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
By
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
ii
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.
iii
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.
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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
v
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
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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
vii
ABSTRACT
EFFECTS OF ECOSYSTEM ENGINEERING BY THE GIANT KANGAROO RAT
ON THE COMMON SIDE-BLOTCHED LIZARD
By
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
viii
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.
ix
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
1
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
2
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
3
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 densitymediated, 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 traitmediated 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
4
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 webmaking 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.
5
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,
6
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
7
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
8
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
9
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 sideblotched 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 sideblotched 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
10
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.
Mechanism
Refuge from predation
Refuge from predation
Trophic facilitation
Abiotic stress amelioration
Description
Burrow tunnels create
physical refuge from
predators
Alteration of refuging
behavior
Higher arthropod
abundance in the
presence of kangaroo
rats
Precinct structure, e.g.,
burrow tunnels, create
thermal environment
microsites
11
Direct or
indirect
Indirect
Density- or traitmediated
Trait-mediated
Indirect
Trait-mediated
Indirect
Density-mediated
Indirect
Trait-mediated
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
12
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
13
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
14
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 sideblotched lizards and giant kangaroo rat ecosystem engineering.
Hypothesis
Giant kangaroo rats facilitate
common side-blotched lizards at
multiple spatial scales
Prediction
Lizard density increases with burrow tunnel and
precinct density. Lizards found more often on
precincts than off.
Kangaroo rat engineering facilitates
lizards through:
 Refuge from predators
Lizards use burrow tunnels as refuge. Lizards on
precincts display shorter flight initiation distance
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.
Lizards translocated to experimental precincts
with more burrow tunnels persist longer than
lizards translocated to precincts with fewer or no
burrow tunnels.
Lizard microhabitat use is dependent
on burrow tunnel density
15
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).
16
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.
17
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.
18
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
19
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.
20
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
21
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.
22
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
23
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).
24
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
25
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
precincts (n = 48; 21,166 = 29.52, P < 0.001). Non-precinct microhabitat covered a
significantly larger portion of the study area (69%; n = 248) than precincts, (31%; n =
112; 21,360 = 51.38, P < 0.001).
Lizard density per 100-m2 plot
12
10
8
6
4
2
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).
26
Lizard density per 100-m2 plot
12
10
8
6
2013
2012
4
2
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
refuges more frequently than vegetation (n = 8; 21,54 = 29.63, P < 0.001). In 2013, lizards
were equally likely to be nearest to vegetation as burrow tunnels (21,52 = 1.59, P = 0.21)
but still chose burrow tunnels (n = 48) as refuges more frequently than vegetation (n = 4;
21,52 = 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
choice did not differ between temperature classes, (24,54 = 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
significant predictor of flight initiation distance (F1,49 = 0.74, P = 0.39, r2 = 0.09).
27
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).
28
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
29
(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.
Microhabitat
Precinct (aboveground)
Burrow tunnel
Minimum Precinct (aboveground)
Burrow tunnel
Maximum Precinct (aboveground)
Burrow tunnel
Average
Temperature
(˚C)
18.6 ± 0.4
22.5 ± 0.2
4.7 ± 0.2
20.3 ± 0.2
40.1 ± 1.0
24.4 ± 0.2
Humidity
(%RH)
41.3 ± 1.2
30.3 ± 0.5
14.5 ± 1.7
25.8 ± 0.5
71.3 ± 1.5
34.6 ± 0.6
Table 6. Mean and standard deviation temperature values for 3 different
microhabitats.
Microhabitat
Burrow tunnel
Shrub
Intermound
Minimum Burrow tunnel
Shrub
Intermound
Maximum Burrow tunnel
Shrub
Intermound
Average
Temperature
(˚C)
20.2 ± 0.5
18.6 ± 0.4
18.3 ± 0.6
16.1 ± 1.2
10.6 ± 1.2
6.1 ± 1.6
24.9 ± 1.8
31.1 ± 1.7
35.0 ± 2.3
30
Figure 7. Differences in mean, average minimum, and average maximum
temperature for three microhabitats at the Carrizo Plain National Monument
(Mean and SE).
31
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).
32
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).
33
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).
34
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
35
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
36
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
37
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
38
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).
39
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
40
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
41
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 nonengineering 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
42
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 contextdependent, 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
43
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.
44
Literature Cited
Abrams, P. A. (1982). Functional responses of optimal foragers. The American
Naturalist, 120, 382—390.
