FORAGING BEHAVIOR IN GAMBELIA WISLIZENII ...

FORAGING BEHAVIOR IN GAMBELIA WISLIZENII, THE LONG-NOSED LEOPARD LIZARD, IN HARNEY COUNTY, OREGON BY ELEANOR LOUISA ROSE

Accepted in Partial Completion of the Requirements for the Degree Master of Science

_____________________________________ Moheb A. Ghali, Dean of the Graduate School

ADVISORY COMMITTEE ___________________________ Chair, Dr. Roger A. Anderson ___________________________ Dr. David Hooper ___________________________ Dr. Alejandro Acevedo-Gutiérrez

MASTER’S THESIS In presenting this thesis in partial fulfillment of the requirements for a master’s degree at Western Washington University, I agree that the Library shall make its copies freely available for inspection. I further agree that copying of this thesis in whole or in part is allowable only for scholarly purposes. It is understood, however, that any copying or publication of this thesis for commercial purposes, or for financial gain, shall not be allowed without my written permission. Signature ____________________ Date ________________________

FORAGING BEHAVIOR IN GAMBELIA WISLIZENII, THE LONG-NOSED LEOPARD LIZARD, IN HARNEY COUNTY, OREGON

A Thesis Presented to the Faculty of Western Washington University

In Partial Fulfillments of the Requirements for the Degree Master of Science

by Eleanor L. Rose March 2003

FORAGING BEHAVIOR IN GAMBELIA WISLIZENII, THE LONG-NOSED LEOPARD LIZARD, IN HARNEY COUNTY, OREGON ABSTRACT Every animal has 4 basic tasks: acquire food, acquire mates, avoid predation and avoid environmental extremes. Of these, acquiring food usually assumes prime importance. Although there is a variety of foraging behavior in lizards, two contrasting food-acquisition modes (FAM) are recognized into which most lizards can be divided. These two modes are “ambushing” and “intensively foraging.” The focus on categorizing each species as a particular type of forager has caused intraspecific variation in FAM to be largely ignored, yet this area of study may provide the most convincing evidence for the specific links between FAM and ecological factors. Members of the lizard family Crotaphytidae are typically ambush predators of arthropods, except for Gambelia wislizenii, which eats lizards and has unique morphology and behavior for its family. There is a latitudinal cline in prey types consumed by G. wislizenii; southern populations rely on lizard prey and northern populations rely more on arthropods. This study aimed to characterize foraging behavior of G. wislizenii in a northern population and determine whether changes in prey type and availability, associated with time of day and time during the activity season, caused changes in foraging behavior and microhabitat selection. The constraints of environmental temperatures, body size and social structure on foraging behavior were also examined. Predation risk was believed to be slight and individuals were post-reproductive, minimizing the influence of 2 of the 4 basic tasks. Foraging behavior of G. wislizenii was recorded during 57, thirty-minute long focal observations, in late June/early July and early August. Notable variables included: MPM (number of movements per minute), PTM (percent time spent moving), aspects of the microhabitat, and types of prey pursued. Standardized searches of a 2.89 ha plot were used to calculate hourly changes in the abundance of G. wislizenii and home range use. Grasshopper and prey lizard availability in different mesohabitats were also measured by standardized visual searches. Laboratory prey choice trials investigated which visual cues most strongly stimulated G. wislizenii to attack prey. G. wislizenii exhibited foraging behavior best characterized as a brief-wait ambush predation. Low PTM values were characteristic of ambushers, but the high MPM values were characteristic of intensive foragers. Pauses were necessary to visually detect slight movements of their principal prey, cryptically colored grasshoppers. Grasshopper availability diminished between July and August but did not vary significantly throughout the day. Foraging behavior differed between sexes in July but not in August. In July, females paused longer between movements than males in the morning, perhaps increasing successful ambushes of whiptail lizards, which are most available early in the day. Females may have switched foraging behavior in response to adult lizard availability because, unlike the smaller males, they were able to capture adult lizards or because they needed to replace nutrients used in egg production. The similarity between G. wislizenii foraging behavior of males in July and both sexes in August suggests the same search behavior was used for hatchling lizards (found only in August) and grasshoppers. Movements of G. wislizenii related to patrolling territories, seeking mates and avoiding predation were minimized by researcher choice of lizard, time period and study site. Thus, the subtle effects of prey availability on foraging behavior were discernable, and the effect of high temperatures at midday, resulting in a generally bimodal pattern of activity throughout the day, was obvious. G. wislizenii moved infrequently during the heat of the day, and caught fewer prey, but did not retreat to burrows; they moved to the shade of shrubs and became extended-wait ambushers. Verification of the effect of arthropod and lizard abundance on foraging behavior could be achieved by detailed studies of foraging behavior in G. wislizenii across its geographical range. Investigation of the proximate factors affecting foraging behavior in northern and southern populations could lead not only to a better understanding of foraging behavior in lizards, but could also reveal the factors that cause an evolutionary shift in the food-acquisition mode of a population or species.

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ACKNOWLEDGEMENTS

I am grateful to the students in the reptile ecology field course of 2003 for their assistance in the field and help in data organization. In particular, I would like to thank Ellen Ward, Heather Pedersen, Brian Levenhagen, Erin Wigge, Jesse Johnson, Caitlin Miller, Maia Schramm, Jim Howard, Alex McHuron, Dave Ramseyer, Jud Hall and Val Ledesma. My advisor, Roger Anderson, and thesis committee members, David Hooper, Alejandro Acevedo-Gutiérrez, Merrill Peterson and David Schneider provided valuable input at various stages of my thesis and I am grateful for their help. Western Washington University Graduate School and the Bureau for Faculty Research supported this work through the Fund for the Enhancement of Graduate Research.

