis spp.).
Data Collection
We used Tomahawk live traps (model No. 201) baited with peanut butter to capture individuals, following the American Society of Mammalogists guidelines for humane trapping
(Sikes et al. 2016). We placed traps at localities where we identified squirrel presence. We used a cloth handling cone (Koprowski 2002) when handling squirrels to ensure efficient handling and minimal stress to the squirrels. We recorded weight, sex, life stage, and reproductive condition of
31 captured animals. We fit a VHF radio collar (Wildlife Materials; 3-4g, <5% body weight) to each captured adult and monitored 20 adult A. harrisii of both sexes. We used the homing technique to locate radio collared individuals at least twice weekly throughout the year, and up to eight times weekly during the summer field season until the radio collar died or the individual disappeared. A. harrisii move frequently and widely between locations, such that allowing one hour to pass between tracking an individual was enough time to allow movement to any location within the home range. Because squirrels were small and well camouflaged, individuals were often not seen before running from their original location, indicated by a large change in radio signal strength. In these circumstances, a point was recorded with a GPS unit where the signal was initially strongest to avoid chasing the squirrel and affecting location. We collected behavior and location data for all marked and unmarked squirrels detected visually or audibly. Detections of antipredator vocalizations and general location were collected opportunistically throughout the day. All antipredator vocalizations detected were documented with notes on the general location, number of calls included in the bout, and whether any variation in amplitude, trill duration, or call rate was detected by ear. If possible, we attempted to localize the caller by slowly approaching to within 15m of the caller while recording with a ME66 Sennheiser omnidirectional microphone and a Marantz PMD661 MKIII Recorder. We also used this microphone-recorder system to record any calls given from individuals while confined in a trap or during handling.
Statistical Analysis
We used R version 3.5.0 (R Development Core Team) software to complete analyses.
We installed the “move” package (Kranstauber, Smolla, and Scharf 2018) to determine minimum locations per individual needed to compute a home range. A bootstrap analysis shows home
32 range size plateaus at 20 points, which informed our threshold for minimum number of locations required per individual to estimate a reliable home range. We used the “adehabitathr” package
(Calenge 2006) to calculate 95% and 50% kernel densities for all individuals with enough points
We calculated the smoothing factor calculated with least square cross validation, LSCV, in all cases except to calculate nonbreeding seasonal home ranges, in which an ad hoc method was used because cross-validation criterion could not be minimized. To avoid including points in which squirrel location was influenced by observer presence, all points in which the squirrel moved just before homing, or in which a point had been taken within the prior hour, were eliminated from home range analyses. We used locations and home range boundaries to analyze home range size and overlap.
To estimate proximity to another known individual and therefore get a sense of interindividual overlap both temporally and spatially, we used Ranges software (v 9.1.2) to run an analysis of dynamic interactions. This analysis provides overlap percentages between individual home ranges as well as a Jacob’s index: ( DO - DE / DE + DO) comparing observed distances between 2 individuals of interest (DO) with the mean distance to all possible locations of individual 2 (DE) (Jacobs 1974, Kenward et al. 1993b). The resulting value ranges from -1 to
1, in which a positive value indicates that the animals are found within close proximity relative to home range boundaries and a negative value indicates avoidance between individuals.
We used Welch’s nonparametric t-test for unequal sample sizes to test null hypotheses regarding our predictions of home range size, home range overlap and calling rate between seasons. To compare home range sizes and calling rate among seasons, we divided the year into three seasons: mating (Jan-Apr), juvenile (May-Aug), and nonbreeding (Sep-Dec). We used the earliest and latest dates of juvenile (<90g) detections to inform seasonal boundaries. Seasonal
33 divisions allowed us to examine the effect of juvenile presence on antipredator vocalizations and/or whether propensity to call could be associated with reproductive activity. The three seasons represent times when squirrels are reproductively active (as evidenced by visual assessment of reproductive condition) but no juveniles are aboveground, females are reproductively active and juveniles are above ground, and no squirrels are reproductively active and juveniles have dispersed, respectively. Juveniles were considered dispersed from the natal burrow the week following the last day seen at the burrow or with an adult female. Juveniles and subadults are distinguished from adults by relative size and pelage color, which dulls with age. In some cases, new unmarked individuals appeared in nearby areas and/or within the home range of the reproductive females after juveniles had dispersed from the natal burrow, and so these juveniles were thought to have dispersed to an adjacent or overlapping home range.
Results
Social & Spatial Organization
Adult squirrels interacted or were within close proximity of neighboring adults throughout the year, albeit at low frequency. Another adult squirrel was detected within 20m in
5.5% of observed squirrel locations (n=1654 total observations). Juveniles emerged above ground in mid to late May and dispersed away from the natal burrow in late July or August.
During the juvenile season, unknown female adults were seen within 5m of a reproductively active collared females’ burrow on eight different occasions. On one occasion, we observed an adult female in October interacting with two subadults believed to be her offspring from May that year. Two females shared a burrow together during the winter months of 2017. We observed an adult female emerge from another marked adult female’s burrow on two occasions within one week in December 2017, during which the marked female was either in the burrow or interacting
34 with the unknown adult female. We captured and collared an adult female, believed to be the unknown above, outside of the same marked female’s burrow approximately one month later in
January 2018. Within 7 days of collar deployment, her collar was chewed so we were unable to obtain further movement data. A week later, we observed the unknown female with a scrotal male and one other squirrel of unidentified sex. On a separate occasion, an adult female was also captured outside the burrow of a marked adult female in the morning in October 2018. Collars chewed at the base of the antenna or on the radio transmitter, out of the owner’s reach, provides further evidence that adults interact. Throughout the study period, we observed chewing on six collars deployed and collected outside of the juvenile season (after the month of August and before the month of May).