Adolph, S. C. (1990). Influence of behavioral thermoregulation on microhabitat use by
two Sceloporus lizards. Ecology, 71, 315–327.
Adolph, S. C., & Porter, W. P. (1993). Temperature, activity, and lizard life
histories. American Naturalist, 142,273–295.
Angelini, C., Altieri, A. H., Silliman, B. R., & Bertness, M. D. (2011). Interactions
among foundation species and their consequences for community organization,
biodiversity, and conservation. BioScience, 61, 782—789.
Bagchi, S., Namgail, T., & Ritchie, M. E. (2006). Small mammalian herbivores as
mediators of plant community dynamics in the high-altitude arid rangelands of
trans-Himalaya. Biological Conservation, 127, 438–442.
Bangert, R. K., & Slobodchikoff, C. N. (2006). Conservation of prairie dog ecosystem
engineering may support arthropod beta and gamma diversity. Journal of Arid
Environments, 67, 100–115.
Belthoff, J. R., & Smith, B. W. (2003). Patterns of artificial burrow occupancy and reuse
by burrowing owls in Idaho. Wildlife Society Bulletin, 31,138–144.
Bertness, M. D., & Callaway, R. (1994). Positive interactions in communities. Trends in
Ecology & Evolution, 9, 191—193.
Brock, R. E., & Kelt, D. A. (2004). Keystone effects of the endangered Stephens’
kangaroo rat (Dipodomys stephensi). Biological Conservation, 116, 131–139.
Bronstein, J. L. (2009). The evolution of facilitation and mutualism. Journal of Ecology,
97, 1160—1170.
Brown, J. H. & Heske, E. J. (1990). Control of a desert grassland transition by a keystone
rodent guild. Science, 250, 1705–1707.
Bruno, J. F., Stachowicz, J. J., & Bertness, M. D. (2003). Inclusion of facilitation into
ecological theory. Trends in Ecology & Evolution, 18, 119–125.
Bryce, R., van der Wal, R., Mitchell, R., & Lambin, X. (2013). Metapopulation dynamics
of a burrowing herbivore drive spatio-temporal dynamics of riparian plant
communities. Ecosystems, 16, 1165–1177.
45
Bureau of Land Management. (2013, November 12). Checklist of birds. Carrizo Plain
National Monument. Retrieved 1 June 2014 from
http://www.blm.gov/ca/st/en/fo/bakersfield/Programs/carrizo/birds.html
Byers, J., Cuddington, K., Jones, C., Talley, T., & Hastings, A. (2006). Using ecosystem
engineers to restore ecological systems. Trends in Ecology & Evolution, 21, 493–
500.
Cáceres-Charneco, R. I., & Ransom, T. S. (2010). The influence of habitat provisioning:
use of earthworm burrows by the terrestrial salamander, Plethodon cinereus.
Population Ecology, 52, 517–526.
Caley, M. J., & St. John, J. (1996). Refuge availability structures assemblages of tropical
reef fishes. Journal of Animal Ecology, 65, 414–428.
Callaway, R. M. (1995). Positive interactions among plants. The Botanical Review, 61,
306—349.
Canals, R. M., Herman, D. J., & Firestone, M. K. (2003). How disturbance by fossorial
mammals alters N cycling in a California annual grassland. Ecology, 84, 875–881.
Ceballos, G., Pacheco, J., & List, R. (1999). Influence of prairie dogs (Cynomys
ludovicianus) on habitat heterogeneity and mammalian diversity in Mexico.
Journal of Arid Environments, 41, 161–172.
Cooper, L. D., & Randall, J. A. (2007). Seasonal changes in home ranges of the giant
kangaroo rat (Dipodomys ingens): A study of flexible social structure. Journal of
Mammalogy, 88, 1000—1008.
Cooper, W. E. (1997). Escape by a refuging prey, the broad-headed skink (Eumeces
laticeps). Canadian Journal of Zoology, 75, 943–947.
Cooper, W. E. (2000). Effect of temperature on escape behaviour by an ectothermic
vertebrate, the keeled earless lizard (Holbrookia propinqua). Behaviour, 137,
1299–1315.
Cooper, W. E. (2003). Effect of risk on aspects of escape behavior by a lizard,
Holbrookia propinqua, in relation to optimal escape theory. Ethology, 109, 617–
626.
Cooper, W. E. (2006). Dynamic risk assessment: prey rapidly adjust flight initiation
distance to changes in predator approach speed. Ethology, 112, 858–864.
46
Cooper, W. E. (2009a). Fleeing and hiding under simultaneous risks and costs.