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LIST OF FIGURES

Figure 1

Geographic distribution of Gambelia wislizenii ............................................ 11

Figure 2

Hourly changes in air and sand temperatures during June and July 2003 ..... 27

Figure 3

Mass and snout-vent length for male and female G. wislizenii ..................... 34

Figure 4a

MPM and number of prey pursued by G. wislizenii per hour ........................ 39

Figure 4b

PTM and number of prey pursued by G. wislizenii per hour ......................... 39

Figure 5a

MPM and time of day .................................................................................... 41

Figure 5b

PTM and time of day ..................................................................................... 41

Figure 6a

MPM and air temperature .............................................................................. 42

Figure 6b

PTM and air temperature ............................................................................... 42

Figure 7a

MPM and time spent in the open ................................................................... 44

Figure 7b

PTM and time spent in the open .................................................................... 44

Figure 8a

Position relative to shrub base of G. wislizenii during long pauses ............... 46

Figure 8b

Direction G. wislizenii faced relative to shrub base during long pauses ....... 46

Figure 9

Prey types consumed by female G. wislizenii in July in each 2-hour period . 48

Figure 10

Prey types consumed by male G. wislizenii in July in each 2-hour period .... 49

Figure 11

Prey types consumed by all G. wislizenii in August in each 2-hour period ... 50

Figure 12a

Grasshopper abundance in 3 mesohabitats in each 2-hour period in July ..... 55

Figure 12b

Grasshopper abundance in sandy flats in each 2-hour period in August ....... 55

Figure 13

Percentage of nymphs in grasshopper population in early July ..................... 57

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Figure 14

G. wislizenii and A. tigris abundance in each 2-hour period in July .............. 59

Figure 15

G. wislizenii and A. tigris abundance in each 2-hour period in August ......... 60

Figure 16

Cumulative number of G. wislizenii seen on study plot in July ..................... 61

Figure 17

Iterative calculations of home range size for three G. wislizenii ................... 63

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LIST OF TABLES

Table 1

Correlates of food-acquisition mode in ambushers and intensive foragers ..... 4

Table 2a

Foraging variables differing significantly between July males, July females and both sexes in August ............................................................................... 37

Table 2b

Mann-Whitney U values for pair-wise comparisons between certain foraging variables of July males, July females and August lizards .............................. 37

Table 3

Means of body temperature and principal measures of foraging behavior for July males, July females and August lizards ................................................. 38

Table 4

Prey types pursued by males and females, and in July and August; capture success for each prey type, and svl of lizard pursuing prey ........................... 51

Table 5

Behavioral tactics used by G. wislizenii to pursue different prey types ........ 53

Table 6

Comparisons between mesohabitats for plant and grasshopper abundance and proportion of G. wislizenii and A. tigris seen during searches ....................... 54

Table 7

Differences between the cricket pursued-and-caught and the cricket not pursued in prey choice trials .......................................................................... 65

Table 8

Comparison of MPM and PTM among ambushers, intensive foragers and Gambelia wislizenii ........................................................................................ 86

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TABLE OF CONTENTS

Abstract

iv

Acknowledgements

v

List of Figures

vi

List of Tables

viii

Introduction

1

Methods

10

Results

33

Discussion

66

Literature cited

89

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INTRODUCTION

Overview The current focus of studies of foraging behavior, particularly in lizards, appears to be on characterizing the foraging mode of several species and making comparisons and correlations among species (e.g. Cooper, 1995; Perry and Pianka, 1997; Perry, 1999; Cooper et al., 2001). While the choice of foraging variables and the influence of phylogeny on foraging mode has been discussed at length, intraspecific variation in food-acquisition mode has been largely ignored. Without a thorough understanding of the variability of foraging behavior within a species, along with the ecological conditions associated with that variability, comparisons of foraging behavior between species are problematic. The prey items in the diet of the lizard Gambelia wislizenii vary greatly among populations and between times of the activity season (Tanner and Krogh, 1974; Parker and Pianka, 1976). It is expected that the foraging behavior of G. wislizenii would be similarly variable. Although no detailed analysis of G. wislizenii foraging behavior has been attempted, anecdotal evidence suggests G. wislizenii forages in a different manner to all other species in the family Crotaphytidae, and, in fact, most other species of lizards (Montanucci, 1978; Tollestrup, 1979). This study sets out to examine the variation in foraging behavior between sexes of G. wislizenii, throughout the day and over the warmer half of the activity season, in southeast Oregon. Prey availability, environmental temperatures, habitat structure, and sizes and overlap of home ranges were also measured to investigate some of the influences and constraints on foraging behavior.

