California State University, Northridge Effects Of

CALIFORNIA STATE UNIVERSITY, NORTHRIDGE

EFFECTS OF ECOSYSTEM ENGINEERING BY THE GIANT KANGAROO RAT

ON THE COMMON SIDE-BLOTCHED LIZARD

A Thesis submitted in partial fulfillment of the requirements

For the degree of Master of Science in Biology

Camdilla D. Wirth

August, 2014

The thesis of Camdilla D. Wirth is approved:

Dr. Paula M. Schiffman Date

Dr. Robert E. Espinoza Date

Dr. Tim J. Karels, Chair Date

California State University, Northridge

Acknowledgements

I have many people to thank for helping me throughout the process of obtaining my Master’s. First, I would like to thank Dr. Tim Karels for guiding me through the challenging process of choosing a problem and developing methods to tackle it. You’ve been an amazing source of knowledge, and I am grateful for your mentorship. I’d also like to thank my committee members Dr. Paula Schiffman and Dr. Robert Espinoza for providing me with valuable advice and suggestions throughout my career at CSUN, both in regards to my project and in academia and science in general. I have learned so much from all three of you. Thank you.

I also would like to thank Dr. Justin Brashares, Dr. Laura Prugh, and Rachel

Endicott for allowing me to work under their umbrella and providing me with amazing advice, logistical support and resources. I am so grateful to have been a part of the

Carrizo team. Thank you to the Bureau of Land Management for allowing me to conduct my research at the Carrizo Plain National Monument.

A big, heartfelt thanks to everyone who helped me collect or analyze my data. I’d like to thank Dr. Mark Steele for being a “ghost” member of my committee and taking the time to answer my many, many stats questions. I also want to thank my friends and research volunteers: Tom Chen, Rachel Rhymer, Jimmy Rogers, Jason Warner, Amanda

Lindgren, Josh Sausner, Patrick Exe, and Tianqing Huang for braving summertime temperatures in the Central Valley and helping me in the field. I would not have been able to complete this project without your manpower and company during the many long and tedious days at the Carrizo.

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I’d also like to thank my lab mates Alex Johnson and Sean Dunagan. Having you guys alongside me for the three years of grad school was wonderful. You both always helped me see things in a way I hadn’t before. And, of course, you were great company during the long hours at school.

Finally, thank you to my family and friends: my mother Robyn Lynn, my sister

Merewyn Lynn, and my brother Braum Wirth. Thank you for giving me the confidence to achieve my dreams. Thank you for supporting me on one grand adventure after another.

You are my rock. A special thank you to my friends Lauren Valentino, Sara Zabih, and

Heather Hillard. You have been there with me through the worst and best parts of this process, and I am grateful every day for your friendship, support, and love. Kelli Waugh,

Matt Fritsvold, Morgan Rumble, Amy Maus, Whitney Gerlach: Thank you for putting up with your weird science friend and continuing to be there for me, no matter how many miles away I am.

TABLE OF CONTENTS

Signature Page ...... ii

Acknowledgements ...... iii

LIST OF TABLES ...... vi

LIST OF FIGURES ...... vii

ABSTRACT ...... viii

Introduction ...... 1

Methods...... 16

Results ...... 26

Discussion ...... 35

Literature Cited ...... 45

LIST OF TABLES

Table 1: Ecosystem Engineering Mechanisms and Description ...... 11

Table 2: Hypotheses and Predictions ...... 15

Table 3: Flight Initiation Distance ANCOVA Model...... 25

Table 4: Arthropod Assemblage ANOVA Model ...... 25

Table 5: Temperature and Humidity Values for Paired Microhabitat ...... 30

Table 6: Temperature Values for 3 Microhabitats ...... 30

LIST OF FIGURES

Figure 1: Precinct Manipulation Experimental Design ...... 21

Figure 2: Paint Marking on Uta stansburiana ...... 22

Figure 3: Scatterplot of Lizard Density Against Precinct Density ...... 26

Figure 4: Scatterplot of Lizard Density Against Burrow Tunnel Density ...... 27

Figure 5: Bar Graph of Distance to Nearest Refuge by Microhabitat ...... 28

Figure 6: Bar Graph of Flight Initiation Distance by Microhabitat ...... 28

Figure 7: Bar Graph of Temperature at Three Microhabitats ...... 31

Figure 8: Interaction Plot for Arthropod Abundance by Block and Treatment ...... 32

Figure 9: Temporal Persistence Curves for Translocated Lizards ...... 34

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ABSTRACT

EFFECTS OF ECOSYSTEM ENGINEERING BY THE GIANT KANGAROO RAT

ON THE COMMON SIDE-BLOTCHED LIZARD

Camdilla D. Wirth

Master of Science in Biology

Ecosystem engineers are organisms that control the availability of resources to other species by creating and modifying habitat (Jones et al. 1994). Ecosystem engineers alter habitat in such a way as to reduce physical and biological stresses for other organisms (Crain & Bertness 2006). Burrowing mammals are keystone ecosystem engineers in many communities because burrowing is an engineering activity that can directly and indirectly alter the availability of resources, have effects at multiple spatial and temporal scales, and have a significant role in community organization (Prugh &

Brashares 2012).

Giant kangaroo rats (Dipodomys ingens), are a federally listed endangered species and keystone ecosystem engineers that modify habitat by building extensive burrowing systems. They are associated with greater density and diversity of vertebrate, invertebrate, and plant populations. However, few studies have addressed the functional mechanisms behind these associations and how ecosystem engineering affects the behavior of associated species. The purpose of this study was to investigate the functional attributes of ecosystem engineering by giant kangaroo rats and quantify their effects on

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the common side-blotched lizard. Lizard abundance is positively correlated with giant kangaroo rat density in this system, and although an increased presence of arthropods has been suggested as the mechanism, the causative factor has not been determined (Prugh &

Brashares 2012). I investigated both landscape and local scale effects of habitat modification by giant kangaroo rats on the density, microhabitat use, and behavior of the common side-blotched lizard in 2012 and 2013. I determined that lizards are associated with greater burrow tunnel density at the landscape scale and are found more often on precincts on a local scale. A translocation experiment revealed that lizards prefer precincts with more burrow tunnels and remain at those precincts longer. I investigated whether giant kangaroo rats facilitate lizard density by three possible mechanisms: by providing refuge from predators, by providing thermal refuge, or by providing increased arthropod prey resources. Additionally, I investigated whether lizards altered their behavioral response to predation risk in the presence of burrow tunnels. I found that lizards use burrow tunnels as refuge from predators and display differences in escape behavior on and off precincts. Precincts also provide thermal refuge where temperature and humidity is more stable than the outside environment. However, at the local scale, there were no differences in arthropod resources. Giant kangaroo rats likely facilitate common side-blotched lizards by a combination of supplying refuge from predators and from extreme temperature and humidity.

Introduction

Facilitation is an interaction in which the presence of one species modifies the environment in such a way that the growth, survival or reproduction of a neighboring species is positively affected (Bertness & Callaway 1994; Stachowicz 2001; Bronstein

2009). Facilitation is a pervasive interaction in natural communities in both aquatic and terrestrial habitats. The mechanisms that lead to facilitation are both numerous and diverse, and the strength and sign of the interaction can vary along environmental gradients (Crain & Bertness 2006; Bronstein 2009; Maestre et al. 2009). Facilitation often occurs more frequently and with stronger effects in environments that are particularly stressful for the organisms that inhabit them (Bertness & Callaway 1994;

Stachowicz 2001; Hart & Marshall 2013). Sources of stress include physical factors, such as temperature, moisture, and salinity; interactions with other organisms, such as predation or competition among conspecifics or between heterospecifics; and poor resources, such as nitrogen deprived soil (Callaway 1995; Stachowicz 2001; Bruno et al.

2003).

Ecosystem engineers are organisms that control the availability of resources to other species by creating and modifying habitat (Jones et al. 1994). Though “habitat building” organisms (e.g., beavers, corals) have long been recognized by ecologists, until the concept of the ecosystem engineer was formally introduced in 1994 by Jones and colleagues, ecosystem engineering had remained undescribed as an interaction, with little credence given to its role in the organization of communities (Wright & Jones 2006).