Behavioral Ecology, 20, 665–671.
Cooper, W. E. (2009b). Flight initiation distance decreases during social activity in
lizards (Sceloporus virgatus). Behavioral Ecology and Sociobiology, 63, 1765–
1771.
Cooper, W. E., & Wilson, D. S. (2007). Beyond optimal escape theory: microhabitats as
well as predation risk affect escape and refuge use by the phrynosomatid lizard
Sceloporus virgatus. Behaviour, 144, 1235–1254.
Cox, D. R. (1972). Regression Models and Life-Tables. Journal of the Royal Statistical
Society, 34, 187–220.
Crain, C. M., & Bertness, M. D. (2006). Ecosystem engineering across environmental
gradients: Implications for conservation and management. BioScience, 56, 211—
218.
Cully, Jr, J. F., , Collinge, S. K., VanNimwegen, R., Ray, C., Johnson, W. C.,
Thiagarajan, B., Conlin, D. B., & Holmes, B. E. (2010). Spatial variation in
keystone effects: Small mammal diversity associated with black-tailed prairie dog
colonies. Ecography, 33, 667–677.
Davidson, A. D., & Lightfoot, D. C. (2007). Interactive effects of keystone rodents on the
structure of desert grassland arthropod communities. Ecography, 30, 515–525.
Davidson, A. D. & Lightfoot, D. C. (2008). Burrowing rodents increase landscape
heterogeneity in a desert grassland. Journal of Arid Environments, 72, 1133–
1145.
Davidson, A. D., Detling, J. K., & Brown, J. H. (2012). Ecological roles and conservation
challenges of social, burrowing, herbivorous mammals in the world’s grasslands.
Frontiers in Ecology and the Environment, 10, 477–486.
Davis, J. R., & Theimer, T. C. (2003). Increased lesser earless lizard (Holbrookia
maculata) abundance on Gunnison’s prairie dog colonies and short term
responses to artificial prairie dog burrows. American Midland Naturalist, 150,
282–290.
Davis, J., & Verbeek, N. A. (1972). Habitat preferences and the distribution of Uta
stansburiana and Sceloporus occidentalis in coastal California. Copeia, 1972,
643—649.
47
Dayton, P. K. 1972. Toward an understanding of community resilience and the potential
effects of enrichment to the benthos of McMurdo Sound, Antarctica. Pp. 81–95 in
B. C. Parker (Ed.). Proceedings of the Colloquium on Conservation Problems in
Antarctica. Allen Press, Lawrence, KS
de Jong, A., Magnhagen, C., & Thulin, C. (2013). Variable flight initiation distance in
incubating Eurasian curlew. Behavioral Ecology and Sociobiology, 67, 1089–
1096.
Delibes-Mateos, M., Smith, A. T., Slobodchikoff, C. N., & Swenson, J. E. (2011). The
paradox of keystone species persecuted as pests: a call for the conservation of
abundant small mammals in their native range. Biological Conservation, 144,
1335–1346.
Derraik, J. G., Closs, G. P., Dickinson, K. J., Sirvid, P., Barratt, B. I., & Patrick, B. H.
(2002). Arthropod morphospecies versus taxonomic species: A case study with
Araneae, Coleoptera, and Lepidoptera. Conservation Biology, 16, 1015—1023.
Dhillion, S. S. (1999). Environmental heterogeneity, animal disturbances, microsite
characteristics, and seedling establishment in a Quercus havardii community.
Restoration Ecology, 7, 399–406.
Dickman, C. R. (1999). Rodent–ecosystem relationships: a review. Ecologically-based
Management of Rodent Pests. ACIAR Monograph, 59, 113–133.
Dickinson, H. C., and Fa, J. E. (2000). Abundance, demographics and body condition of
a translocated population of St Lucia whiptail lizards (Cnemidophorus vanzoi).
Journal of Zoology, London, 251, 187—197
Dill, L. M., & Houtman, R. (1989). The influence of distance to refuge on flight initiation
distance in the gray squirrel (Sciurus carolinensis). Canadian Journal of Zoology,
67, 233–235.
Dodd, C. K. and Seigel, R. A. (1991). Relocation, repatriation, and translocation of
amphibians and reptiles: Are they conservation strategies that work?
Herpetologica, 47, 336—350
Downes, S. (2001). Trading heat and food for safety: costs of predator avoidance in a
lizard. Ecology, 82, 2870–2881.