Food-Acquisition Mode An animal faces four basic ecological tasks. It must avoid and evade predators, cope with environmental stresses, find mates and reproduce, and acquire food (Anderson, 1993). When, where and how a particular task is performed, and the time and energy expended on that task, may constrain performance of the other tasks. Of the four basic autecological tasks, obtaining food usually assumes prime importance, having the greatest ecological and evolutionary influence on the behavior, physiology and morphology of the animal (Eckhardt, 1979; Anderson, 1993; Rose and Lauder, 1996). From an evolutionary standpoint, net rates of energy intake can determine an individual’s scope for future activity, growth and reproduction, aspects of fitness on which natural selection acts (Hughes, 1993). Because food is often considered the most important resource to an animal, the principal adaptive syndrome in animals is that associated with acquiring food. An adaptive syndrome is a coordinated set of adaptations related to the manner in which resources are used (Eckhardt, 1979). The food-acquisition mode is an adaptive syndrome that may be defined as a coordinated set of physiological, behavioral, and morphological characteristics that are integrally involved in the search, detection, capture, and eating of food (Anderson and Karasov, 1988). Some of the primary behavioral features of food-acquisition mode that can be compared among animals are: 1) the movement patterns while searching for food, 2) the methods and modalities used for food detection, 3) the means of capturing prey. Studies of food-acquisition mode are therefore more concerned with ultimate causal factors, that is, those factors that may have caused the evolution and maintenance of such behavioral features, rather than those that determine the short-term variation in behavioral phenotypes. 2

The dichotomy of foraging modes In 1966, Pianka posited a bimodal pattern of foraging behavior of predators, based on observations of North American lizards. These two foraging “modes” were defined as “ambushing” and “widely-foraging.” Numerous papers have expounded on Pianka’s (1966) thoughts on the dichotomy of foraging modes, investigating the different behavioral methods to search for different prey in birds, fish, amphibians and reptiles (respective order: Thiollay, 1988; Crowder, 1985; Toft, 1980; Pietruszka, 1986). Several models have been put forth to explain the dichotomy. For example, Speakman (1986) theorized that effective predators should be either sedentary or moving at their maximum search speed. Archetypal wide foragers, such as lizards in the genus A. tigris, do not usually move at their maximum aerobic speed most of foraging time, however (Anderson, 1993; Garland, 1993), and the proximate factors that limit search speed are poorly understood. Another explanation for the dichotomy in foraging modes of predators is a bimodality in the behavior of prey species. Ambushing lizards rely on vision to detect prey, and they efficiently capture active prey, typically adult insects such as grasshoppers and beetles. In contrast, widely foraging lizards detect prey by chemoreception and vision, and are best suited to detect and catch sedentary or hidden prey, often immature insects such as lepidopteran larvae (Gerritsen and Strickler, 1977; Anderson and Karasov, 1981). Wide foragers are therefore commonly referred to as intensive foragers to distinguish them from the ambushers by more than movement patterns alone (Regal, 1978; Anderson, 1993). The bimodality in prey behavior and the methods and modalities needed to capture them are now commonly accepted, at least for insectivorous lizards (e.g. Perry and Pianka, 1997), hence use of the more inclusive term “food-acquisition mode” rather than “foraging mode” which 3

focuses on movement only (Anderson, 1993). Cooper (1994, 1995) has demonstrated the strong phylogenetic connection between sensory abilities and foraging mode. The few apparent changes in foraging mode within taxa have coincided with a change from more chemosensory to more visual detection. Senses and foraging mode may be related because a predator has difficulty moving and visually detecting prey at the same time (Sonerud, 1992; Avery, 1993), but the predator’s hearing and chemoreception are relatively unaffected as it moves (Kramer and McLaughlin, 2001). In addition to the aforementioned differences between ambushing and intensive foraging predators, other traits have apparently co-evolved and also contribute to the dichotomy of the two food-acquisition modes (Table 1). Of those listed in Table 1, two measurement variables, number of moves per minute (MPM) and proportion of time spent moving (PTM) have become the standard, expedient method for evaluating whether a lizard is an intensive forager or ambusher (Cooper et al., 2001). There are no quantitative definitions of ambushing versus intensive foraging (McLaughlin, 1989), though Perry (1995) suggested the use of PTM < 10 to indicate ambush predation mode. Authors have typically compared movement patterns among lizards sharing the same habitat and geographic location to define the food-acquisition mode under which each species falls (e.g. Huey and Pianka, 1981), thereby defining ambushers or wide foragers in relative, rather than absolute, values of MPM and PTM. For example, Gekkonidae has variously been referred to as a family of wide foragers, ambushers and intermediate foragers (Werner et al. 1997). Measuring rates of movement have the additional complication of determining whether movements relate to foraging, social interactions or thermoregulation.

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Table 1. Comparison of the correlates of food-acquisition mode for ambushing and intensive foraging lizards. Trait

Ambusher

Intensive Forager

References

Prey types

Mobile, large (especially adult insects)

Hidden,sedentary (e.g. termites, larvae, inactive scorpions)

Huey & Pianka, 1981; Nagy et al., 1984; Magnusson et al. 1985

Sensory mode for prey detection

Primarily vision

Vision and chemoreception

Cooper, 1994, 1995

Prey mass consumed/day

Low

High

Anderson & Karasov, 1981

Daily metabolic rate

Low

High

Anderson & Karasov, 1981

Number of movements per minute (MPM)

Low

High

Perry et al., 1995; Cooper et al., 2001

Percent time spent Low moving (PTM)

High

Perry et al., 1995; Cooper et al., 2001

Thermoregulatory Use variety of postures and behavior microhabitats to extend daily activity