Since then, the literature surrounding the ecosystem engineering concept has progressed

into a sizable area of scientific discourse and discovery. As defined by Jones et al.

(1994), most, if not all, organisms engage in ecosystem engineering to some degree

(Wright & Jones 2006). However, as with the concepts of competition and predation, the generality of the ecosystem engineering concept does not belie its usefulness in developing models, theory, and hypotheses about the process and its influence on communities (2006). Because engineering is a ubiquitous process, the concept of engineering is most effective when applied to interactions in which the biologically mediated changes to the environment are distinctive from, and large relative to, abiotic processes (Reichman & Seabloom 2002). The ecosystem engineering concept allows us to decouple engineers’ trophic effects from those of habitat modification, helps us understand bidirectional relationships between organisms and the abiotic environment, and provides us with an attendant range of theories and models that further the study of facilitation (Bruno et al. 2003). The inclusion of ecosystem engineering into ecological theory and empirical study promotes a more holistic understanding of community dynamics, species coexistence, and niche partitioning (Hasting et al. 2007).

Engineers alter their environment and the flow of resources to other organisms by two paths: autogenic engineers by their own tissue (e.g., corals build reefs, trees build forests, Sphagnum spp. create bogs), and allogenic engineers by other materials (e.g., beavers build dams, elephants disturb trees and shrubs). These processes are distinctly separate from assimilatory processes in which organisms consume or are consumed, i.e., trophic interactions (Jones et al. 1994; Wright & Jones 2006). Foundation species (sensu

Dayton 1972) are spatially dominant allogenic engineers that determine whole

community structure and modulate ecosystem processes. Coral reefs, kelp and seagrass beds, temperate grasslands, and many forests (e.g., eastern hemlock, Douglas fir, mangrove spp.) are examples of ecosystems controlled by foundation species (Dayton

1972; Bruno et al. 2003; Ellison et al. 2005; Angelini et al. 2011). Ecosystem engineers alter habitat in such a way as to reduce physical and biological stresses for other organisms by alleviating limiting local abiotic conditions, providing enemy-free space, and increasing the availability of poor resources (Crain & Bertness 2006). For example, engineers alleviate stress caused by low shade and moisture availability (e.g., nurse plants; Tewksbury & Lloyd 2001), high salinity (e.g., salt-tolerant plants in salt marshes;

Shumway & Bertness 1994), low nitrogen availability (e.g., soil turnover by fossorial mammals; Canals et al. 2003), and high predator abundance (e.g., kelp beds provide cover for temperate fishes; Johnson 2006).

Engineering can produce shifts in the spatial distribution of organisms across the landscape through population responses to engineering such as differences in survival, reproduction, and dispersal (Jones et al. 1997). On a local scale, engineering can influence the movement and behavior of individual organisms within a population

(1997). For example, an individual’s preferential use of engineered habitat could reflect that the individual is cuing in on resources that are more abundant in engineered patches.

Shifts in behavior could manifest as changes in intraspecific interactions (e.g., aggression, mating) or in habitat use (e.g., foraging time or refuging from predators). The tendency of ecosystem engineering to produce distinct patches that differ in a qualitative way from unmodified patches increases habitat heterogeneity and biodiversity (Hastings

et al. 2007). Engineering is an integral part of niche construction for many species and can profoundly influence the ecology (distribution) and evolution (diversification) of some species (Erwin 2008).

Engineers can directly or indirectly control resources and their interaction with other organisms is mediated through the abiotic environment (Jones et al. 1997). For example, soil disturbance by pocket gophers directly alters the bulk density and surface microtopography of soil, while it indirectly alters the availability of nutrients to plants, trophic resources to herbivores, and shelter to organisms that live in and on plants at sites of soil turnover (Reichman & Seabloom 2002).

The effects of ecosystem engineering on other organisms can be density- mediated, in which the strength of the effect on the abundance of other species is mediated by the abundance of the engineering species, or trait-mediated, in which the strength of the effect on species abundance is mediated by alteration of traits exhibited by those species (e.g., behavioral, morphological, physiological) in the presence of ecosystem engineers (Preisser et al. 2005; McCoy & Bolker 2008). Though trait- mediated effects have been given significant attention in predator-prey studies, few studies have expressly tested for trait-mediated effects of engineers (Werner & Peacor

2003; Paterson et al. 2013). One class of traits noticeably lacking in the ecosystem engineering literature is behavior. Few studies have empirically tested for behavioral changes in response to the presence of ecosystem engineering. Cáceres-Charneco &

Ransom (2010) found that the refuging behavior of red-backed salamanders (Plethodon cinereus) was dependent on whether earthworms (Lumbricus terrestris) were present or

absent. When earthworms were absent, salamanders used cover objects as refuge, but in the presence of earthworms, they preferentially used earthworm burrows instead of cover objects. Fraser et al. (2014) found that the orientation of limpets (Cellana tramoserica) was influenced by the presence of autogenic engineering barnacles, which provide shelter from wave action. Recently, efforts have been made to classify the indirect effects of ecosystem engineers as density-mediated or trait-mediated. Density-mediated indirect interactions are those that indirectly produce changes in the abundance of one species by a second directly altering the abundance of a third species, whereas trait-mediated indirect interactions affect the abundance of one species through a second species inducing changes in the behavioral or physiological traits of a third species (Abrams et al.

1982, Křivan & Schmitz 2004). For example, one autogenic engineer, spotted knapweed

(Centaurea maculosa), affects the abundance of a predatory spider by adding structural complexity to the environment. Higher spider abundance results in higher prey consumption, an example of a density-mediated indirect interaction between the engineer and the prey. In addition, the presence of spotted knapweed alters the spider’s web- making behavior, which increases prey capture rates, thereby resulting in a trait-mediated indirect interaction between the engineer and the prey (Pearson 2010). However, organismal interactions involving ecosystem engineering are distinct from other relationships because the abiotic environment can be considered the intermediary between the engineer and the organism (Hasting et al. 2007). Therefore, density-mediated and trait-mediated indirect interactions may occur without the interposition of a third species.

Though ecosystem engineering is most often perceived to have net positive effects on communities, engineers can also have negative effects (Jones et al. 1997). For example, when beavers create dams, some aquatic species become locally rare after losing access to appropriate stream habitat, though the net effect on community species richness is positive (Wright et al. 2002). Engineering organisms occur across trophic and taxonomic levels but their effects are limited to neither. In addition, many engineering species have effects on their communities that are disproportionately large relative to their abundance in the environment, thus acting as keystone species (Hastings et al.

2007). Though some engineering is ephemeral, in many cases engineered structures have effects at spatial scales far larger than other effects (such as trophic) of the engineer and can last longer than the lifetime of individual engineers, with decay rates of the engineered structures unique to each type of engineering and engineer (Hasting et al.

2007).

Burrowing mammals as ecosystem engineers

Burrowing mammals are keystone ecosystem engineers in many communities because burrowing is an engineering activity that can directly and indirectly alter the availability of resources, have effects at multiple spatial and temporal scales, and have a significant role in community organization (Dickman 1999; Reichman & Seabloom 2002;

Zhang et al. 2003; Brock & Kelt 2004; Prugh & Brashares 2012). Burrowing mammals disturb soil by excavating burrow tunnels and constructing burrow mounds, digging out foraging pits and resting sites, and by repeatedly using established trails (Whitford & Kay

1999). The size and longevity of the disturbance varies between species. For example,

individual mounds created by burrowing mammals can range from less than two cm

(cansu mole rat) to 10 m in diameter (prairie dogs) (Whitford & Kay 1999). Some disturbances are short-lived (e.g., temporary foraging pits) while others can last on the timescale of decades (e.g., burrow systems occupied by successive generations) or even centuries (e.g., mima mounds) (Meadows 1991; Whitford & Kay 1999; Milcu et al.