Dunn, C. P., Bowles, M. L., Rabb, G. B., and Jarantoski, K. S. (1997). Endangered
species “hot spots.” Science, 276, 513–515.
48
Ebrahimi, M., Fenner, A. L., & Bull, C. M. (2012). Lizard behaviour suggests a new
design for artificial burrows. Wildlife Research, 39, 295–300.
Eldridge, D. J., Koen, T. B., Killgore, A., Huang, N., & Whitford, W. G. (2012). Animal
foraging as a mechanism for sediment movement and soil nutrient development:
evidence from the semi-arid Australian woodlands and the Chihuahuan Desert.
Geomorphology, 157, 131—141.
Ellison, A. M., Bank, M. S., Clinton, B. D., Colburn, E. A., Elliot, K., Ford, C. R., Foster,
D. R., Kloeppel, B. D., Knoepp, J. D., Lovett, G. M., Mohan, J., Orwig, D. A.,
Rodenhouse, N. L., Sobczak, W. V., Stinson, K. A., Stone, J. K., Swan, C. M,
Thompson, J., Von Holle, B., & Webster, J. R. (2005). Loss of foundation
species: Consequences for the structure and dynamics of forested ecosystems.
Frontiers in Ecology and the Environment, 3, 479—486.
Erwin, D. H. (2008). Macroevolution of ecosystem engineering, niche construction and
diversity. Trends in Ecology & Evolution, 23, 304—310.
Fajardo, A., & McIntire, E. J. (2011). Under strong niche overlap conspecifics do not
compete but help each other to survive: facilitation at the intraspecific level.
Journal of Ecology, 99, 642—650.
Fleming, P., Anderson, H., Prendergast, A., Bretz, M., & Valentine, L. (2014). Is the loss
of Australian digging mammals contributing to a deterioration in ecosystem
function? Mammal Review, 44, 94–108.
Fraser, C. M. L., Coleman, R. A., & Seebacher, F. (2014). Trying to fit in: are patterns of
orientation of a keystone grazer set by behavioural responses to ecosystem
engineers or wave action? Oecologia, 174, 67—75.
Gabet, E. J., Reichman, O. J., & Seabloom, E. W. (2003). The effects of bioturbation on
soil processes and sediment transport. Annual Review of Earth and Planetary
Sciences, 31, 249–273.
Gálvez Bravo, L., Belliure, J., & Rebollo, S. (2009). European rabbits as ecosystem
engineers: warrens increase lizard density and diversity. Biodiversity and
Conservation, 18, 869–885.
Germano, D. J., Rathbun, G. B., & Saslaw, L. R. (2001). Managing exotic grasses and
conserving declining species. Wildlife Society Bulletin, 29, 551–559.
Gribben, P. E., & Wright, J. T. (2014). Habitat-former effects on prey behaviour increase
predation and non-predation mortality. Journal of Animal Ecology, 83, 388–396.
49
Grillet, P., Cheylan, M., Thirion, J., Dore, F., & Bonnet, X. (2010). Rabbit burrows or
artificial refuges are a critical habitat component for the threatened lizard, Timon
lepidus (sauria, lacertidae). Biodiversity and Conservation, 19, 2039–2051.
Gross, K. (2008). Positive interactions among competitors can produce species-rich
communities. Ecology Letters, 11, 929—936.
Goldingay, R. L., Kelly, P. A., & Williams, D. F. (1997). The kangaroo rats of
California: Endemism and conservation of keystone species. Pacific Conservation
Biology, 3, 47–59.
Hart, S. P., & Marshall, D. J. (2013). Environmental stress, facilitation, competition, and
coexistence. Ecology, 94, 2719–2731.
Hastings A., Byers J. E., Crooks J. A., Cuddington, K., Jones, C. G., Lambrinos, J. G.,
Talley, T. S. & Wilson, W. G. (2007) Ecosystem engineering in space and time.
Ecology Letters, 10, 153—164.
Hawkins, L. K., & Nicoletto, P. F. (1992). Kangaroo rat burrows structure the spatial
organization of ground-dwelling animals in a semiarid grassland. Journal of Arid
Environments, 23, 199—208.
Heath, J. E. (1970). Behavioral regulation of body temperature in poikilotherms.
Physiologist, 13, 399–410.
Hein, E. W., and Whitaker, S. J. (1997). Homing in eastern fence lizards (Sceloporus
undulatus) following short distance translocation. Great Basin Naturalist, 57,
348—351
Huang, W., Lin, S., Dubey, S., & Pike, D. A. (2013). Predation drives interpopulation
differences in parental care expression. Journal of Animal Ecology, 82, 429—437
Iraeta, P., Monasterio, C., Salvador, A., and Diaz, J.A. (2006). Mediterranean hatchling
lizards grow faster at higher altitude: A reciprocal transplant experiment.