Limit daily period of activity

Bowker, 1984

Anti-predator behavior

Avoidance via cryptic behavior

Evasion via speed

Huey & Pianka, 1981; Vitt, 1983

Physiological correlates

Limited endurance; fast, short chases

High endurance; efficient locomotion

Ruben, 1976; Huey et al., 1984; Bauwens et al., 1995

Morphotype

Stocky body; wide mouth

Gracile body; narrow mouth

Vitt & Congdon, 1978; Moermond, 1979; Losos, 1990

Relative clutch mass

High

Low

Anderson & Karasov, 1981, 1988; Vitt & Price, 1982

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The methods used in calculating MPM and PTM can also cause wide variation in the resulting values. Of particular concern are those determined from small sample sizes and short (often less than ten minutes) observation times (e.g. Perry et al., 1990; Cooper et al., 1997) especially when no evidence is given that lizards were not engaged in activities other than foraging. Another complication of studies on foraging mode can be observer effect (Schoener, 1971; Lehner, 1996), especially shortly after encounter with the lizard. In this respect, Gambelia wislizenii is particularly amenable to study, showing little concern for human disturbance. This unwariness was commented on by McCoy (1967), and by Tanner and Krogh (1974) who found them easier to noose than any other fast-running lizard. Even within a species, foraging behavior may not be fixed. Anecdotal short-term variation in foraging mode has been reported in Gambelia silus, which ambushed insects from prominent positions when prey density was low, but foraged more actively in flower patches where insect abundance appeared to be greater (Tollestrup, 1979). Some species of frogs were found to actively forage for ants when arthropods were abundant and became more generalist ambushers when they were scarce (Toft, 1980). Despite the theoretical advantages of shifts in foraging behavior, various physiological limitations, such as low endurance capacity or poor chemoreception may make such shifts uncommon. The convenient concept of two discrete foraging modes has been modified several times since its introduction. In 1978, Regal proposed a system involving three foraging modes: ambush, cruising, and intensive foragers, with cruising foragers employing a movestop-scan-move movement pattern, and intensive foragers investing more effort in searching for concealed prey. He admitted that even this is “still probably inadequate.” Other authors suggest a continuum of foraging behavior (e.g. Pianka, 1973; Regal, 1983; Magnusson et al., 6

1985; Perry et al., 1990), and the fact that ambushers and intensive foragers represent the extremes of a spectrum that may include many types of foragers is widely recognized. A tendency to compare a limited number of distantly related species might have overemphasized the dichotomous pattern of foraging behavior (Perry, 1999) because foraging appears to be relatively fixed within most taxonomic families. More scientific value may be gained from studies investigating differences in foraging behavior on a small (intrafamily) level, where the ecological reasons for such differences may be more easily discovered (Huey et al., 1984). Superficial attempts at classifying foraging mode for a number of species allow no room for variation and adaptability within a species; adaptability can itself be an important aspect of an animal’s behavior. An in-depth perspective on the factors influencing foraging behavior in individual species (or populations) is needed before meaningful conclusions can be drawn from comparisons among species.

The lizard Gambelia wislizenii: neither ambusher nor intensive forager? G. wislizenii may fit Regal’s (1978) definition of cruising foragers (Montanucci, 1978; Tollestrup, 1983). It can also be considered a brief-wait ambusher. When G. wislizenii does exhibit extended-wait ambush behavior, it does not choose vertically prominent sites, as do most ambushers of arthropods (Regal, 1978), but instead it waits in the shade under shrubs (Tollestrup, 1979). G. wislizenii is not believed to be territorial (Tollestrup, 1979), and females are the larger sex (Lappin and Swinney, 1999). In Harney County, males reach a maximum snout-vent length (svl) of 102 mm, and females reach 113 mm (Steffen, 2002). The most likely cause for greater female body size is selective pressure for females to

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produce larger young, which must be able to capture enough large, mobile prey to enable growth and fat storage before their first hibernation (Tanner and Krogh, 1974). There are several published accounts of the types of prey eaten by Gambelia wislizenii, primarily based on stomach contents, showing it to be an opportunistic feeder, with a wide prey base. These studies also show an apparent latitudinal cline in prey types consumed. Southern populations of leopard lizards, where individuals attain a larger body size, consume more vertebrates; about 49% of G. wislizenii had lizards in their stomachs. In the northern populations of G. wislizenii, which are more reliant on invertebrates, only 7% of G. wislizenii had lizards in their stomachs (Parker and Pianka, 1976). Vertebrate prey usually consists of lizards in the genera Callisaurus, Dipsosaurus, Aspidoscelis, Sceloporus or Uta, but G. wislizenii sometimes eats small snakes and the pocket mouse, Perognathus sp. (McCoy, 1967; Pietruszka et al., 1981, R. Anderson, pers. comm.). Invertebrate prey are diverse, but predominantly comprise orthopterans, with hymenopterans, beetles, spiders, cicadas and robberflies also featuring (Knowlton and Thomas, 1936; McCoy, 1967; Tanner and Krogh, 1974; Essghaier and Johnson, 1975; Whitaker and Maser, 1981; Steffen, 2002). In the context of intrafamilial and intraorder differences in foraging behavior, G. wislizenii is a promising species in which to study foraging, due to its unusual adaptations for a saurophagous (lizard-eating) diet. The unusual behavioral and morphological traits of G. wislizenii contrast with lizards in the closely related genus Crotaphytus, which are considered archetypal ambushers (Husak and Ackland, 2003). The diet of G. wislizenii also varies widely between populations (Parker and Pianka, 1976). Therefore, it may be possible to investigate the differences in foraging behavior between G. wislizenii and its close relatives, and among populations of G. wislizenii. Combined with the knowledge of differences in 8

environmental conditions and prey availability among populations, a link may be established between changes in food-acquisition mode and changes in a species’ habitat and prey.