Home ranges did not differ between sex, season, or reproductive stage (all p values
>0.5). Therefore, subgroups were pooled for remaining analyses. Home range average (±SE) of
95% kernel densities averaged 2.76±0.47 ha and 50% kernel densities of home range averaged
0.63±0.15 ha (n=20 individuals) (Fig. 1), however, home range size varied considerably from 0.5 to 7.5 ha. In the field, we observed individuals shift areas of core activity from week to week and did not always use the entire home range every day. Individuals that were tracked for several months with >50 points often showed a secondary plateau at ~40 points, indicative of a gradual shift in home range over time, consistent with field observations.
Home ranges overlapped intra and intersexually in time and space (Fig. 2). Overall overlap between individuals averaged 44.75 ± 19.8% overlap among 95% kernel density areas and 27.47 ± 5.01% among 50% kernel density areas. Overlap did not differ between male- female, male-male, or female-female subgroups (all p>0.06), except for female-female 50% kernel density overlap, which was smaller than overlap between 50% kernel densities for pooled
35 sexes (Welch’s t-test, t=-2.37 df= 27.095, p=0.025). The mean Jacob’s index (Jacobs 1974,
Kenward et al 1993b) was 0.028 ± 0.019, with no significant differences between male-male, male-female, or female-female indices (all p>0.3).
Antipredator Vocalizations System
A. harrisii gave antipredator vocalizations throughout the year, though the average number of antipredator vocalizations detected per field visit varied between season (Fig. 3). We pooled the breeding and nonbreeding season and compared the resulting call rate with that of the juvenile season to test whether offspring presence affected calling behavior. There was no statistical difference between the juvenile season and the remainder of the year (t= -0.169, df=206.85, p=0.865). Average hourly rates of call detections were initially low in the mating season (mean=0.06 ± 0.02 bouts/hour), increasing in April to a mean of 0.17 ± 0.03 bouts/hour throughout the juvenile season, and peaking in the nonbreeding season (mean=0.27 ±0.06 bouts/hour). Calls differed between mating and juvenile season (Welch’s t-test: t=2.92, df=148.89, p=0.004) as well as the mating and nonbreeding season (Welch’s t-test: t= -3.45, df=76.04, p<0.001), but not between the juvenile and the nonbreeding season (Welch’s t-test: t=
-1.66, df=87.14, p= 0.099).
Detections of spontaneous antipredator vocalizations in which the sex of the caller was positively identified (n=18) were female-biased (88.8% of callers). Although squirrels of both sexes emitted calls from within traps (14.1% of 73 trapped squirrels), callers were female-biased
(73% female). In comparison, the sex ratio of the population based on trapping data was roughly
1:1 female to males, or the proportion of squirrels caught that were female was 0.49 (n=73 total squirrels caught). Juveniles and subadults also produced antipredator vocalizations
36 spontaneously (n=3) and when confined (n=4). All juvenile and subadult callers with positively identified sex were female (n=5).
Harris’ antelope squirrels emitted antipredator vocalizations both singly (n=43 detections) and in bouts (n=111 detections). Antipredator vocalizations (Fig. 4) that included more than one trill call from a consistent distance and direction were defined as an alarm bout.
The average (±SE) number of calls for a bout was 5.7±0.52 vocalizations. Average vocalizations per bout differed between the strategy used to collect vocalizations. When we only listened and tallied the calls (n=67 call bouts), the average (±SE) was 4.3±0.39 vocalizations per bout. When we attempted to localize the caller (n=42 call bouts), however, the average was 8.3±1.12 vocalizations per bout (Welch’s t-test: t=3.41, df=50.08, p=0.001). Calls within bouts varied considerably in amplitude, duration, and call rate. We detected variation in at least one of these elements in 54.4% of call bouts. Alarm call bouts were followed by one or more bouts given by other individuals in 33% of call detections, resulting in up to four individuals calling at the same time. Finally, we documented two additional call types that were previously undescribed. We have observed juveniles and an adult female give a repeated chirp-like call toward threats close to the burrow (<20m) on five occasions (Fig. 5). We documented an additional instance in which an adult female emitted a trill, followed by several chirps, and repeating this sequence four times.
She emitted this call combination in October after her juveniles dispersed.
Discussion
Social & Spatial Organization
Adult social and spatial organization resembles that of other nonhibernating ground squirrels living in scrub or grassland environments (i.e. White-tailed antelope squirrel (A. leucurus, Karasov 1983), African unstriped ground squirrels (Xerus rutilus; O’Shea 1976)), in
37 that adults live in large, overlapping home ranges composed of several isolated burrows and adults may share burrows and interact occasionally. Warm temperatures throughout the year permit extended breeding seasons, such that there are only a few months throughout the year in which neither males or females are reproductively active, however, females produce only one litter a year. These conditions allow for continued parental care or late dispersal among subadults. Breeding and rearing of young were consistent with patterns described by Neal
(1965), who sampled A. harrisii throughout southeastern Arizona. Juveniles emerged above ground in May and dispersed between August and October. Similarly, Nelson’s antelope squirrels (Ammospermophilus nelson) in the San Joaquin Desert emerge aboveground in April, but may not disperse until as late as November (Hawbecker 1958). Whorley and Kenagy (2007) found that breeding and lactation periods were longer in southern populations of white-tailed antelope squirrels (A. leucurus) than northern populations.