Functional Ecology, 20, 865—872.
James, A. I., Eldridge, D. J., Koen T. B., & Moseby, K. E. (2011) Can an invasive
European rabbit (Oryctolagus cuniculus) assume the soil engineering role of
locally-extinct natives? Biological Invasions, 13, 3027–3038.
Johnson, D. W. (2006). Predation, habitat complexity, and variation in density-dependent
mortality of temperate reef fishes. Ecology, 87, 1179–1188.
50
Jones, C. G., Lawton, J. H., & Shachak, M. (1994). Organisms as ecosystem engineers.
Oikos, 69, 373—386.
Jones, C. G., Lawton, J. H., & Shachak, M. (1997). Positive and negative effects of
organisms as physical ecosystem engineers. Ecology, 78, 1946—1957.
Kay, F. R., & Whitford, W. G. (1978). The burrow environment of the banner-tailed
kangaroo rat, Dipodomys spectabilis, in southcentral New Mexico. American
Midland Naturalist, 99, 270–279.
Kearney, M., Shine, R. & Porter, W. P. (2009). The potential for behavioral
thermoregulation to buffer ‘coldblooded’ animals against climate warming.
Proceedings of the National Academy of Sciences, USA, 106, 3835–3840.
Koontz, T. L., Shepherd, U. L., & Marshall, D. (2001). The effect of climate change on
Merriam’s kangaroo rat, Dipodomys merriami. Journal of Arid Environments, 49,
581–591.
Kurek, P., Kapusta, P., & Holeksa, J. (2014). Burrowing by badgers (Meles meles) and
foxes (Vulpes vulpes) changes soil conditions and vegetation in a European
temperate forest. Ecological Research, 29, 1–11.
Kretzer, J. E., & Cully Jr, J. F. (2001). Effects of black-tailed prairie dogs on reptiles and
amphibians in Kansas shortgrass prairie. The Southwestern Naturalist, 46, 171—
177.
Křivan, V., & Schmitz, O. J. (2004). Trait and density mediated interactions in simple
food webs. Oikos, 107, 239—250.
Krueger, K. (1986). Feeding relationships among bison, pronghorn, and prairie dogs: an
experimental analysis. Ecology, 67,760–770.
Lagos, P. A., Meier, A., Tolhuysen, L. O., Castro, R. A., Bozinovic, F., & Ebensperger,
L. A. (2009). Flight initiation distance is differentially sensitive to the costs of
staying and leaving food patches in a small-mammal prey. Canadian Journal of
Zoology, 87, 1016–1023.
Lane, D. M., & Sándor, A. (2009). Designing better graphs by including distributional
information and integrating words, numbers, and images. Psychological methods,
14, 239—257.
Larkin, D., Vivian-Smith, G., & Zedler, J. B. (2006). Topographic heterogeneity theory
and ecological restoration. pp. 142–164 in Larkin, D., Palmer, M., & Zedler, J. B.
(Eds.). Foundations of Restoration Ecology. Island Press, Washington, DC
51
Lomolino, M. V., & Smith, G. A. (2006). Terrestrial vertebrate communities at blacktailed prairie dog (Cynomys ludovicianus) towns. Biological Conservation, 115,
89—100.
Machicote, M., Branch, L. C., & Villarreal, D. (2004). Burrowing owls and burrowing
mammals: are ecosystem engineers interchangeable as facilitators? Oikos, 106,
527–535.
Maestre, F. T., Callaway, R. M., Valladares, F., & Lortie, C. J. (2009). Refining the
stress-gradient hypothesis for competition and facilitation in plant communities.
Journal of Ecology, 97, 199—205.
Marco, A., Díaz-Paniagua, C., & Hidalgo-Vila, J. (2004). Influence of egg aggregation
and soil moisture on incubation of flexible-shelled lacertid lizard eggs. Canadian
Journal of Zoology, 82, 60—65.
Martín, J., & López, P. (1995). Influence of habitat structure on the escape tactics of the
lizard Psammodromus algirus. Canadian Journal of Zoology, 73, 129–132.
Martín, J., & López, P. (2000). Fleeing to unsafe refuges: effects of conspicuousness and
refuge safety on the escape decisions of the lizard Psammodromus algirus.