Questions asked in this study The high population density of Gambelia wislizenii in southeast Oregon, and the ease with which the lizard can be observed and captured make G. wislizenii an easier lizard to study than most other lizards for which foraging studies have been performed. Moreover, unlike many prior studies on food-acquisition mode in lizards, two of the four basic autecological tasks can be considered to have little influence during this field study of G. wislizenii. Mate seeking can be disregarded because observations took place after the reproductive season. Also, in this region, G. wislizenii face relatively little risk of predation, therefore predator avoidance is unlikely to have a significant effect on G. wislizenii foraging behavior. This presumption is made because very few predators of G. wislizenii were seen in the general area of the study site and no predation attempts on G. wislizenii were witnessed in more than five hundred person-search-days of lizard searches and observations on the study site over five years (R. Anderson, pers. comm). The remaining two tasks, acquiring food and avoiding environmental stresses are therefore the focus of the study. The main questions are how availability among prey types affects foraging behavior in G. wislizenii in southeast Oregon, and whether temperature constrains foraging behavior. Ancillary questions that contribute ecological context are whether food resource defense occurs in Gambelia wislizenii and whether food resource distribution affects the movements of individual lizards. Determining whether there are differences in foraging behavior between the smaller males and the larger females would also provide useful perspective on their foraging behavior. To 9

answer these questions, foraging behavior in G. wislizenii was observed throughout the day at different times of the activity season. Based on current knowledge of G. wislizenii foraging and preliminary observations in southeast Oregon, the following hypotheses were formed: 1. G. wislizenii will use extended-wait ambush behavior to attempt to capture wide ranging lizards, but forage more actively to find and capture more subtly moving grasshoppers. G. wislizenii will switch from extended-wait to brief-wait ambushing when whiptail lizard availability declines relative to grasshopper availability. 2. Smaller G. wislizenii will be prohibited from successfully capturing adult lizards, so extended-wait ambushing will only be seen in larger individuals. As females are larger than males, this will result in a difference in foraging behavior between sexes. 3. Because G. wislizenii searches visually for cryptic grasshoppers that appear to move infrequently, it is expected that G. wislizenii in the laboratory will capture crickets that (a) move faster in prey choice experiments, or (b) contrast most with the background. 4. As G. wislizenii is a heliothermic lizard living in a desert habitat, intensity of sunlight and high air and sand temperatures will constrain movement rates during the hottest part of the day, with consequences for foraging behavior. 5. For individual G. wislizenii to best search for prey distributed patchily in time and space, within and among mesohabitats, its home range should cover all three mesohabitats on the study plot, and territorial defense of resources should be absent. Extensive home range overlap with numerous other individuals would confirm movements are not related to patrolling territories. 10

METHODS

The study species Gambelia wislizenii, the long-nosed leopard lizard, is a medium-sized lizard, which can be found in the Great Basin, Sonoran, Mojave and Chihuahuan deserts throughout much of the western United States (Stebbins, 1985). It is found as far south as northern Mexico and as far north as southern Oregon and southern Idaho (Figure 1). In Oregon, where this study takes place, they occur in eastern and southern Malheur county, southern Harney county and southern Lake county (Brown et al., 1995). In southern Harney county, where the lizard was studied for this research, G. wislizenii can be found up to an elevation of 1,460 meters. While recorded in variety of habitats, leopard lizards are usually found on desert flats with sandy to gravelly soil and sparse vegetation (McGuire, 1996). G. wislizenii ranked third most at risk of displacement by cheatgrass out of forty animal species officially listed as species of conservation concern in the Great Basin, with about 55% of its habitat at high risk of displacement (Wisdom et al, 2003). Long-nosed leopard lizards are polymorphic in dorsal color pattern across the species’ geographic range (Montanucci, 1978) with the size of the dark dorsal spots against the tan ground color and the degree of reticulation varying with vegetation type. The high degree of reticulation in the Great Basin populations of leopard lizards ensures cryptic coloration in the dappled shade on the ground under small-leaved shrubs, the microhabitat where leopard lizards are commonly found. Cryptic coloration minimizes the chance that stationary G. wislizenii will be seen by their predators and the lizards G. wislizenii prey upon. Females display bright nuptial coloration, however, in the form of orange-red spots along the 11

Figure 1. Geographic distribution of Gambelia wislizenii, redrawn from McGuire, 1996. The cross marks the location of the study site in southeast Oregon. 12

sides of the body and as a solid color on the underside of the tail, from the time of ovulation (late May/early June in Oregon) until a few weeks after the deposition of eggs. Steffen (2002) found nuptial coloration of Oregon females to remain bright after the breeding season into early August. Gambelia wislizenii has a variable length of activity season across its geographic range; the activity season lasts about three (Colorado) or four (southern Idaho) months in northern regions (McCoy, 1967; Essghaier and Johnson, 1975), yet in southern regions (southern California) the activity season of G. wislizenii may last six months, from early April to late October (Miller and Stebbins, 1964; Tollestrup, 1979). Despite G. wislizenii being at the northern limit of its geographic range in Oregon (allowing an activity season of around three months), long-nosed leopard lizards are nonetheless found at greater densities further north than in southern parts of its range (Steffen, 2002). For example, Tanner and Krogh (1974) calculated a density of 2.3 G. wislizenii per hectare in southern Nevada, and Essghaier and Johnson (1975) calculated 10 per hectare in southern Idaho. There are few reports of predation on Gambelia wislizenii. Tollestrup (1979) observed an unsuccessful attempt by a prairie falcon to capture a leopard lizard. She hypothesized potential predators of G. wislizenii in California to be coachwhip snakes (Masticophis flagellum), sidewinder (Crotales cerastes) and Mojave rattlesnakes (Crotales scutulatus), loggerhead shrikes (Lanius ludovicianus), several raptors, burrowing owls (Speotyto cunicularia), badgers (Taxidea taxus), coyotes (Canis latrans) and kit foxes (Vulpes macrotis). McGuire (1996) also proposed other lizard-eating snakes to prey on G. wislizenii. These are: the patch-nosed snake (Salvadora sp.), common kingsnake (Lampropeltis getula), gopher snake (Pituophis melanoleucus), glossy snake (Arizona 13

elegans) and long-nosed snake (Rhinocheilus lecontei). Of the many potential predators, fewer than half, only the following, were present in the Alvord Basin: loggerhead shrikes, burrowing owls, red-tailed hawks (Buteo jamaicensis), American kestrels (Falco sparverius), badgers, coyotes, whipsnakes, gopher snakes and rattlesnakes (Abts, 1976). Sightings of any of these predators at the study site were rare, however, and no evidence of predation on G. wislizenii was found during this study.