We observed evidence of burrow sharing in several marked adults during winter months. Although winter burrow sharing was previously unknown for this species, it has been observed in their sister species, A. leucurus (Karasov 1983), and may be a common behavior for
‘asocial’ species. Tree squirrels, which are nonhibernating and solitary during the breeding season, also exhibit communal nesting during winter months (Edelman and Koprowski, 2007,
Halloran and Bekoff, 1994; Koprowski, 1996; Ramos-Lara and Koprowski 2012, Williams et al.
2013). Burrow sharing could function as a means of thermoregulation during cooler winter months (Karasov 1983, Williams et al 2013) and implies that squirrels may benefit from maintaining social relationships. We also observed two adult females within 5m of a single active burrow on several occasions throughout the study period. Burrow sharing and adult persistence at a reproductively active female’s burrow could also be evidence of extended
38 parental care (Williams et al. 2013). Adults with more individuals at a burrow may also benefit from greater collective vigilance (van der Marel, Lopez-Darias, and Waterman 2019) or decreased foraging trade-offs (Ortiz et al. 2019). A genetic study analyzing the relatedness between neighboring individuals is needed to determine dispersal patterns, informing social organization and whether kin selection is likely to have a strong influence.
Compared to home ranges of other North American ground squirrels, which typically fall below 1 hectare (Evans and Holdenreid 1943, Evans 1951, Smith and Johnson 1985, Drabek
1973), A. harrisii home ranges are quite large. Other antelope squirrels in neighboring deserts also maintain expansive home ranges of similar size, however, ranging from 3 to 6 hectares
(Hawbecker 1958; Bradley 1967). African ground squirrels living in arid environments exhibit large home ranges (O’Shea 1976) and home ranges in arid environments may be larger than that of northern ground squirrels due to lower resource density (Bradley 1967, Fridell and Litvaitis
1991, Fisher and Fisher 2000, Doherty et al. 2019). Home ranges overlapped intra and intersexually in A. harrisii and did not differ between sexes, characteristic of polygamous mating systems (Clutton Brock 1989) in arid environments (Fisher and Fisher 2000).
Antipredator Vocalization System
We found that although both sexes gave antipredator vocalizations, alarm callers were disproportionately female when calls were given freely as well as when confined. Calls were heard year-round, but peaked during the nonbreeding season, after juvenile dispersal.
Antipredator vocalizations also persisted at approach, suggesting that antipredator vocalizations are intended for the predatory threat (Hasson 1991). However, because our initial assumption of winter solitary behavior may not hold, it is possible that antipredator vocalizations do function as a warning to conspecifics and continue to provide social benefit in the winter time, in which case
39 alarm calling behavior would not cease entirely during nonbreeding months. Antipredator vocalization rate peaks during nonbreeding seasons and presence of calling across age and sex indicate that endocrine cycles are not a likely mechanism driving calling behavior.
Communication systems that include multiple vocalizations and/or vocalizations with multiple functions and graded variation represent higher complexity (Freeberg et al. 2012,
Fischer et al. 2017). Our findings suggest that antipredator vocalizations function as both a predator deterrent and a warning to offspring, indicating that selective forces other than sociality shape antipredator vocalizations. A. harrisii communication system exhibited high variation within and among call bouts. Variation may represent a graded response to the predator’s approach or transmit information to the receiver. Graded variation in trill length or amplitude may be perceived as different signals by the receiver (Fischer et al. 2017, Peckre et al. 2019,
Marler 1974) or prevent the intended receiver from habituating to antipredator vocalizations
(Loughry and McDonough 1988, Owings 2010. The number of trills included in a call bout also varied considerably, and call repetition may be used to incite increased vigilance in conspecifics
(i.e. tonic calling) (Loughry and McDonough 1988, Owings and Hennessey 1984, Owings 2010).
Alternatively, variation may represent levels of information that are used to inform conspecifics of threat details (Ackers and Slobodchikoff 1999, Blumstein and Armitage 1997a, van der Marel,
López-Darias, and Waterman 2019). The different call types and call combinations we observed provide further evidence of greater complexity (Freeberg et al. 2012, Hebets et al. 2016, Peckre et al. 2019) and could be designed to alert different species of predators (Guilford and Dawkins
1991) or communicate threat urgency to conspecifics (Blumstein and Armitage 1997a). Finally, we observed multiple individual callers, which could further communicate risk (Weary and
Kramer 1995) or location of the predator (Thompson and Hare 2010).
40
We observed non-aggressive adult interactions, possible burrow sharing, and home range overlap throughout the year, such that kin selection may play a larger role in shaping this species’ sociality and communication than previously thought. Thus, species living in low densities with the ability to communicate long distances could exhibit a higher degree of social selective pressures than has been appreciated traditionally. Research in tree squirrels and ground squirrels has revealed a number of alternative social tactics to offset energetic constraints. A number of tree squirrel species gain thermoregulatory benefits from engaging in winter social behavior and territorial North American red squirrels (Tamiasciurus hudsonicus) benefit from having familiar neighbors (Siracusa et al. 2019), even when unrelated (Siracusa et al. 2017).