Canadian Journal of Zoology, 78, 265–270.
Martinsen, G. D., Floate, K. D., Waltz, A. M., Wimp, G. M., & Whitham, T. G. (2000).
Positive interactions between leafrollers and other arthropods enhance
biodiversity on hybrid cottonwoods. Oecologia, 123, 82–89.
McIntire, E. J., & Fajardo, A. (2011). Facilitation within species: a possible origin of
group-selected superorganisms. The American Naturalist, 178, 88—97.
McCoy, M. W., & Bolker, B. M. (2008). Trait-mediated interactions: Influence of prey
size, density and experience. Journal of Animal Ecology, 77, 478—486.
Meadows, P. S. (1991). The environmental impact of burrowing animals and animal
burrows – conclusions and a model. Symposium of the Zoological Society of
London, 63, 37—338.
Meysman, F. J., Middelburg, J. J., & Heip, C. H. (2006). Bioturbation: a fresh look at
Darwin's last idea. Trends in Ecology & Evolution, 21, 688—695.
Milcu, A., Schumacher, J., & Scheu, S. (2006). Earthworms (Lumbricus terrestris) affect
plant seedling recruitment and microhabitat heterogeneity. Functional Ecology,
20, 361—268.
52
Milne, T., & Bull, C. M. (2000). Burrow choice by individuals of different sizes in the
endangered pygmy blue tongue lizard Tiliqua adelaidensis. Biological
Conservation, 95, 295—301.
Moritz, C., Patton, J. L., Conroy, C. J., Parra, J.L., White, G. C., & Beissinger, S. R.
(2008). Impact of a century of climate change on small-mammal communities in
Yosemite National Park, USA. Science, 322, 261–264.
Nagy, K. A. (1988) Seasonal patterns of water and energy balance in desert vertebrates.
Journal of Arid Environments, 14, 201–210.
Niewiarowski, P., and Roosenburg, W. (1993). Reciprocal transplant reveals sources of
variation in growth rates of the lizard Sceloporus undulates. Ecology, 74, 1992—
2002.
Noble, J. C., Muller, W. J., Detling, J. K., & Pfitzner, G. H. (2007). Landscape ecology of
the burrowing bettong: warren distribution and patch dynamics in semiarid
eastern Australia. Austral Ecology, 32, 326–337.
Orrock, J., Preisser, E., Grabowski, J., & Trussell, G. (2013). The cost of safety: refuges
increase the impact of predation risk in aquatic systems. Ecology, 94, 573–579.
Parker, W. S., & Pianka, E. R. (1975). Comparative ecology of populations of the lizard
Uta stansburiana. Copeia, 1975, 615–632.
Paterson, R. A., Pritchard, D. W., Dick, J. T. A., Alexander, M. E., Hatcher, M. J., &
Dunn, A. M. (2013). Predator cue studies reveal strong trait-mediated effects in
communities despite variation in experimental designs. Animal Behaviour, 86,
1301—1313.
Pearce, T. (2011). Ecosystem engineering, experiment, and evolution. Biology &
Philosophy, 26, 793–812.
Peacor, S. D., & Werner, E. E. (2001). The contribution of trait-mediated indirect effects
to the net effects of a predator. Proceedings of the National Academy of Sciences,
98, 3904—3908.
Pearson, D. E. (2010). Trait- and density-mediated indirect interactions initiated by an
exotic invasive plant autogenic ecosystem engineer. American Naturalist, 176,
394–403.
Pintor, L. M. & Soluk, D. A. (2006). Evaluating the nonconsumptive, positive effects of a
predator in the persistence of an endangered species. Biological Conservation,
130, 584–591.
53
Preisser, E. L., Bolnick, D. I., & Benard, M. E. (2005). Scared to death? The effects of
intimidation and consumption in predator-prey interactions. Ecology, 86, 501—
509.
Pringle, R. M. (2008). Elephants as agents of habitat creation for small vertebrates at the
patch scale. Ecology, 89, 26–33.
Prugh, L. R. & Brashares, J. S. (2012). Partitioning the effects of an ecosystem engineer:
kangaroo rats control community structure via multiple pathways. Journal of
Animal Ecology, 81, 667–678.
Quinn, G. P., & Keough, M. J. (2002). Experimental design and data analysis for
biologists. Cambridge University Press, New York, N.Y.
Read, J. L., Carter, J., Moseby, K. M. & Greenville, A. (2008). Ecological roles of rabbit,
bettong and bilby warrens in arid Australia. Journal of Arid Environments, 72,
2124–2130.