The study site The area chosen for investigation of foraging behavior in Gambelia wislizenii is the Pueblo Valley in the south end of the Alvord Basin, Harney county, Oregon. The Alvord Basin is small (approximately 82km2) and is surrounded by Steens mountain, Pueblo mountains and Trout Creek mountains (Baldwin, 1964). The Alvord Basin forms part of the Great Basin desert, which runs from southeast Oregon and south Utah through Nevada to eastern California and western Utah (Grayson, 1993), and represents the northernmost limit of the long-nosed leopard lizard range. The Great Basin is a “cold desert” characterized by high elevation deserts, with saltpans at “basin bottoms” (Larson, 1977). Sagebrush (Artemesia spp.) dominates the vegetation, together with shadscale (Atriplex spp.) and greasewood (Sarcobatus spp.). There are three identifiable mesohabitats in approximately equal proportions on the study plot: small dunes, slightly less densely vegetated sandy flats, and sparsely vegetated hardpan.

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Documenting spatiotemporal patterns of lizards The sighting data from standardized plot searches (SPS) were used to document hourly changes in the abundance of each species of lizard, and to estimate home range size and overlap for individual G. wislizenii that were frequently sighted. SPS were systematic searches for all species of lizards, performed regularly throughout the day in a predetermined area. Precise location of the lizard and the type of mesohabitat in which it was found during searches were also collected to examine the relationship between mesohabitat uses and the availability of prey among mesohabitats. The area selected to be the focus of this study was a 150m by 150m (2.25 ha) plot, which had been marked out and gridded at 10m intervals in a previous year. Flags at each interval listed a Cartesian coordinate, describing its location within the grid. The southernmost edge of the plot represented the x-axis, the easternmost edge the y-axis and the southeastern corner 0,0. This allowed lizard sightings to be estimated to the nearest 0.5m. Since the area within 10m of the perimeter of the plot was surveyed as intensely as the area inside the grid, the total area included in the survey was 2.89 ha. Standardized searches of the study plot in 2003 took place every day from June 27July 15 and from August 11-14. In July, to best represent daily patterns of activity for each lizard species, the day was divided into two-hour time periods, from 0730 to 1930, and standard plot surveys (SPS) took place in approximately equal numbers in each time period. Between six and sixteen people (on average, eleven) searched the plot during a survey, in teams of either three or four. In August, SPS only occurred during the first three time periods (0730-1330), when either one or two teams of three searched.

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The principal search method used was systematic, with all teams slowly moving parallel in either a north-south or east-west direction. Surveys continued until the entire area of the plot had been covered or until one hour had passed since the start of the search, whichever was soonest. Each team walked slowly through the plot, following the plot markers such that a 10m wide, 150m long transect was covered. After 15 minutes, upon reaching the edge of the plot, the team would shift over 10 or 20 meters and continue the survey in the reverse direction. By dividing the plot among teams, all of the plot could be surveyed without repetition of transects. One team commonly would also search the perimeter of the plot in a 10m-wide swath, walking a circuit around the entire plot. All lizards seen during the SPS were recorded, so data were collected on five lizard species: leopard lizard, Gambelia wislizenii; western whiptail, Aspidoscelis tigris; desert horned lizard, Phrynosoma platyrhinos; sagebrush lizard, Sceloporus graciosus and sideblotched lizard, Uta stansburiana. The SPS technique was best suited to census G. wislizenii and A. tigris because a team of several searchers could routinely and readily flush these two lizard species from cover of vegetation and out into the open. Only data from these two species are presented here. Each survey team had a scribe to record information about each lizard seen: time, species, identifying paint mark (see below), plot coordinates and details of location (such as nearest shrub species, substrate and degree of shade). Lizards with paint marks were not caught, whilst those without paint marks were caught by noose pole or by hand and placed alone in a cloth bag for later morphometric study. With few exceptions, within a day of capture each lizard was weighed and measured. A stiff, transparent plastic ruler was used to measure snout-vent length to the nearest 0.5mm, 16

and tail length (detailing which, if any, portions of the tail had regrown after breakage). Mass was recorded to the nearest 0.01g using a portable electronic balance (Ohaus model CT200S). Sex of the individual, reproductive status of females and food in the gut, detected by palpation (Steffen, 2002) were also recorded. If the lizard had not been caught previously on the site (including earlier years), it was permanently identified through toe clipping; two or three toes were removed from each individual, though never more than one from each foot and never the longest toe on either hind foot. The combination of removed toes was unique to each lizard. To facilitate identification in the field, each lizard was also painted with a unique combination of one to three transverse stripes, choosing from five colors of non-toxic paint markers. Any lizard that had shed its skin, and therefore lost its paint mark, was recaptured and painted with the same combination of colors. Data collected throughout all SPS were used to determine lizard population densities on the plot and to document mesohabitat and microhabitat preferences, but only searches carried out from July 1-13, and from August 11-14 were used to calculate relative lizard abundances throughout the day. This was because an intensive effort was made in the first few days to capture, weigh, measure and mark most of the lizards on the study plot, causing frequent interruptions during searches and complicating calculations of abundance. Only when the majority of lizards on the study plot were painted was most time spent searching for and sighting lizards during SPS, rather than capturing them. At this point, reliable estimates of abundance for each species at each time period could be calculated. Every team recorded the time they began the SPS, when they paused to record a sighting or to capture a lizard, when search was resumed and when the survey ended. From 17