Thus, communication with conspecifics may be selected for in species that are primarily regarded as solitary and may result in the higher variation observed than expected given low levels of sociality. Further study is needed to determine whether conspecifics alter behavior in response to antipredator vocalizations and if so, whether call variation is meaningful to conspecifics.
Conclusions
Species considered to be nonsocial by classic definitions may exhibit more complex sociality and communication than models currently predict. Traditional assumptions about seasonal energetic constraints based on Nearctic fauna are not met throughout much of the planet’s geographic area, which can lead to vastly different mammalian social systems (Jarman
1974, Rayor and Armitage 1991, Waterman 1995). Therefore, a broader spectrum of species ecology that includes those in tropical or arid locations, should be included in future comparative analyses. Though A. harrisii is typically seen solitarily and at low densities, as predicted in an arid biome, individuals maintain large, overlapping home ranges, are seen interacting non-
41 aggressively with neighboring squirrels on occasion, and may benefit from long-distance vocalizations. Other non-hibernating squirrels also benefit from neighboring relationships (Eason
2010, Karasov 1983, Waterman 1995), including territorial, ‘asocial’ species (Siracusa et al.
2017, 2019, Williams et al. 2013), suggesting that traditional social systems are not required for social relationships to evolve.
We also found that A. harrisii may direct antipredator vocalizations toward predators, and alarm calling may serve a dual function of deterring predators and warning nearby relatives.
Alarm signals alter predator behavior across taxa (Clark 2005, Isbell and Bidner 2016, Woodland
1980), however other prey animals, both conspecific (Ackers and Slobodchikoff 1999, Blumstein and Daniels 2004, Leger and Owings 1978) and heterospecific (Aschemeier and Maher 2011,
Igic et al. 2019, Magrath et al. 2009, Magrath et al. 2015, Zuberbühler 2000), monitor such signals. Antipredator signals therefore likely serve multiple functions, introducing a number of potential drivers constraining or selecting for variation. If alarm signals do serve both functions, a more expansive view of alarm communication systems that accounts for nonlinear communication involving three or more parties (Bradbury and Vehrencamp 2014) should be evaluated when considering alarm behavior and call structure. By implementing a systems approach, future studies of antipredator vocalizations may find that communicative complexity is not restricted to more social species as initially concluded. Supporting this view, we found evidence of a graded repertoire and multiple call types with combination. Prey species exposed to a variety of predator strategies may result in variation that provides a framework for information transfer to conspecifics to flourish, thereby increasing the benefits of sociality and imposing selection for social and communicative complexity to evolve.
42
Acknowledgements
We would like to thank our reviewers, B. Mannan and B. Pasch, for their comments that
improved the manuscript. We thank our field assistants for their countless hours of tracking and
observing. Finally, we thank T&E Inc., and the American Society of Mammalogists for
providing funding for equipment and field assistance.
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Figure 1: Average home range size (ha) of Ammospermophilus harrisii in southeastern Arizona throughout 2017 and 2018. Data are divided by the mating season (Jan-Apr), juvenile season
(May-Aug), and nonbreeding season (Sep-Dec). There are no statistical differences of home ranges sizes among season or sex.
55
a) b)
d) c)
Figure 2: 95% and 50% kernel densities of individual antelope squirrels (Ammospermophilus harrisii) in southeastern Arizona. Home ranges of a) all individuals found within study site 2 and
3 of the Santa Rita Experimental Range in which we collected enough points for a home range.
Males are represented by warmer colors (red, orange, yellow) and females are represented by cooler colors (green, blue, purple). Individuals overlapped intra- and intersexually: b) female
(green)-male (red) overlap during the months of June-August 2018, b) female-female overlap during the months of June-August 2017, and c) male-male overlap during the months of October and November 2017.
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Figure 3: Average number of antipredator vocalizations given by Harris’ antelope ground squirrels (Ammospermophilus harrisii) detected per hour in each month of 2017 and 2018
(pooled) in southeastern Arizona. Dashed lines represent seasonal boundaries. Both years start with a low hourly rate of antipredator vocalizations until April in the mating season (months 1-
4), remain at a moderate level through the juvenile season (months 5-8), and peak in the nonbreeding season after juvenile dispersal (months 9-12).
57
Figure 4: Spectrogram of an adult Harris’ antelope squirrel (Ammospermophilus harrisii) call given in southeastern Arizona, looking at frequency (kHz) over time(s). Color represents amplitude; warmer colors represent higher amplitudes. Calls feature a trill with high-frequency overtones that descends in amplitude over time. Squirrels frequently give calls repeatedly, in bouts.
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Figure 5: Spectrogram of a juvenile Harris’ antelope squirrel (Ammospermophilus harrisii) call in the presence of a Western diamondback rattlesnake (Crotalus atrox) in southeastern Arizona.
Frequency (kHz) is represented on the y-axis and time (s) is represented on the x-axis. Chirps consist of a short, broadband syllable that is repeated.