2006). Burrowing activity is a physical process that mixes and aerates soils. This process creates microsites of soil turnover, bringing subsoil elements to the surface and reducing the bulk density of soil (Gabet et al. 2003). This is turn increases the rate of water infiltration into the soil as well as the concentrations of soil nutrients such as carbon, nitrogen, and phosphorus, at the soil surface (Gabet et al. 2003; Eldridge et al. 2012).

Because burrowing changes the soil nutrient profile, areas of disturbed soil can create favorable microhabitat for seedling recruitment and establishment (Dhillion 1999;

Whitford & Kay 1999; Milcu et al. 2006). Disturbed areas often differ markedly in plant biomass and cover, community composition, and productivity from undisturbed areas

(Schiffman 1994; Whicker & Detling 1988; Dhillion 1999; Weshe et al. 2007; Villarreal et al. 2008). The areas on and around burrow systems tend to have a greater presence of symbiotic fungi than the surrounding habitat (Whitford & Kay 1999).

The presence of these burrowing systems is often demarcated by elevated mounds of soil, creating both topographic and microhabitat heterogeneity across the landscape

(Noble et al. 2007; Ceballos 1999; Davidson & Lightfoot 2008). Invertebrate abundance, biomass, community composition, and species richness all can differ between burrow systems and undisturbed areas (Bangert & Slobodchikoff 2006; Davidson & Lightfoot

2007; Davidson et al. 2008). These changes in invertebrate and plant communities at burrow sites can create higher quality foraging sites for vertebrates (Whitford & Kay

1999; Davidson et al. 2012). Burrow tunnels and mounds also serve as refuge and microhabitat for other species (Schiffman 2007a; Davidson et al. 2012). The presence of burrowing mammals is associated with higher species richness, diversity, and population density of vertebrate species, including birds, rodents, large herbivores, lizards and anurans (Krueger 1986; Smith & Foggin 1999; Gálvez Bravo et al. 2000; Bagchi et al.

2006). Burrowing promotes biodiversity by increasing the amount of available niches on both a large, landscape scale, as well as at the level of an individual burrow mound (i.e., local scale) (Wu & Loucks 1995; Tews et al. 2004; Larkin et al. 2006).

Burrowing is a complex engineering activity that has strong facilitative effects on many different species of plant and animals across taxonomic and trophic levels

(Meysman et al. 2006). Many burrowing mammals strongly influence the distribution, abundance and diversity of other members of the communities in which they are found

(Whicker & Detling 1988; Smith & Foggin 1999; Whitford & Kay 1999; Read et al.

2008; Delibes-Mateos et al. 2011). Although burrowing has community-wide consequences across many ecosystems, it is most important in resource-limited environments. Burrowing small mammals are integral to the functioning of desert or semiarid ecosystems because of the ecosystem services they provide (Brown & Heske

1990; Davidson et al. 2012). In deserts, soil disturbance by animals is the single most significant process contributing to soil turnover (Whitford & Kay 1999). Burrowing maintains open habitat, slows desertification, and creates landscape level habitat

heterogeneity in grasslands (Davidson et al. 2012). Burrowing can maintain ecosystem productivity by promoting microsites of nutrient facilitation for plants. Understanding the relationships that keystone burrowing mammals have with other components of the ecosystem is crucial to the management of rapidly disappearing habitats around the globe, especially under changing climate regimes and other anthropogenic influences such as cattle-grazing and biological invasions (Goldingay et al. 1997; Schiffman 2007;

Davidson et al. 2012).

Current study

The Carrizo Plain National Monument is California’s largest remaining grassland and has been recognized as a “hotspot” of species endangerment (Dunn et al. 1997). The stability of this ecosystem relies on the services of the giant kangaroo rat (Dipodomys ingens), a keystone ecosystem engineer and federally listed endangered species. The

Carrizo Plain ecosystem is one of the last remaining habitats for the giant kangaroo rat and many other threatened or endangered native species such as the San Joaquin antelope squirrel and the blunt-nose leopard lizard, and so conservation of this ecosystem depends on the ability to understand and preserve the role this keystone species plays in the community. The giant kangaroo rat influences plant productivity and diversity, invertebrate abundance and biomass, and the abundance of other vertebrate species through their engineering and non-engineering (e.g., trophic and competitive) effects

(Prugh & Brashares 2012). They also serve as an important prey population to the endangered San Joaquin kit fox (Schiffman 1994; Goldingay et al. 1997). Many of the interactions kangaroo rats have are indirect, mediated by their influence on soil properties

and plant productivity (Prugh & Brashares 2012). Common side-blotched lizards (Uta stansburiana) have a landscape scale positive association with kangaroo rats (2012).

However, whether this is due to kangaroo rat engineering activity or some other factor is unknown, as is whether the interaction is density-mediated or trait-mediated.

The purpose of this study is to investigate the functional attributes of ecosystem engineering by giant kangaroo rats and quantify their effects on the common side- blotched lizard. Common side-blotched lizard abundance is positively correlated with giant kangaroo rat density in this system, and although an increased presence of arthropods has been suggested as the mechanism, the causative factor has not been determined (Prugh & Brashares 2012). Giant kangaroo rats are allogenic engineers that create extensive burrow systems called precincts that can range in size from two to three meters in diameter aboveground, with a complex system of burrow tunnels that can extend more than one meter underground (Prugh & Brashares 2012). Giant kangaroo rats may have both indirect density-mediated and trait-mediated effects on common side- blotched lizard density, microhabitat use, and behavior (Table 1). Kangaroo rats may indirectly affect lizard density by providing physical places of refuge from predators in their burrow tunnels. Lizards may also alter their behavioral response to predation risk in the presence of burrow tunnels, a trait-mediated effect. Arthropod abundance is positively correlated with kangaroo rat abundance, and so they may indirectly affect lizard density through trophic facilitation, mediated through arthropod density. The structural modifications kangaroo rats make to the environment is likely to have a distinct effect on ectothermic species, including common side-blotched lizards, because of the importance

of microhabitat to thermoregulation (Adolph 1990). Kangaroo rats may indirectly affect lizard density by creating microclimates (i.e., burrow tunnels and elevated precincts) distinct from the surrounding habitat in which lizards may thermoregulate, again an interaction that is mediated by lizard behavioral traits.

Kangaroo rats may also have effects on lizards at multiple spatial scales. Lizards display microhabitat preferences that reflect their thermal requirements as well as resource acquisition and predator avoidance (Downes 2001; Smith & Ballinger 2001). On the landscape scale, kangaroo rats may influence the spatial distribution of lizards by creating distinct patches of favorable conditions through their engineering activities, while on a local scale, they may influence lizard movement and behavior by supplying refuges from predators, creating higher quality foraging patches by increasing the abundance of arthropod resources, and providing physical structure for thermoregulation.

Table 1. Giant kangaroo rat ecosystem engineering possible mechanisms and categorization as direct or indirect, and density- or trait-mediated.

Direct or Density- or trait- Mechanism Description indirect mediated Refuge from predation Burrow tunnels create Indirect Trait-mediated physical refuge from predators Refuge from predation Alteration of refuging Indirect Trait-mediated behavior Trophic facilitation Higher arthropod Indirect Density-mediated abundance in the presence of kangaroo rats Abiotic stress amelioration Precinct structure, e.g., Indirect Trait-mediated burrow tunnels, create thermal environment microsites

Hypotheses and predictions

1. Giant kangaroo rats facilitate common side-blotched lizards at multiple spatial scales

Burrowing mammals have a landscape scale positive association with herptofaunal density in many systems (Kretzer & Cully 2001; Lomolino & Smith 2006;

Shipley & Reading 2006; Gálvez Bravo et al. 2009). Fewer studies have tested for a local scale association. Hawkins and Nicoletto (1992) demonstrated that two lizard species were more abundant at bannertail kangaroo rat (D. spectabilis) burrow mounds than in the grassland matrix between burrow mounds. Davidson and colleagues (2008) also found that lizard abundance was two- to threefold higher on bannertail kangaroo rat mounds then on the surrounding landscape, citing the importance of precincts as refuge from predators. I expected to find that lizards associated with precincts on a landscape

(plot) level at the Carrizo Plain. I also investigated whether this association occurred on a local level (at the scale of an individual precinct). I predicted that lizard density would positively correlate with precinct and burrow tunnel density, and that lizards would occur more often on kangaroo rat precincts than off precincts (Table 2).