this information, person search time could be calculated by summing the time a team actually spent searching for lizards (start to end of SPS, less time paused) and multiplying the time by the number of people in the team. These data were then used to determine the average number of each species seen per person, per search hour at each time period. Differences in lizard abundance between time periods were tested for using ANOVA, with post-hoc Scheffe’s tests. Germano et al. (1997) compared ten-day censuses of Gambelia silus to whole season censuses and found them to be an accurate index of population size, so the short duration of the census in this study should not have affected density estimates. Locations recorded from SPS were also used to determine the home range locations and sizes of Gambelia wislizenii seen in July. August data were too few for this analysis. All individuals seen eight or more times were included in the analysis, once the data had been corrected for lizards observed twice on the same day and time period (the latter of the two sightings was omitted), yielding a sample size of six females and eight males. The minimum convex polygon was used to estimate home range for the three lizards with more than twenty sightings. For all fourteen lizards, the Home Ranger software package (Version 1.5; Hovey, 1999) was used to estimate home range by the least squares cross validation (LSCV) fixed kernel method. This method has been demonstrated to have the least bias in estimating home range size from low sample sizes or non-normal distributions (Seaman and Powell, 1996), compared to other estimators of home range. Ranges based on the 0.95 density contour (indicating the area an individual is expected to be found 95% of the time) were plotted to compare home range overlap because this area best fits the definition of home range as “the area traversed by the individual in its normal activities of food gathering, mating and caring for young. Occasional sallies outside 18

the area, perhaps exploratory in nature, should not be considered as in part of the home range” (Burt, 1943). The percentage of home range overlap was determined only from lizards that were sighted eight or more times, therefore home range overlap may be higher than estimated.

Focal observations to investigate foraging behavior in G. wislizenii Data from a thirty-minute long focal observation for each of 57 individual G. wislizenii enabled measures of prey pursuits, the number of movements per minute and percent time spent moving for each lizard. Both sexes and all two-hour time periods of the daily activity period were equally represented in the focal observation data set, and individuals were not observed twice in the same month. The individuals observed were also all post-reproductive. Consequently, relationships of foraging behavior to environmental temperatures could be examined and differences in behavior between males and females could be investigated. Moreover, correlations of foraging behavior throughout the day and in two months in the activity season could be made to variation in both environmental temperatures and prey availability. All focal observations of Gambelia wislizenii in 2003 were carried out by one observer (ELR) from June 29-July 14 and from August 10-14, between 0730 and 1730. By splitting the day into two-hour time periods, as with the SPS, equal numbers of observations were attempted throughout the day. Most observations (approximately 70%) took place on the gridded 2.25 ha plot where SPS were conducted. The remaining observations occurred within 150m of the study plot in similar, contiguous habitat.

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Gambelia wislizenii were located by walking slowly through the area until one was seen. Although around half the lizards sighted moved 50-70cm in response to the observer walking very close to them before they were seen, they quickly resumed normal activities in almost all cases. Lizards were watched for at least five minutes before the recording of focal observations began to ensure they displayed no lingering wariness from the discovery encounter. About 5-10 % of G. wislizenii were still wary of the observer at this point, as evidenced by repeated head turns in the observer’s direction, or “freezing” behavior whereby a lizard remained unmoving beneath a shrub yet made certain it could keep the observer in view; these observations were abandoned. The focal observations were begun only on ostensibly unwary individuals; activities of the lizard were voice-recorded continuously onto microcassettes and time from a stopwatch was frequently vocalized to verify timing and duration of observed behaviors. To reduce even further any subtle effects of the observer on the lizards, the observer maintained a minimum distance of 5m from the lizard (except when it happened to move towards the observer). When a lizard moved frequently prior to the start of the focal observation, the observer stood to the side of the lizard and its direction of movement, behind shrubs, if possible. When a lizard moved less frequently, the observer stood behind the lizard, away from its line of sight, also behind shrubs. As an extra precaution, greater distances between the observer and lizard were maintained when the vegetation was sparser. From previous field observations and experiments, it quickly became apparent leopard lizards are particularly adept in noticing movement (compared to form or color). Therefore, to avoid distracting the lizard, the observer remained as still as possible throughout the focal observation period. When the lizard did not move for a relatively long time (greater than five 20

minutes), the observer slowly moved to a position approximately 5m directly behind the head of the animal, in a position where the lizard would not be able to see the observer without moving its head in a noticeable way. If the lizard did not turn its head sharply towards the observer, it was assumed that the observer was not affecting the lizard’s behavior. When the lizard was moving more frequently, the observer had to change the observation location to ensure continuous observations. The observer changed locations by moving in a generally parallel direction to the lizard’s movement, circling slightly away from the leopard lizard as the lizard moved and returning slightly toward as the lizard paused, thereby limiting the chance of the lizard perceiving itself to be stalked or chased. Detailed information collected on the voice recorders included: •

The start and end of each behavior

•

Direction, and distance for each movement and whether the lizard was walking, running, jumping, climbing, lunging or changing position.

•

Type of prey seen, chased and/or eaten by the lizard.

•

Any interactions the lizard had with other lizards.