59
Appendix B: Effects of shrub encroachment on antipredator behavior
Burnett, Alexandra D.*, Koprowski, John L.*
*School of Natural Resources and the Environment, University of Arizona, Tucson, AZ, USA
Habitat degradation and loss is a significant driver of extinction, limiting species resilience to rapid change and resulting in widespread declines. Monitoring whether behaviors arise or survival strategies falter can be the first indicator of a potential threat. Management agencies often struggle against time and lack of resources when saving a species already in critical decline, and so recognizing and mitigating threats in a timely fashion is paramount. Further, understanding how animals respond to environmental stimuli is useful for predicting responses to future disturbance. The Harris’ antelope ground squirrel (Ammospermophilus harrisii) is representative of many species adapted to open, arid environments in that they rely on vigilance and alarm signals to evade predators. However, many of these areas are shifting from open desert grassland to mesquite, a phenomenon known as shrub encroachment. We conducted a two-year study of A. harrisii in the Santa Rita Mountains, monitoring individuals in areas of high- and low-density velvet mesquite (Prosopis velutina) cover to assess reliance on mesquite as a resource and quantify differences in antipredatory behavior. We found evidence that the presence of mesquites may alter or reduce anti-predatory behaviors that could affect adult and juvenile survival. A. harrisii were also found to select against woody vegetation and areas of thick vegetation. Thus, shrub encroachment may have adverse effects on antelope squirrel populations and limit future distribution.
60
Introduction
Habitat degradation and loss are significant drivers of extinction (Heinrichs, Bender, and Schumaker 2016), limiting species resilience to rapid change and resulting in widespread declines (Thomas 2004; Mantyka-Pringle, Martin, and Rhodes 2011). Widespread landscape change over short periods of time leaves wildlife isolated from dwindling refuges and unable to adapt before population numbers are decimated beyond recovery (Thomas 2004). Environments with high temperatures that are prone to drought, including arid grasslands and savannas, are particularly threatened by habitat degradation, fragmentation, and climate change (Mantyka-
Pringle et al. 2011). Shrub encroachment, generally defined as the increase of woody vegetation in areas previously dominated by herbaceous vegetation, is a global phenomenon threatening grassland communities (Archer 1995). The main drivers of shrub encroachment vary by region, climate, and community composition (Archer 1995; Barger et al. 2011; Stevens et al. 2016,
Archer et al. 2017). General trends show that anthropogenic activities such as overgrazing and fire suppression alter plant-soil interactions that are further complicated by increasing concentrations of atmospheric carbon dioxide and changing hydrological regimes, triggering ecosystem shifts (Archer et al. 1995; Van Auken 2009). Shrub encroachment significantly alters hydrological trends (Pierini et al. 2014), soil composition (Barger et al. 2011), and population distributions, leading to declines in local biodiversity (Bakker 2003; Dutra et al. 2011,
Ratajczack 2012; Smit and Prins 2015). One such mechanism of wildlife decline may be the breakdown of predator-prey dynamics due to shrub encroachment. Animals reliant on open environments for anti-predatory strategies and communication may alter or increase vigilance behavior in response to lateral obstruction (Arenz and Leger 1997; Wheeler and Hik 2014), thereby increasing the costs of foraging (Metcalfe 1984; Edwards and Waterman 2011;
61
Jayadevan, Mukherjee, and Vanak 2018; Ortiz et al. 2019). Many taxa in open, arid environments evolve alarm signals that deter predator pursuit (Primates: Isbell and Binder 2016;
Artiodactyla: Caro et al. 2004; Lagomorpha: Kamlar and Ballard 2006; Rodentia: Clark 2005;
Barbour and Clark 2012; Gruiformes: Woodland et al. 1980; Passeriformes: Jones and
Whittingham 2008), indicating that these signals may function as a means for prey to communicate that the predator is detected. Once the prey is alert, further pursuit is likely a waste of the predator’s energy and the individual gives up the chase. However, this defense is contingent on the ability of the prey to identify and track the predator through the environment before revealing its location (Shelley & Blumstein 2005) as well as the ability of the predator to detect the prey’s signal (Guilford and Dawkins 1991; Rowe 2013; Patricelli and Hebets 2016).
Without adequate visibility, the conditions required for effective communication between the predator and prey are degraded and anti-predatory defenses may be ineffective, resulting in wasted energy and injury potential for both parties.
Species inhabiting North American deserts and grasslands evolved in an open environment in which wildlife employ predator-deterrent strategies that capitalize on high visibility and allow animals to forage efficiently in these risky environments (Berger et al. 1983;
Kamler and Ballard 2006). Geographical barriers such as mountain ranges or expanses of desert also result in hundreds of endemic species in southeastern Arizona that, after epochs of isolation have evolved unique genetic diversity and adaptations to extreme environments (Koprowski et al. 2013). Despite their impressive resilience to arid conditions, southwestern species face many new challenges that threaten their populations, including urban expansion, grazing pressure, and shrub encroachment. While the southwestern United States has been a focus of research on shrub encroachment for decades, behavioral studies examining Sonoran wildlife response to such
62 landscape changes are lacking. If shrub encroachment does affect anti-predatory behavior, there could be negative consequences for offspring recruitment that result in local extirpation. Further, understanding whether open-adapted species select for or against woody vegetation may provide insight into how population distributions may shift with future shrub encroachment.
The Harris’ Antelope Ground Squirrel (Ammospermophilus harrisii) is a small-bodied
(~120g), diurnal animal that exhibits anti-predatory communication suited to open, desert scrubland (Bolles 1988; Best 1990). While A. harrisii are considered common, their range is limited to upland Sonoran Desert scrub and like many endemic Sonoran species, the land they occupy has faced significant disturbance in the past century due to grazing pressure, urban expansion, and shrub encroachment. Much of their core distribution in Southeastern Arizona is scattered across mid-elevation desertscrub and semidesert grasslands currently threatened by encroachment of native velvet mesquites (Prosopis velutina) (Bahre and Shelton 1993). Ground squirrels are particularly sensitive to lateral occlusion, and must compensate for poor visibility by increasing vigilance and scanning events (Arenz and Leger 1997; Wheeler and Hik 2014).