2. Kangaroo rat engineering provides refuge from predators

Assessing refuge choice and other escape behaviors is an important aspect of understanding how animals use microhabitat (Schall & Pianka 1980; Martín & López

1995; Cooper & Wilson 2007). Animals must balance the costs and benefits of escape when responding to predation risk, and microhabitat structure can have marked effects on these factors. Previous research has shown that the type of refuge chosen can vary with microhabitat and refuge quality, though only a few studies have directly addressed the

use of burrows as refuges by lizards. Two previous studies have shown the use of burrows as refuge by lizards is dependent on temperature. Burrows were more frequently chosen as refuge when temperatures were extreme, indicating that the quality of burrows as refuge shifts with thermoregulatory needs (Cooper 2000; Davis & Theimer 2003). I predicted that lizards would use burrows more frequently than other refuge types and that their use of burrows as refuges would be contingent on ambient temperature (Table 2).

Optimal escape theory predicts that flight initiation distance (the distance between predator and prey when escape begins) is longer when predation risk is greater (Cooper

2009a). If precincts offer more refuges (burrow tunnels) than the surrounding landscape, then predation risk should be lower for lizards on precincts because the distance to the nearest refuge is shorter than in the intervening grassland matrix. I predicted that lizards on precincts would display shorter flight initiation distance in response to predation risk than lizards that were on unmodified habitat in between precincts (Table 2).

3. Kangaroo rat engineering provides lizards with thermal refuge

Temperature affects many life-history traits of lizards, including their embryonic development, growth, age at maturity, reproduction, temporal and seasonal activity patterns, and survival (Adolph & Porter 1993). Humidity can affect the rate of evaporative water loss in lizards. Therefore maintaining preferred body temperature and humidity through behavioral thermoregulation is a fundamental aspect of lizard life history. One reason lizards may associate with precincts is because of the unique thermal microclimate they provide and thus opportunity for thermoregulation. I predicted that

temperature and humidity within burrow tunnels and substrate temperatures on top of precincts would differ from the surrounding unmodified area (Table 2).

4. Kangaroo rat engineering provides lizards with increased prey resources

The attraction of arthropods to burrows are often attributed to increased microhabitat complexity and food subsidies from stored seed and vegetation clippings

(Hawkins & Nicoletto 1992; Davidson & Lightfoot 2007; Prugh and Brashares 2012). I experimentally manipulated the number of burrow tunnels on precincts, thus increasing the amount of refuge and microhabitat available to arthropods. I predicted that arthropod species richness, abundance, and biomass would be higher on experimental precincts with more artificial burrow tunnels than precincts with fewer tunnels (Table 2). Increased arthropod prey availability on precincts has been proposed as a mechanism behind the association of lizards with burrowing rodents, with conflicting evidence (Davidson et al.

2008; Gálvez Bravo et al. 2009; Prugh & Brashares 2012). If arthropod abundance and biomass were higher on experimental precincts with more artificial burrow tunnels then prey availability on a local scale could partially or fully account for any observations of increased lizard presence on precincts. If arthropod abundance and biomass were not higher on precincts with more burrow tunnels, then increased prey availability would most likely not be mechanism for lizard association with kangaroo rats on a local scale.

5. Lizard microhabitat use is dependent on burrow tunnel density

Translocations have been used extensively and successfully for decades in ecological research to determine the effects of experimental manipulations on individuals

(Dodd & Seigel 1991; Niewiarowski & Roosenburg 1993; Dickinson & Fa 2000; Soutera

2004; Iraeta et al. 2006; Huang et al. 2013). In one notable example, translocation was used to assess how habitat modification by elephants created patches of favorable habitat for lizards (Pringle 2008). Translocation offers a way to assess the effects of kangaroo rat habitat modification on lizard microhabitat use by placing lizards at experimental precincts and determining whether burrow tunnel density had an effect on the length of time lizards remained at the precinct. I predicted that lizards would stay longer if translocated to precincts with more burrow tunnels than lizards translocated to precincts with fewer burrow tunnels (Table 2).

Table 2. Hypotheses and predictions for the interaction between common side- blotched lizards and giant kangaroo rat ecosystem engineering.

Hypothesis Prediction Giant kangaroo rats facilitate Lizard density increases with burrow tunnel and common side-blotched lizards at precinct density. Lizards found more often on multiple spatial scales precincts than off. Kangaroo rat engineering facilitates Lizards use burrow tunnels as refuge. Lizards on lizards through: precincts display shorter flight initiation distance  Refuge from predators than lizards off precincts.  Thermal refuge Temperature and humidity is more variable and extreme outside of precincts than inside burrow tunnels.  Increased prey resources Arthropod species richness, abundance, and biomass is higher on precincts with more burrow tunnels than on precincts with fewer burrow tunnels. Lizard microhabitat use is dependent Lizards translocated to experimental precincts on burrow tunnel density with more burrow tunnels persist longer than lizards translocated to precincts with fewer or no burrow tunnels.

Methods

Study area

The Carrizo Plain National Monument is a 101,215-ha protected area within the

Carrizo Plain, a semiarid grassland in San Luis Obispo County, California. The region is

dominated by invasive annual grasses but still supports a large diversity of native plant

taxa (Schiffman 1994, 2007b; Germano et al. 2001). The Carrizo Plain is occupied by 13

animal species listed as threatened or endangered on a state and/or federal level.

Fieldwork was conducted at the study site May–October 2012, April–September 2013,

and June 2014. Cattle are routinely grazed in the study area, although no cattle were

present in 2012 and 2013 because drought severely limited forage production.

Study species

The common side-blotched lizard (Uta stansburiana) is a small, diurnal

phrynosomatid lizard found throughout western North America (Parker & Pianka 1975).

They prefer open areas and associate with a variety of arid and semi-arid habitats,

including pinyon-juniper, desert shrub-steppe, coastal scrub, and grassland (Davis &

Verbeek 1972; Parker & Pianka 1975). Common side-blotched lizards are primarily

insectivorous, with beetles, grasshoppers, ants, and termites constituting a large

proportion of their diet, although some herbaceous vegetation is also consumed (Parker &

Pianka 1975; Nagy 1987). They are sit-and-wait predators that position themselves on

perches or under vegetation to survey for prey (Waldschmidt 1983).

Giant kangaroo rats (Dipodomys ingens) are a federally endangered endemic

rodent of the western San Joaquin Valley region of California (Goldingay et al. 1997).

They are highly territorial, nocturnal rodents that occur in high densities throughout the

Carrizo Plain National Monument (Cooper & Randall 2007; Prugh & Brashares 2012).

Lizard, precinct and burrow tunnel surveys

Lizard, precinct, and burrow tunnel densities were visually surveyed along seven

100-m north-south line transects placed 20 m apart in twenty 100 × 100 m plots. The lizard and burrow tunnel surveys were conducted in June and July of 2012 and 2013; precincts were only surveyed in 2013. Each plot was surveyed for lizards three times, in random order, on different days between 0730–1500 hrs and when air temperature was between 25ºC–35ºC. Lizards sighted within 10 m of either side of the transects were counted, and their age class (adult, juvenile, or hatchling) and location (on or off a precinct) were recorded. Lizard counts were averaged for each plot across the three surveys and analyzed separately for 2012 and 2013. Surveys for precincts and burrow tunnels were conducted separately on the same twenty 100 × 100-m plots. To determine precinct density, precincts that had at least one edge within three meters of either side of each transect were counted. Spacing between transects prevented precincts from being counted multiple times. All burrow tunnels within three meters of either side of each transect were also counted. To determine the proportion of plots that was covered by precincts and unmodified habitat, an additional survey was conducted in June 2014 on the same twenty 100 × 100-m plots. I ran three transects on each plot and recorded the type of microsite as either a precinct or unmodified habitat at 10 m intervals along each transect. This gave a total of 18 sampling points for each plot.