Reichman, O. J., & Seabloom, E. W. (2002). The role of pocket gophers as subterranean
ecosystem engineers. Trends in Ecology & Evolution, 17, 44—49.
Rosier, J. R., Ronan, N. A., & Rosenberg, D. K. (2006). Post-breeding dispersal of
burrowing owls in an extensive California grassland. The American Midland
Naturalist, 155, 162-167.
Roznik, E. A., & Johnson, S. A. (2009). Burrow use and survival of newly
metamorphosed gopher frogs (Rana capito). Journal of Herpetology, 43, 431–
437.
Sanders, D., Jones, C. G., Thébault, E., Bouma, T. J., van der Heide, T., van Belzen, J., &
Barot, S. (2014). Integrating ecosystem engineering and food webs. Oikos, 123,
513–524.
Schall, J. J. & Pianka, E. R. (1980). Evolution of escape behavior diversity. American
Naturalist, 115,551–566.
Scheffers, B. R., Edwards, D. P., Diesmos, A., Williams, S. E., & Evans, T. A. (2014).
Microhabitats reduce animal’s exposure to climate extremes. Global Change
Biology, 20, 495–503.
Schiffman, P. M. (1994). Promotion of exotic weed establishment by endangered giant
kangaroo rats (Dipodomys ingens) in a California grassland. Biodiversity and
Conservation, 3, 524–537.
54
Schiffman, P. M. 2007a. Ecology of native animals in California Grasslands. pp. 180-190
in M. R. Stromberg, J. D. Corbin, C. M. D’Antonio (eds). California Grasslands:
Ecology and Management. University of California Press, Berkeley
Schiffman, P. M. 2007b. Species composition at the time of first settlement. Pp. 52-56 in
M. R. Stromberg, J. D. Corbin, C. M. D’Antonio (eds). California Grasslands:
Ecology and Management. University of California Press, Berkeley
Scyphers S. B., & Powers, S. P. (2013). Context-dependent effects of a marine ecosystem
engineer on predator-prey interactions. Marine Ecology Progress Series, 491,
295–301.
Shipley, B. K., & Reading, R. P. (2006). A comparison of herpetofauna and small
mammal diversity on black-tailed prairie dog (Cynomys ludovicianus) colonies
and non-colonized grasslands in Colorado. Journal of Arid Environments, 66,
27—41.
Shumway, S. W., & Bertness, M. D. (1994). Patch size effects on marsh plant secondary
succession mechanisms. Ecology, 75, 564–568.
Simon, C. A., & Bissinger, B. E. (1983). Paint marking lizards: does the color affect
survivorship? Journal of Herpetology, 17, 184–186.
Sinervo, B., Méndez de la Cruz, F. F., Miles, D. B., Heulin, B., Bastiaans, E., VillagránSanta Cruz, M., Lara-Resendiz, R., Martínez-Méndez, N., Calderón-Espinosa, M.
L., Meza-Lázaro, R. N., Gadsden, H., Avila, L. J., Morando, M., De la Riva, I. J.,
Victoriano Sepulveda, P., Rocha, C. F. D., Ibargüengoytía, N., Aguilar Puntriano,
C., Massot, M., Lepetz, V., Oksanen, T. A., Chapple, D. G., Bauer, A. M.,
Branch, W. R., Clobert, J. & Sites, J.W., Jr. (2010). Erosion of lizard diversity by
climate change and altered thermal niches. Science, 328, 894–899.
Smith, A. T., & Foggin, J. M. (2006). The plateau pika (Ochotona curzoniae) is a
keystone species for biodiversity on the Tibetan plateau. Animal Conservation, 2,
235–240.
Smith, G. R., & Ballinger, R. E. (2001). The ecological consequences of habitat and
microhabitat use in lizards: a review. Contemporary Herpetology, 3, 1–37.
Smyth, M., & Coulombe, H. N. (1971). Notes on the use of desert springs by birds in
California. Condor, 73, 240—243.
Souter, N. J., Bull, C. M., & Hutchinson, M. N. (2004). Adding burrows to enhance a
population of the endangered pygmy blue tongue lizard, Tiliqua adelaidensis.
Biological Conservation, 116, 403–408.
55
Stachowicz, J. J. (2001). Mutualism, Facilitation, and the Structure of Ecological
Communities Positive interactions play a critical, but underappreciated, role in
ecological communities by reducing physical or biotic stresses in existing habitats
and by creating new habitats on which many species depend. Bioscience, 51,
235—246.