Thus, A. harrisii behavior and space use may differ between areas of high and low woody cover.
To better understand A. harrisii behavioral response to shrub encroachment and predict how encroachment might affect future distributions, we gathered spatial and behavioral data to inform three questions: 1) Are shrubs used as a resource by squirrels? 2) How is A. harrisii antipredator behavior affected by shrub density? and 3) Do squirrels select for or against shrub patches during daily activity?
Methods
Study Area
63
The Santa Rita Experimental Range (SRER) is a 21,000-ha area in Pima County,
Arizona, about 32 km south of Tucson. The SRER boundary lies at the base of the Santa Rita
Mountains at ~900 m elevation and gradually inclines to ~2500m elevation. This area receives
~300 mm of rainfall yearly in a bimodal pattern, driving seasonal vegetation blooms and peaks in wildlife activity (Krausman and Morrison 2003, McClaran 2003). Generally, vegetation shifts from open Sonoran desertscrub to woodland as elevation increases, however, the SRER has a well-documented history of shrub encroachment over the past century and velvet mesquite (P. velutina) is the dominant shrub between 1000m and 1200m (McClaran 2003). Knowledge regarding wildlife response to such disturbance is warranted but severely lacking (Krausman and
Morrison 2003). We focused on a specific study area of the Santa Rita experimental range covering ~5km2 area between a 950 and 1150m elevation gradient where squirrels were most abundant. The vegetation between these elevations is largely dominated by desert scrub and cacti, including prickly pear (Opuntia spp.), mesquite (Prosopis spp.), and desert hackberry
(Celtis spp). We further broke down the area into five main study sites (~0.1km2 each) that generally encompassed the home ranges of collared squirrels to compare sites of high and low mesquite cover.
Data Collection
We used Tomahawk live traps (model No. 201) baited with peanut butter to capture individuals, following the American Society of Mammalogists guidelines for humane trapping
(Sikes et al. 2016). Squirrels were trapped opportunistically due to low squirrel density and trapping success. We used a cloth handling cone (Koprowski 2002) to handle squirrels and record weight, sex, life stage, and reproductive condition of captured animals. We fit a VHF radio collar (Wildlife Materials; 3-4g, <5% body weight) to 20 adult A. harrisii of both sexes.
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We located individuals at least twice weekly throughout the year, and up to eight times weekly during the summer field season until the radio collar died or the individual disappeared. A. harrisii move frequently and widely between locations, such that allowing one hour to pass between tracking an individual was enough time to allow movement to any location within the home range. Data were not collected when temperatures rose above 40℃, due to safety concerns, resulting in more locations during morning hours. To avoid influencing results, a point was taken where the signal was initially strongest in circumstances where the squirrel ran from its initial location. We collected behavior and location data for all unmarked squirrels detected visually or audibly. Locations with visual detections used in vegetation analyses may be biased toward open areas, where the observer was more likely to detect the squirrel.
Statistical Analysis
We used R version 3.5.0 (R Development Core Team) software to complete home range analyses. We installed the “move” package (Kranstauber, Smolla, and Scharf 2018) to determine minimum locations per individual needed to compute a home range. We then used the
“adehabitathr” package (Calenge 2006) to calculate 95% and 50% kernel densities for all individuals with enough points, (smoothing factor calculated using least square cross validation,
LSCV). To avoid including points in which squirrel location was influenced by observer presence, all points in which the squirrel moved just before homing, or in which a point had been taken within the prior hour, were eliminated from home range analyses. We used locations and home range boundaries to analyze vegetation associations and selection behaviors.
For resource selection analyses, we quantified squirrel use of burrows, food items, and alarm locations within each vegetation class as well as selection behaviors during general activity. We loaded high resolution (10cm) imagery of the study area provided by NEON (2019)
65 into ArcMap (v.10.6.1) and ran a supervised classification analysis to divide the region into four classes: bare ground, herbaceous cover, cacti, and woody plants. Classification output was used to quantify the proportion of each vegetation class over the entire study area as well as within each of our five study sites. Based on maximum likelihood estimates of supervised classification, the study area is composed of ~17% woody shrubs, 21% cacti, 48% bare ground, and 14% herbaceous cover. We used this output to distinguish between high-density mesquite (greater than 25% woody cover) and low-density mesquite study sites (less than 25% proportion woody cover). We calculated Jacobs index to compare the proportions of observations within each vegetation class to the average proportion throughout the entire study area for burrow, forage, and antipredator vocalization locations (O-E)/(O+E) (Jacobs 1974). For these analyses, observed proportions of vegetation class were informed by direct observations. Burrow locations were informed by radio telemetry data on collared individuals and classified into vegetation class based on direct observations. We included observations of both marked and unmarked individuals in selection analyses of forage and alarm calling locations. To compare behavioral differences between high- and low-density sites, we included observations from study site 3, a low-density mesquite site, and study site 5, a high-density mesquite site of equal area. We used
Welch’s t-test for unequal sample sizes to test for differences between visual and auditory detections and trapping success between the two study sites. To quantify second order habitat selection (Johnson 1980), we compared the proportion of each vegetation class available in the study site (~0.1km2) against the proportion of the marked squirrel’s active locations in each vegetation class using Jacob’s index. For this analysis, we included only GPS locations of marked individuals in which we had a visual confirmation of the squirrel. We estimated
66 significance of observed patterns with Pearson’s chi squared test for analyses of all four selection datasets.