Escape behavior and refuge choice

I conducted simulated predation risk trials in July–August 2012 and May–July

2013. I selected lizards haphazardly for trials by walking in a random direction from a starting point near the plots and including all lizards sighted. All trials took place between

0800–1100 hrs and when air temperature was 25ºC–35ºC to minimize differences due to lizard activity patterns. Trials were done near a new plot each day to avoid resampling individuals. Lizards that fled before the start of the trial were excluded from the study. I began a trial immediately after sighting a lizard. I recorded the initial microhabitat (bare ground, burrow entrance, or under vegetation) of the lizard and approached the lizard in a direct line path at a speed of approximately 40 m/min. All lizards initiated flight by the time I had approached within 3 m of their original location. I continued to pursue the focal lizard until it reached a refuge it remained in longer than 3 minutes (terminal refuge). I recorded the type of refuges the lizards chose to hide in and for lizards that chose multiple refuges, I recorded their initial refuge choice and their terminal refuge choice. All lizards sought refuge in vegetation, burrow tunnels, or stopped on bare ground. Air temperature was recorded at the focal lizard’s original location to determine if refuge choice differed with ambient temperature. After a trial was complete, I selected a new individual by walking in a random direction from the ending location of the last trial. If I determined that the new individual was close enough to the location of the previous trial that it potentially was aware of my presence before the start of the trial, I did not select that lizard and searched for a different individual.

In 2013, I repeated the trials and included additional data on whether the lizard was on or off a precinct at the start of the trial, the flight initiation distance (distance from the focal lizard to myself when the lizard initiates escape), the type of refuge nearest to the focal lizard, and the distance to the nearest refuge. To obtain flight initiation distance and distance to nearest refuge, I dropped a weighted strip of flagging tape during pursuit at the moment the focal lizard initiated flight. I tossed a second weighted strip to the original location of the lizard. I continued pursuit and marked refuges the focal lizard entered in the same manner until the lizard chose a terminal refuge. Terminal refuge choice signified the end of the trial. I recorded substrate surface temperature at the focal lizard’s original location as well as each refuge it entered using an infrared thermometer

(Oakton Mini-IR Thermometer, Oakton Instruments, Vernon Hills, IL).

Thermal microhabitat

I used temperature and humidity dataloggers (models DS1923 and DS1921G,

Maxim Integrated, San Jose, CA) to quantify thermal differences between burrow tunnels, precincts, shrubs, and unmodified bare substrate. I haphazardly selected precincts by walking 20 m from the road in a random direction and selecting the closest precinct to that point. Another 20 m was walked in a random direction and a precinct again chosen, until 13 precincts had been selected. Eight of the precincts were paired with an adjacent non-precinct area. Dataloggers were placed on the most elevated point on top of the unpaired precincts (n = 5), inside a burrow tunnel on each precinct (n = 13), and on adjacent non-precinct grassland matrix (n = 8). To prevent dataloggers from being lost inside burrows, I attached each to a 1-m long wire secured to a roofing nail embedded in

the ground outside the burrow. I selected shrubs in the same manner as precincts. I walked 20 m in a random direction from a predetermined starting point near one of the plots and chose the closest shrub to that point. All other shrubs were chosen by walking

20 m in a random direction from the last shrub and selecting the shrub closest to that point. GPS coordinates were taken for each datalogger (eTrex 20, Garmin, Olathe, KS) and locations flagged. Dataloggers were deployed from 1–30 September 2013.

Precinct Manipulation

In April 2013, I experimentally manipulated the number of burrow tunnels at unoccupied precincts, thus increasing or decreasing the number of available refuges and hence, the number of microhabitats for predator avoidance and thermoregulation. I employed a randomized block design to investigate the effect of burrow tunnel density on lizard occupancy (Figure 1). Precincts with no discernible signs of occupation by kangaroo rats (absence of recent soil disturbance) were selected for inclusion in this study as the experimental units. Two sites located 2-km apart were selected for the experiment.

Five blocks of eight precincts each were located at least 100-m apart at each site.

Treatments were replicated once within blocks so that two precincts in each block received the same treatments. Unoccupied precincts were experimentally manipulated to simulate a range of kangaroo rat burrowing activity with eight, four, two, or zero burrow tunnels. Artificial burrows tunnels were constructed using a hand auger and measured approximately 20 mm in diameter, 1.5 m in depth, and were angled approximately at a 5º decline. Precincts were monitored weekly to maintain the experimental treatment, removing loose dirt from inside artificial burrows as necessary.

Figure 1. Schematic showing generalized experimental design. Colored circles represent precincts, squares represent blocks.

Precinct surveys and translocation experiment

I conducted a lizard translocation experiment in July and August 2013 by transplanting 32 common side-blotched lizards to experimental precincts. Four of the 10 blocks were randomly selected for inclusion in this experiment. I collected lizards by hand using a modified telescopic fishing pole with a noose. Individuals used in this study were collected at least 100 m away from the area to which they were translocated (Hein

& Whitaker 1997; Tinker et al. 1962). I marked each individual on the dorsum with two stripes of non-toxic paint in a unique color combination (Figure 2) so that they could be

identified at up to 20 m without being recaptured (Simon & Bissinger 1983). Paint markings typically last until the animal sheds.

Once lizards were collected and marked, I introduced a single lizard to each of eight precincts in a given block on the same day; however, I only introduced lizards to two blocks per week. Translocations occurred over a 2.5-week period and resulted in 32 lizard translocations. I surveyed each precinct for translocated lizards once a day for seven days. I scanned each precinct using binoculars from 20–30 m away before approaching and using a burrow cam (Peeper 2000, Sandpiper Technologies, Manteca,

CA) to briefly inspect each of the artificial burrow tunnels. The burrow cam is a small camera attached to a long flexible cord and can be inserted into burrows to identify inhabitants. If a lizard was not seen at a precinct, I continued to survey that precinct for two additional days. If the lizard was not sighted during this period, I eliminated the precinct from the surveys. I ended the experiment and censored the data after seven days.

Figure 2. Common side-blotched with unique color coded paint marking on dorsum.

Arthropod sampling

I sampled arthropods at the experimental precincts by pitfall trapping. I set pitfall traps out at the precincts on 12 June 2013. Two traps were placed on each precinct, approximately 40 cm from the precinct edge and at least 50 cm apart. Pitfall traps were constructed by digging a small hole with a spade and placing a plastic cup (12.7 cm height × 8.9 cm dia; 473 ml capacity) into the hole so that the top of the cup was level with the ground. Traps were filled with 2 cm of propylene glycol and a piece of plastic aviary fencing placed inside the cup at the rim to prevent incidental take of vertebrates.

Traps were covered with 25 × 25-cm pieces of aluminum flashing with 2.5 cm of space between the cover and ground to prevent desiccation of the fluid inside the trap. I left traps in the field for two weeks, collecting them on 26 June 2013. I checked traps for disturbance after one week, refilling as necessary.

All arthropods captured in the pitfalls were counted and identified to order and morphospecies. Morphospecies are recognizable taxanomic units that are classified based on easily identifiable morphological characteristics and provide an alternative to time consuming taxonomic species identification (Derraik et al. 2002). Voucher specimens were kept to ensure consistent classification across all experimental units. Each pitfall trap sample was weighed to obtain biomass estimates.

Statistical analyses

The lizard, precinct and burrow tunnel density data was analyzed separately for

2012 and 2013 using parametric correlation. Lizard location on or off precinct in 2013 was analyzed using a chi-square goodness of fit test. The proportion of precincts to

unmodified habitat was also compared using a chi-square goodness of fit test. Refuge choice was analyzed separately for 2012 and 2013 using chi-square goodness of fit tests as was nearest refuge type in 2013. Distance to nearest refuge by type in 2013 was log transformed and analyzed using a two-sample t-test. Flight initiation distance data was log transformed and analyzed using ANCOVA with flight initiation distance as the dependent variable, location (on or off a precinct) as a fixed predictor variable and substrate surface temperature included as a covariate (Table 3). ANCOVA evaluates whether two or more group means are equal while statistically controlling for the influence of one or more covariates. ANCOVA models therefore adjust group means and standard error to remove variance due to the covariate (Quinn & Keough 2002).