State of California. (2012). California Drought. Retrieved 5 July 2014 from
http://www.ca.gov/drought/
Tewksbury, J. J., & Lloyd, J. D. (2001). Positive interactions under nurse-plants: spatial
scale, stress gradients and benefactor size. Oecologia, 127, 425–434.
Tews, J., Brose, U., Grimm, V., Tielbörger, K., Wichmann, M. C., Schwager, M., &
Jeltsch, F. (2004). Animal species diversity driven by habitat
heterogeneity/diversity: the importance of keystone structures. Journal of
Biogeography, 31, 79–92.
Thébault, E., & Fontaine, C. (2010). Stability of ecological communities and the
architecture of mutualistic and trophic networks. Science, 329, 853—856.
Tinkle, D. W., McGregor, D., & Dana, S. (1962). Home Range Ecology of Uta
stansburiana stejnegeri. Ecology, 43, 223—229.
Verdú, M., & Valiente‐Banuet, A. (2008). The Nested assembly of plant facilitation
networks prevents species extinctions. The American Naturalist, 172, 751—760.
Vitt, L. J., Colli, G. R., Caldwell, J. P., Mesquita, D. O., Garda, A. A., & FranÇa, F. G. R.
(2007). Detecting variation in microhabitat use in low-diversity lizard
assemblages across small-scale habitat gradients. Journal of Herpetology, 41,
654—663.
Villarreal, D., Clark, K. L., Branch, L. C., Hierro, J. L., & Machicote, M. (2008).
Alteration of ecosystem structure by a burrowing herbivore, the plains vizcacha
(Lagostomus maximus). Journal of Mammalogy, 89, 700–711.
Walde, A. D., Walde, A. M., Delaney, D. K. & Pater, L. L. (2009). Burrows of desert
tortoises (Gopherus agassizii) as thermal refugia for horned larks (Eremophila
alpestris) in the Mojave Desert. Southwestern Naturalist, 54, 375–381.
Waldschmidt, S. (1983). The effect of supplemental feeding on home range size and
activity patterns in the lizard Uta stansburiana. Oecologia, 57, 1–5.
56
Waldschmidt, S. R., & Porter, W. P. (1987). A model and experimental test of the effect
of body temperature and wind speed on ocular water loss in the lizard Uta
stansburiana. Physiological zoology, 60, 678—686.
Waldschmidt, S., & Tracy, C. R. (1983). Interactions between a lizard and its thermal
environment: implications for sprint performance and space utilization in the
lizard Uta stansburiana. Ecology, 64, 476–484.
Warner, D. A., & Andrews, R. M. (2009). Nest-site selection in relation to temperature
and moisture by the lizard Sceloporus undulatus. Herpetologica, 58, 399—407.
Werner, E. E., & Peacor, S. D. (2003). A Review of trait-mediated indirect interactions in
ecological communities. Ecology, 84, 1083—1100.
Wesche, K., Nadrowski, K., & Retzer, V. (2007). Habitat engineering under dry
conditions: the impact of pikas (Ochotona pallasi) on vegetation and site
conditions in southern Mongolian steppes. Journal of Vegetation Science, 18,
665–674.
Whicker, A. D. & Detling, J. K. (1988). Ecological consequences of prairie dog
disturbances. Bioscience, 38, 778–785.
Whitford, W. G. & Kay, F. R. 1999. Biopedturbation by mammals in deserts: a review.
Journal of Arid Environments, 41, 203–230.
Whittington-Jones, G. M., Bernard, R. T. F., & Parker, D. M. (2011). Aardvark burrows:
a potential resource for animals in arid and semi-arid environments. African
Zoology, 46, 362–370.
Wright, J. P., & Jones, C. G. (2006). The concept of organisms as ecosystem engineers
ten years on: progress, limitations, and challenges. BioScience, 56, 203—209.
Wright, J. P., Jones, C. G., & Flecker, A. S. (2002). An ecosystem engineer, the beaver,
increases species richness at the landscape scale. Oecologia, 132, 96–101.
Wu, J., & Loucks, O. L. (1995). From balance of nature to hierarchical patch dynamics: a
paradigm shift in ecology. Quarterly Review of Biology, 70,439–466.
Zhang, Y., Zhang, Z., & Liu, J. (2003). Burrowing rodents as ecosystem engineers: the
ecology and management of plateau zokors Myospalax fontanierii in alpine
meadow ecosystems on the Tibetan Plateau. Mammal Review, 33, 284–294.
57