Results
Are shrubs used as a resource by squirrels?
Squirrels dug burrows most frequently beneath mature prickly pear plants (63.9% of observations) but also occasionally used woody shrubs such as mesquite (10.4% of observations)
(n= 22 animals, 192 observations). Squirrels selected for cacti and shrubs and against bare ground and herbaceous cover for burrows compared to expected values that assume neutral selection toward vegetation classes (Chi-squared test: χ2= 316.09 under the null hypothesis, p<<0.0001) (Fig. 1). We observed A. harrisii foraging on a variety of food sources (n= 47 observations total), including flower buds, grass seeds, berries, mesquite beans, and cacti fruits.
Observations of foraging behavior most frequently involved prickly pear fruits and flowers
(69.6% of observations). In contrast, individuals were observed foraging on mesquite beans in
5.3% of observations. Individuals consumed cacti and grasses greater than measured availability and consumed shrubs less than expected given availability (Chi-squared test: χ 2=26.71, p<<0.0001; Fig. 2). When alarm calling, squirrels selected for both cacti and woody vegetation but avoided bare ground and herbaceous cover (Chi-squared test: χ 2=32.33, p<<0.0001, n=18 observations) (Fig 3). Individuals were seen alarm calling in mesquite trees and prickly pear in
38.8% and 33.3% of known locations, respectively. We also observed squirrels alarm calling from cholla (11.1%) and hackberry (11.1%).
How is squirrel behavior affected by shrub density?
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We compared two years of visual and auditory detections between a low-density (<25% woody cover) study site (study site 3: 251.05 total hours of observation) to a high-density (>25% woody cover) study site (study site 5: 116.7 total hours of observation), both measuring approximately 0.1km2. We observed fewer squirrel detections at our high-density study site compared to our low-density study site (Welch’s t-test: t=2.16, df=267.19, p=0.03). We documented squirrels at a rate of 1.19±0.12 (SE) detections/hour in areas of low-density mesquite and 0.8 ±0.09 detections/hour in areas of high density. Call detection rate also varied between study sites of high and low mesquite density (n=68 call detections, t= 3.94, df=273.62, p=0.0001). Squirrels gave 0.24 ±0.04 antipredator vocalizations per hour at open study sites with
<25% woody cover. At the study site with >25% woody cover, squirrels gave only 0.03±0.02 antipredator vocalizations per hour, totaling to only three detections of antipredator vocalizations over the course of the two-year study. Trapping success did not vary between site (Welch’s t- test: t=0.21, df=56.67, p=0.83), averaging (±SE) 0.09±0.005 successful captures per trap hour.
Do squirrels select for or against shrub patches?
We observed active individuals <1 m from cover in 58.6% of total observations (n=22 animals, 257 observations), 41.4% of active observations were recorded ≧1 m from cover.
Squirrels selected for slightly more bare ground and herbaceous cover during daily activity than given availability but selected slightly against woody vegetation and cacti (Chi-squared test: χ
2=9.92, p=0.019) (see Fig. 4).
Discussion
Shrubs as a resource for squirrels
We observed A. harrisii using woody vegetation, including mesquite trees, as a resource for burrows, forage, and antipredator strategies, however, cacti were favored over
68 shrubs for burrow locations and forage items. Cacti and shrubs act as food and water sources, cover from predators, a watch post to scan for threats, and vegetation for burrowing beneath. A. harrisii are adept at climbing woody vegetation and will spend several minutes foraging, vigilant, or alarm calling in tall vegetation. As the tallest vegetation on the landscape, mesquites offer a valuable vantage point traditionally provided by large cacti, which may explain why shrubs were preferred over cacti for alarm calling locations.
Shrub density affects squirrel antipredator behavior
Despite the resources that mesquite trees provide, the antipredatory behavior of A. harrisii was altered in areas with high-density mesquite. We recorded fewer visual and auditory detections of squirrels. Due to low trapping reliability, we cannot confirm whether fewer detections of the squirrel correlates with a lower density or whether squirrels instead employed more cryptic behavioral strategy to avoid detection. Regardless, antipredator vocalizations were detected on only three occasions in high-density mesquite areas but on hundreds of occasions in low-density mesquite sites, a difference that time spent in each area cannot account for. This result suggests that individuals occupying dense vegetation may alter antipredatory strategies and inhibit predator-deterring behavior. These changes could be in part due to lack of visibility or inability to track the predator through thick vegetation (Arenz and Leger 2000; Wheeler and Hik
2014; Ortiz et al. 2019). Squirrels may also fail to detect predators until they are within a proximity that most individuals choose not to call (Hasson 1991). Alternatively, dense areas could represent a different density or composition of predators that affects perceived predation risk or antipredator strategy. Another possible reason that squirrels fail to call is the lack of reproductive females present in the area, however, our trapping records indicate that at least four reproductive females inhabited the high-density site during the study period.