Differences in daily ambient average relative humidity as well as minimum and maximum relative humidity between burrow tunnels and aboveground on precincts (at the most elevated point) were assessed using paired t-tests for each variable. Differences in overall average temperature, average minimum temperature, and average maximum temperature between burrow tunnels, intermound areas, and underneath shrubs was analyzed using one-way ANOVA. Translocation data were analyzed using a Cox

Proportional-Hazards model (Cox 1972). The block and the number of burrow tunnels (8,

4, 2, and 0) were included as effects and lizard temporal persistence on the precincts as the response variable. I analyzed log-transformed arthropod abundance, biomass, and species richness data with split-plot nested ANOVA with site and experimental treatment as factors and block as the nested factor (Table 4).

Table 3. ANCOVA table for tests of predictor variables and covariates on flight initiation distance.

* Denotes covariate

Source df F ratio

Location 1 MSmicrohabitat/MSresidual

Temperature* 1 MStemperature/MSresidual

Residual 45

Table 4. ANOVA table for tests of experimental manipulations on arthropod assemblage parameters.

Source df F ratio

Site 1 MSsite/MSblock(site)

Block(Site) 8 MSblock(site)/MSresidual

Treatment 3 MStreatment/MStreatment*block(site)

Treatment*Site 3 MStreatment*site/MStreatment*block(site)

Treatment*Block(Site) 24 MStreatment*block(site)/MSresidual

Residual 34

Results

Facilitation of common side-blotched lizards

Common side-blotched lizard density was significantly positively correlated with precinct density in 2013 (Pearson’s r = 0.54, P = 0.02; Figure 3). Lizard density was also positively correlated with burrow tunnel density in both 2012 (r = 0.67, P < 0.01; Figure

4) and 2013 (r = 0.51, P = 0.04; Figure 4). Lizards sighted during censuses in 2013 were significantly more likely to be seen on precincts (n = 118) than in the areas between

2 precincts (n = 48;  1,166 = 29.52, P < 0.001). Non-precinct microhabitat covered a significantly larger portion of the study area (69%; n = 248) than precincts, (31%; n =

2 112;  1,360 = 51.38, P < 0.001).

plot

2 m - 8

2 Lizard density Lizard density per 100

0 0 50 100 150 200 Precinct density per 100-m2 plot

Figure 3. Relationship between common side-blotched lizard density and giant kangaroo rat precinct density on 100-m2 plots (n = 20) in 2013 at Carrizo Plain National Monument (r = 0.54, P = 0.02).

plot

2 m - 8

6 2013

4 2012

2 Lizard density Lizard density per 100 0 100 150 200 250 300 350 400 Burrow tunnel density per 100-m2 plot

Figure 4. Relationship between common side-blotched lizard density and giant kangaroo rat burrow tunnel density in 2012 (open circles; r = 0.67, P < 0.01, n = 20) and 2013 (black circles; r = 0.51, P = 0.03, n = 17) at Carrizo Plain National Monument.

Refuge from predators

During the 2012 predation risk trials, lizards chose burrow tunnels (n = 46) as

2 refuges more frequently than vegetation (n = 8;  1,54 = 29.63, P < 0.001). In 2013, lizards

2 were equally likely to be nearest to vegetation as burrow tunnels ( 1,52 = 1.59, P = 0.21) but still chose burrow tunnels (n = 48) as refuges more frequently than vegetation (n = 4;

2  1,52 = 40.69, P < 0.001). The distance between lizards and the nearest refuge did not differ between vegetation and burrow tunnels (t1,49 = -1.30, P = 0.20; Figure 5). Refuge

2 choice did not differ between temperature classes, ( 4,54 = 3.70, P = 0.16). Lizards on precincts (n = 35) displayed shorter flight initiation distance than lizards off precincts

(n = 17; F1,49 = 4.65, P = 0.04; Figure 6). Ambient substrate temperature was not a

2 significant predictor of flight initiation distance (F1,49 = 0.74, P = 0.39, r = 0.09).

Figure 5. Log-transformed distance from focal lizards to the nearest burrow tunnel refuges (n = 30) and nearest vegetation refuges (n = 21). Means and standard error are shown.

Figure 6. Log-transformed flight initiation distance of lizards on (n = 35) and off precincts (n = 17). Means and standard error shown have been adjusted to remove variance due to the covariate (Lane & Sándor 2009).

Thermal refuge

Average daily temperature was higher inside burrow tunnels than aboveground on precincts (difference = 3.9˚C, t114 = –10.94, P < 0.001, as was minimum daily temperature (difference = 15.6˚C, t114 = –88.69, P < 0.001). However, maximum daily temperature was lower inside burrow tunnels than aboveground on precincts (difference

= –15.7˚C, t114 = 16.12, P < 0.001; Table 5).

Average daily relative humidity was higher aboveground on precincts than inside burrow tunnels (difference = 11.0˚C, t114 = –10.821, P < 0.001). Minimum daily relative humidity was lower aboveground on precincts than inside burrow tunnels (difference =

11.3˚C, t114 = 8.55, P < 0.001). Maximum daily relative humidity was higher aboveground on precincts than inside burrow tunnels (difference = 36.7˚C, t114 = –29.73,

P < 0.001; Table 5).

Microhabitat had a significant effect on average temperature (F2,19 = 4.57,

P = 0.02; Figure 8). Average temperature was higher inside burrow tunnels than underneath shrubs (difference = 1.6˚C, P = 0.04) and marginally lower than intermound areas (difference = 1.9˚C, P = 0.05) but did not differ between intermound areas and underneath shrubs (difference = 0.3˚C, P = 0.94; Table 6).

Microhabitat also had a significant effect on average minimum temperature

(F2,19 = 12.89, P < 0.001) and average maximum temperature (F2,19 = 6.65, P = 0.01;

Figure 7). Average minimum temperature was higher inside burrow tunnels than underneath shrubs (difference = 5.5˚C, P = 0.01), and on intermound areas (difference =

10.0˚C, P < 0.001) but did not differ between intermound areas and underneath shrubs

(difference = 4.5˚C, P = 0.08; Table 6). Average maximum temperature did not differ between burrow tunnels and underneath shrubs (difference = 6.2˚C, P = 0.05) but was lower in burrow tunnels than on intermound areas (difference = 10.1˚C, P < 0.007) and did not differ between intermound areas and underneath shrubs (difference = 3.9˚C,

P = 0.36; Table 6).

Table 5. Mean and standard deviation temperature and humidity values for paired belowground burrows and aboveground precincts.

Temperature Humidity Microhabitat (˚C) (%RH) Average Precinct (aboveground) 18.6 ± 0.4 41.3 ± 1.2 Burrow tunnel 22.5 ± 0.2 30.3 ± 0.5 Minimum Precinct (aboveground) 4.7 ± 0.2 14.5 ± 1.7 Burrow tunnel 20.3 ± 0.2 25.8 ± 0.5 Maximum Precinct (aboveground) 40.1 ± 1.0 71.3 ± 1.5 Burrow tunnel 24.4 ± 0.2 34.6 ± 0.6

Table 6. Mean and standard deviation temperature values for 3 different microhabitats.

Temperature Microhabitat (˚C) Average Burrow tunnel 20.2 ± 0.5 Shrub 18.6 ± 0.4 Intermound 18.3 ± 0.6 Minimum Burrow tunnel 16.1 ± 1.2 Shrub 10.6 ± 1.2 Intermound 6.1 ± 1.6 Maximum Burrow tunnel 24.9 ± 1.8 Shrub 31.1 ± 1.7 Intermound 35.0 ± 2.3

Figure 7. Differences in mean, average minimum, and average maximum temperature for three microhabitats at the Carrizo Plain National Monument (Mean and SE).

Prey resources

Arthropod species richness did not differ between sites (F1,8 = 4.57, P = 0.07), but differ between blocks (F8,34 = 0.95, P = 0.49). There was no effect of treatment

(F3,24 = 0.03, P = 0.99). There was no significant interaction between treatment and site

(F3,24 = 0.79, P = 0.51) or treatment and block (F24,34 = 1.07, P = 0.42). Arthropod abundance also did not differ between sites (F1,8 = 0.72, P = 0.42) block (F8,34 = 1.95,

P = 0.08) or treatment (F3,24 = 1.04, P = 0.39). There was no significant interaction between treatment and site (F3,24 = 0.19, P = 0.90) but there was a marginally significant interaction between treatment and block (F24,34 = 1.85, P = 0.05; Figure 8). Arthropod biomass did not differ between sites (F1,8 = 0.01, P = 0.92) block (F8,34 = 0.61, P = 0.76) or treatment (F3,24 = 0.30, P = 0.83). There was no significant interaction between treatment and site (F3,24 =0.51, P = 0.68) or treatment and block (F24,34 =1.20, P = 0.31).

Figure 8. Interaction plot of mean arthropod abundance at precincts with 0, 2, 4, and 8 burrow tunnels at 10 blocks at the Carrizo Plain National Monument (n = 80).

Lizard microhabitat use

Lizard persistence on experimental precincts did not differ between blocks (X2 =

0.43, P = 0.52), so data were pooled for further analyses. The number of burrow tunnels significantly affected lizard persistence (X2 = 4.38, P = 0.04), with lizards transplanted onto experimental precincts with more burrow tunnels occupying those precincts longer

(Figure 9). The persistence of lizards on precincts with relatively high densities of burrow tunnels (4 or 8 per precinct) did not differ from each other. Similarly, persistence on precincts with no or only 2 burrow tunnels also did not differ. However, lizards transplanted onto precincts with 4 or 8 burrow tunnels occupied their precincts longer than lizards on precincts with 0 or 2 (Mean and S.E. of 2.75 ± 0.33 and 3.63 ± 0.31 days vs. 0.13 ± 0.04 and 1.63 ± 0.13 days, P < 0.01).

Figure 9. Temporal persistence curves (Kaplan–Meier estimates of survival function plotted against time) for lizards occupying experimental precinct with 0, 2, 4, or 8 burrow tunnels during the 7-day study period. Letters denote significant differences (log-rank P < 0.008, n = 8 in each group).

Discussion

Facilitation of common side-blotched lizards

The results of this study clearly demonstrate a facilitative role for giant kangaroo rats in the spatial distribution, microhabitat use, and behavior of common side-blotched lizards. Across plots, lizards were found in higher densities where kangaroo rat precincts were most numerous. At the individual precinct scale, lizards were more than twice as likely to be seen on precincts as in the areas between precincts, even though precincts cover only 30% of the environment. This strongly suggests that in this ecosystem, precincts are more important microhabitat for this lizard species than unmodified microhabitat. These results provide further evidence that burrowing mammals produce positive effects on associated species at multiple scales. They are consistent with the findings of Davidson et al. (2008), who demonstrated that reptile abundance was higher both in areas of higher bannertail kangaroo rat mound density and on individual mounds relative to the surrounding environment. In some ecosystems, the effects of engineering may be more pronounced at smaller scales (Hastings et al. 2007). Ectothermic species, especially those species with small home ranges, are likely to respond to fine-scale differences between microhabitats (Vitt et al. 2007). Giant kangaroo rat engineering likely facilitates the ability of common side-blotched lizards to exploit habitat resources within engineered microhabitat through multiple mechanisms.

Refuge from predators

Precincts provide a complex network of burrow tunnels that are used by lizards as refuge from predators. The function of burrow tunnels as refuges from predators

produces facilitative effects on lizards that are indirect and could be considered both density-mediated (higher densities of kangaroo rats create higher densities of burrow tunnels) and indirect and trait-mediated (altering lizard escape behavior). Similarly, other types of ecosystem engineers directly affect predation rates on associated species by providing physical structures in which to refuge (Caley & St John 1996; Sanders et al.

2014). Martinsen et al. (2000) found that the refuges created by leaf-rolling insects increased arthropod species abundance on cottonwood trees by seven-fold. Roznik &

Johnson (2009) found that the mortality of juvenile gopher frogs that used gopher tortoise burrows as refuge was only 4% of the mortality of gopher frogs that did not use burrows as refuges. In my study, lizards preferred to refuge in burrow tunnels rather than vegetation, even though both features were equally available. Lizards selected burrow tunnels over vegetation even at moderate ambient temperatures, when thermoregulatory costs of refuging in vegetation should be low. This indicates that the perception of burrow tunnels as high quality refuges from predators is separate from their value as thermal refuges. The Carrizo Plain ecosystem is habitat to a multitude of aerial predators, including loggerhead shrikes, burrowing owls, common ravens, and several species of kites, hawks, and falcons (Smythe & Coulombe 1971; Rosier et al. 2006; Bureau of Land

Management 2013). Though burrows probably do not prevent snakes or larger lizards

(e.g., blunt nosed leopard lizards, Gambelia sila) from pursuing common side-blotched lizards, burrow tunnels are likely highly effective refuges from aerial predators.

Interestingly, research at the study site found that plant biomass was low in 2012 and

2013 (L. Prugh, unpublished data). Therefore, it is possible that the frequency with which

lizards use vegetation as refuges may increase in years of high plant productivity. This would be congruent with the general observation that ecosystem engineering is most important in stressful environments (Crain & Bertness 2006).

Animals that are often prey for other species may change their refuging/predator avoidance behavior in the presence of ecosystem engineering (Pintor & Soluk 2006;

Gálvez Bravo et al. 2009; Gribben & Wright 2013). Lizards on precincts allowed a human observer to approach more closely before fleeing than lizards in intermound areas, indicating that lizards on precincts viewed approaching predators to be less of a threat when burrow tunnels were immediately available to refuge in. Prey weigh the costs and benefits of escape from a predator in real time, and should flee from an approaching predator when the cost of staying equals the cost of escape (Cooper 2006). Escape can result in a variety of negative outcomes for potential prey species that include loss of foraging opportunities, decreases in reproductive success, and interruptions in social activity (Cooper 2009b; Lagos et al. 2009; de Jong et al. 2013). Moreover, changes in escape behavior in response to ecosystem engineering can lead to strategies that directly reduce predation or produce positive effects on life history parameters. Gálvez Bravo et al. (2009) demonstrated that lizards in areas with rabbit burrows (used as refuge from predators) were larger (snout–vent length) than lizards in areas that did not include rabbit burrows, controlling for habitat type. Kangaroo rat engineering could have a positive impact on lizard fitness because lizards on precincts should have more time available for foraging, defending territory, and looking for mates than lizards on inter-mound areas due to the differences in flight initiation distance. However, changes in escape behavior do

not always produce net positive effects on prey because refuging can have negative consequences for prey fecundity and growth (Orrock 2013). For example, Gribben and

Wright (2013) found that while high densities of seagrass (ecosystem engineers) reduced the predator encounter rate for clams, mortality due to predation actually increased because high seagrass density also reduced clam predator avoidance behavior (burial in soft sediment).

Thermal refuge

Environmental stress amelioration is one important outcome of many interactions between facilitators and associated species (Jones et al. 2010). Below-ground burrows constructed by ecosystem engineers provide thermal microclimates that are less extreme and more stable over time than ambient, above-ground conditions (Pike & Mitchell

2013). Burrow tunnels were less variable in temperature and relative humidity than the outside environment, whether on precincts mounds, between precincts, or underneath shrubs. Daily temperature varied by less than 5ºC within burrow tunnels but by more than

30ºC on precincts, more than 25ºC between precincts, and more than 20ºC underneath shrubs. Relative humidity varied five-fold more on precincts than inside burrow tunnels.

Lizards must behaviorally thermoregulate to maintain optimum body temperature.