69
Squirrels select against shrub cover
The Santa Rita population of A. harrisii is reliant on cover for burrows and predator avoidance, but also uses areas of bare ground for foraging while maintaining visibility. Squirrels exhibited positive selection for cacti and woody vegetation during alarm calling, however, for day-to-day activity, squirrels selected against woody vegetation but selected for areas of bare ground. Thus, while mesquite trees could serve as an important resource going forward, squirrels may prefer open areas to maintain visibility while foraging, as seen in S. tridecemlineatus (Arenz and Leger 1997) and other herbivores (Valeix et al. 2009). High woody cover presents challenges for maintaining visibility for predator detection and avoidance, and may require a higher state of vigilance while foraging, decreasing foraging efficiency (Metcalfe 1984; Edwards and Waterman 2011; Jayadevan, Mukherjee, and Vanak 2018; Ortiz et al. 2019). A. harrisii therefore may face steep trade-offs as mesquite density increases. Poor quality habitat could act as a sink if squirrels experience reduced survival (Pulliam 1988) or deter recolonization by new residents, which may ultimately exclude A. harrisii from shrub encroached areas and limit their distribution.
Management Implications
Small mammals are known to play an integral role in community composition by affecting plant distribution and cover (Walsberg 2000; Beck & Wall 2010; Hale, Koprowski, and
Hicks 2013; Ewacha 2016), soil characteristics (Davidson, Detling, and Brown 2012; Ewacha
2016), and insect abundances (Ewacha 2016). These effects may be exacerbated in desert environments with low resource density (Walsberg 2000; Ewacha et al. 2016). A. harrisii consume and transport an abundance of fruits and seeds. We frequently observed A. harrisii carrying fruits and seeds several meters and occasionally brought food items into the burrow.
70
This foraging behavior was found to be extremely important for plant distribution in A. harrisii’s sister species, Ammospermophilus leucurus (Beck & Wall 2010). A. harrisii likely benefits the
Sonoran Desert vegetation in a manner similar to that of A. leucurus and other ground squirrels.
If shrub encroachment does result in a lower density of desert rodents such as A. harrisii, it may compound on shrub competition with cacti by limiting seed dispersal.
Our findings provide evidence of potential consequences for the survival and distribution of A. harrisii resulting from shrub encroachment. Other Sonoran wildlife reliant on open environments for antipredator behavior, such as Sonoran pronghorn (Antilocapra americana sonoriensis, Berger et al. 1983), antelope jackrabbit (Lepus alleni, Best and Henry 1993), or black-tailed jackrabbits (Lepus californicus, Kamler and Ballard 2006), could be affected in a similar manner. Shrub encroachment creates a more complicated landscape that can instill a higher depredation of small mammals by aerial predators, or provide more cover for predators to hide (Akunke and O’Connell 2017). Animals that have evolved in open environments increase vigilance behavior in closed areas or increase giving up densities in closed areas (Wheeler and
Hik 2014; Jayadevan et al. 2018) which can result in steep foraging tradeoffs that may alter spatial and temporal use of encroached areas or distribution across the landscape (Valeix et al.
2009). To mitigate the negative consequences outlined above, managers should consider employing controlled burns at regular frequencies to maintain grasslands (Thomas and Goodson
1992; Twidwell et al. 2013). Where shrub encroachment persists, managers may consider thinning and pruning to maintain visibility needed for antipredator strategies. Travel corridors between grasslands should be created and maintained to encourage gene flow between populations and increase resilience to climate change.
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Acknowledgements
We thank our reviewers, B. Mannan and B. Pasch, for their input in improving the manuscript. We also thank the Koprowski Conservation lab for their guidance and support in addition to our numerous field assistants for their contributions. We thank our funding sources
T&E, ASM, and UA for their financial and logistical support. The National Ecological
Observatory Network is a program sponsored by the National Science Foundation and operated under cooperative agreement by Battelle Memorial Institute. This material is based in part upon work supported by the National Science Foundation through the NEON Program.
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Figure 1: Selection indices of burrow locations of Ammospermophilus harrisii in southeastern
Arizona within each vegetation class based on direct observations compared to average availability across study sites. We included all burrow locations that were used by marked individuals at least once (n=22 animals, 192 total burrow locations). Negative values indicate selection against, positive values indicate selection for the vegetation class. Burrows beneath
Opuntia were used most commonly. Prosopis and Celtis were the next most frequent genera for burrowing beneath, though at a significantly lower frequency. Individuals also used burrows beneath Senegalia and Cylindropuntia, as well as Ferocactus, Ephedra, and Heteropogon.
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Figure 2: Selection indices of foraging items within each vegetation class based on direct observations of feeding compared to average availability across study sites (n=47 direct observations of feeding). Negative values indicate selection against, positive values indicate selection for the vegetation class. We observed Ammospermophilus harrisii feeding on flowers and fruits of Opuntia the vast majority of the time in southeastern Arizona. The next most frequently observed food source was grass seeds (Poaceae).
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Figure 3: Selection indices of alarm calling locations within each vegetation class compared to average availability of each vegetation class across study sites. Only observations in which the plant the individual was calling from was positively identified were included in the analyses
(n=18 observations). Negative values indicate selection against, positive values indicate selection for the vegetation class. Ammospermophilus harrisii called from mesquite trees (Prosopis) in
38.8% of known alarm call locations in southeastern Arizona. Prickly pear (Opuntia) were the next most common observed alarm call locations (33.3%), and then cholla (Cylindropuntia,
11.1%) and hackberry (Celtis, 11.1%).
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Figure 4: Selection indices of active individuals within each vegetation class compared to average availability across study sites (n=22 individuals, 257 observations). Negative values indicate selection against, positive values indicate selection for the vegetation class.
Ammospermophilus harrisii in southeastern Arizona selected for bare ground slightly avoided shrub and cacti.