Shuttling between precincts, burrow tunnels, and the surrounding environment, as well as seeking out the more stable thermal environment of burrow tunnels during the hottest and coldest parts of the day, may be one mechanism through which lizards accomplish this

(Heath 1970). In addition, lizards may seek refuge in burrow tunnels in order to avoid water loss during dry weather or high winds (Waldschmidt & Porter 1987). Lizard

reproduction may also benefit from the presence of burrow tunnels. Soil moisture is an important factor in lizard nest-site selection and burrows may provide an ideal environment for oviposition (Marco et al. 2004; Gálvez Bravo et al. 2009; Warner &

Andrews 2009). If lizards do benefit from the thermal microclimate provided by precincts

(not directly tested in this study), thermal stress amelioration is an indirect facilitative effect of kangaroo rat engineering that is mediated by lizard behavioral traits. These results are congruent with studies finding strong positive effects of thermal refuges constructed by engineers on associated species (Milne & Bull 2000; Read et al. 2008;

Whittington-Jones et al. 2011). Walde et al. (2009) demonstrated that diurnal use of desert tortoise burrows by horned larks allow them to inhabit areas with temperatures that regularly exceeded their thermal maximum. Grillet et al. (2010) found that populations of the threatened ocellated lizard were highly dependent on rabbit warrens to provide thermal microhabitat to buffer against temperature extremes, recommending that conservation efforts for the ocellated lizard be focused in areas occupied by rabbits. As the climate continues to change and ambient temperature becomes more extreme, burrow constructing ecosystem engineers may become a crucial factor in the persistence of communities and maintaining biodiversity (Pike & Mitchell 2013). This may be especially important to the persistence of ectothermic species, which are potentially more vulnerable to species extinctions following climate change (Kearney et al. 2009; Sinervo et al. 2010).

Prey resources

The arthropod community generally did not respond to precinct manipulations.

Arthropod species richness, abundance, and biomass did not differ between precincts with zero, two, four, or eight burrow tunnels. However, arthropod species richness significantly differed between blocks. The significant interaction between treatment and block for arthropod abundance reveals that in two of the blocks, abundance was higher at precincts with fewer burrow tunnels, contrary to the predicted outcome, whereas at the other eight blocks, abundance either showed no trend or was higher at precincts with more burrow tunnels (Figure 8). Therefore, the treatment effect was not consistent among blocks and suggests that the number of burrow tunnels is not an important factor in arthropod microhabitat selection. These results are consistent with Prugh and Brashares

(2012), who found that at the plot level, arthropod abundance and biomass were higher when kangaroo rat density was higher, but that there was no difference in arthropod community parameters at the local scale between precincts and surrounding unmodified habitat. These results suggest that though greater prey availability at the landscape level may facilitate common side-blotched lizards, it does not explain why lizards prefer engineered microhabitat to the surrounding environment. It is likely that the availability of refuge from predation and thermal extremes accounts for lizard microhabitat preferences.

Lizard microhabitat use

Translocated lizards occupied experimental precincts longer when the density of burrow tunnels was relatively high. Interestingly, there was no difference in how long

lizards occupied precincts with zero and two burrow tunnels, but lizards stayed significantly longer when precincts had either four or eight. This suggests that there may be a minimum number of burrow tunnels needed to establish favorable conditions for lizards. Two burrow tunnels or fewer may not provide sufficient space for predator avoidance and/or thermoregulatory needs. Lizards occupying precincts with zero burrow tunnels showed the steepest temporal persistence curve, with only one out of eight lizards occupying their precinct for longer than a day, compared with the persistence curves for lizards occupying precincts with four or eight burrow tunnels (of which, each had one out of eight lizards still remaining at their precinct after seven days). Though this study did not determine the fate of lizards that abandoned the precincts to which they had been translocated (presumably to locate more suitable habitat or were depredated), it is possible that kangaroo rat burrow tunnels are more than merely beneficial to common side-blotched lizards, but may actually be a necessary component of suitable lizard habitat at the study site.

Conclusions

Though all organisms create and destroy their environments to some extent, ecosystem engineers can have large and lasting impacts on their communities that rival interactions such as competition and predation as a force in determining where and at what density species are distributed, and produce patterns of species diversity that can last over evolutionary time scales (Erwin 2008; Pearce 2011). The role of burrowing mammals as ecosystem engineers has received much attention in recent years (Davidson et al. 2012). Although their effects on the diversity and spatial distribution of other

species has been well documented, most studies have relied on a correlational approach to investigate these relationships. Since the effects of these keystone species have been attributed to many different mechanisms (e.g., habitat heterogeneity, underground microhabitat construction, soil disturbance and food subsidizing, among others) experimental approaches are required to tease apart the important role burrowing engineers play in the communities in which they occur. The results of this study contributes to our understanding of the impact the functional attributes of structural habitat modification by an ecosystem engineer has on associated species. Furthermore, examples of the effects of ecosystem engineering on the behavior of associated non- engineering species are rare in the literature. This study addresses how habitat modification by an engineer can influence the microhabitat use and escape behavior of an associated species. Examining such relationships has important implications for understanding community dynamics and interactions between species.

Giant kangaroo rats are keystone species that structure their community through two pathways: their engineering activities and trophic interactions (Prugh & Brashares 2012).

Though this study focused on a single species’ response, giant kangaroo rats control the abundances of many other species. The majority of these interactions are indirect, mediated through their effect on the abiotic environment. As with other facilitators, the negative effects of kangaroo rats are suppressed by their positive effects on other species and their presence promotes coexistence within the community (2012). Facilitation can support coexistence even when the net interaction is negative overall (e.g., positive interactions between competitors outweighed by competition), and may even buffer

against species extinction (Gross 2008; Verdú & Valiente‐Banuet 2008). Facilitation is capable of structuring ecological networks that are complex, persistent, and resilient to disturbance, especially when networks are highly connected and nested (Thébault &

Fontaine 2010). However, the strength of facilitative interactions is often context- dependent, varying with the degree of environmental stress (Crain & Bertness 2006;

Farjado & McIntire 2011). During my study, California was in a state of severe drought and precipitation reached a record low in 2013 (http://www.ca.gov/drought/). Vegetation cover on the Carrizo Plain was lower in 2012 and 2012 than in previous years (L. Prugh, unpublished data). Further research should be conducted in years of high productivity to investigate whether the strength of this relationship is influenced by environmental conditions (e.g., stronger in years of drought or other stressful conditions). Given the strong, positive relationship between kangaroo rats and lizards in current conditions, it is likely that ecosystem engineering by kangaroo rats will be become increasingly important to this species of lizard and others as climate change progresses. Microhabitat heterogeneity can reduce community vulnerability to extinction due to climate change

(Sheffers et al. 2014). As conditions become more extreme, kangaroo rat engineering has the potential to buffer the negative impacts of climate change on ectothermic species mortality and fitness as well as slow or prevent shifts in habitat. This presents a significant issue for land managers given that kangaroo rats and other small mammals themselves are likely to be greatly impacted by climate change through loss of habitat and the negative effects of temperature extremes, and highlights the need for conservation efforts to be focused on protecting giant kangaroo rat populations (Koontz

et al. 2001; Moritz et al. 2008). The Carrizo Plain is one of the few areas of suitable habitat that remain for many California endemic species found in semiarid grassland.

Therefore, understanding the interactions between the species inhabiting the Carrizo

Plain has direct implications for the management of this ecosystem.

Burrowing mammals are keystone engineers that create and modify habitat, increase biodiversity, shape plant communities, and influence the density and distribution of associated species (Cully et al. 2010; Davidson et al. 2012; Bryce et al. 2013; Kurek et al. 2014). This is a role that is important in structuring many communities and cannot be replaced by other non-burrowing species (Machiote et al. 2004; James et al. 2011;

Fleming et al. 2014). As such, conservation and restoration of burrowing mammal species and populations are a major conservation concern and deserving of considerable research efforts (Byers et al. 2006; Delibes-Mateos et al. 2011; Davidson et al. 2012).

Further research is needed to determine the ecological impact of the loss of burrowing mammal populations, how these populations will respond to climate change, and how that will affect whole communities. Land owners and managers would benefit from research demonstrating the economic and ecological value of ecosystem services provided by burrowing mammals. Finally, investigating how the strength and direction of interactions between burrowing mammals and associated species change across environmental gradients and are mediated by the traits of associated species can help us understand the causes and consequences of burrowing mammal ecosystem engineering on ecosystem health and diversity.

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