•

Microhabitat used by the lizard at all times, i.e. substrate, proportion of the body of the lizard in the sun, closest shrub species to the lizard, and the lizard’s position relative to it (e.g. edge, center, on).

•

Postural changes by the lizard, e.g. rapid head wags and tail wiggles (both associated with foraging), tongue-touches to substrates, basking and changes in head direction. The thirty-minute, voice-recorded focal observations were transcribed onto data

sheets; timing and duration of behaviors were measured with a stopwatch during playback. Time checks were performed approximately every five minutes, in which the time from the 21

stopwatch was spoken into the voice recorder for comparison to playback time. Only on three focal observations were the playback times more than 1 second/minute different from the times noted during the focal observations and even these were only 2-3 seconds/minute faster or slower. Playback speed did not vary relative to recording speed within a thirty minute focal observation period, as determined by the five minute time checks, enabling a simple adjustment of all times within an observation. For every single focal observation, the times noted in transcription were adjusted so each transcribed observation finished at exactly 30 minutes, simplifying further analysis. Summary statistics of the transcribed focal observations were calculated for each observed behavioral event, including the mean number of movements per minute, MPM (numbers of walking/running/jumping/stalking moves were also recorded individually) and the percent time spent moving, PTM. Values for MPM and PTM both excluded slight changes in body position (movements of less than 10cm, excepting stalking behavior). The distance moved per minute is perhaps the least useful variable to compare among intensive foragers and ambushers as it varies with lizard body size and microhabitat patchiness (Anderson, 1993; Cooper et al., 2001). Moreover, intensive foragers move faster between patches than within patches (Anderson, 1993) and ambushers may move rapidly between ambush sites. MPM may be of less use in distinguishing foraging tactics among species than is PTM, but MPM may be a valuable measure for studying variation in foraging among individuals within a species, particularly for ambushers (Cooper et al., 2001). Also calculated from focal observation data were median pause length (more useful than mean pause length to indicate the movement patterns of particular lizard), total distance moved, percent time spent in the open (defined as more than 20cm from the edge of a shrub 22

for ease and constancy of assessment), and summaries of prey types pursued and caught. The number of prey capture attempts refers to the number of different prey items a lizard pursued, regardless of whether these pursuits resulted in a successful capture, or if the prey evaded the lizard or the lizard abandoned the prey (such as when a grasshopper remained unmoving for a long period of time and the lizard could not find it again after the initial sighting). Multiple capture attempts by a leopard lizard on the same individual prey were only recorded as one pursuit episode. Possible differences in foraging behavior between males and females and between July lizards and August lizards were analyzed, using the computer program SPSS, with nonparametric statistics (Mann-Whitney U for 2 samples, Kruskal-Wallis for more than 2 samples) because the behavioral data did not meet the assumptions of parametric statistics, that is, the data were not normally distributed and most variables failed tests for homogeneity of variance. After log transformation, the data still did not meet parametric assumptions. Correlations between MPM and PTM, and other variables, such as air temperature, were analyzed using linear regression, or a second or third order polynomial regression line if the pattern was not expected to be linear. The figures were produced using Excel. Significance of regressions were attained using SPSS. Multiple regression to distinguish between the effects of temperature and prey availability on movement rates could not be performed because of the collinearity of time of day, environmental temperatures and whiptail abundance. The identity and condition of each lizard subject to a focal observation was verified. Most lizards in focal observations had paint marks and had been weighed and measured in the two weeks prior to the observation. Hence, there was little difficulty in ensuring that any 23

individual lizard was the subject of only one focal observation in July and at most one additional observation in August. These lizards were visually inspected and their stomachs were palpated to allow detection of any large prey items (to assess whether the lizard was likely to be sated during the period of observation), then the lizard was released at the point of capture. Unpainted lizards were captured following a focal observation, painted and measured as necessary, then released at the point of capture, ensuring another focal observation was not carried out on that lizard that month. At the end of each focal observation for all lizards in August and for the last half of the lizards sampled in July, the lizard was caught and, within 15 seconds of capture, its deep body temperature was measured; the tip of a rapid registering mercury-bulb thermometer was inserted about 5cm into the cloaca. These measurements were made to test the assumption that lizards in focal observations were at field-active body temperatures.

Grasshopper abundance surveys The grasshopper surveys were designed to count the number of grasshoppers a leopard lizard would be likely to encounter at a particular microhabitat or time of day. Grasshopper surveys were carried out on nine 10m by 40m transects either on the study plot or within 20m of it. Because there are three mesohabitat types on plot, hardpan (HP) sandy flats (SF) and dunes (D), three transects were used for each mesohabitat. Each transect was gridded and flagged at 5m intervals, giving sixteen 5m by 5m quadrats (two rows of eight), to facilitate a systematic search. On July 6-13 (0730-1930) and August 11–13 (0730-1330), the grasshopper surveys were carried out concurrently with the SPS and focal observations. During each two-hour 24

time period, each mesohabitat was surveyed for grasshoppers 2-6 times (mean = 4). Limited time and personnel in August allowed for surveys of only two SF transects (and no HP or D), with four surveys in each time period. The search technique was the same in both months. Three or four people participated in each grasshopper survey, with one person scribing information about grasshoppers seen by the other members of the team. Eight of the sixteen quadrats were searched during a grasshopper survey, sequentially moving between diagonally opposite quadrats (i.e. sampling no quadrats with a shared side) to best represent the transect. The standard search method involved walking between islands of shrubs, bending close to each shrub and lightly pressing the outside of the shrub from the base to the top in a slow, continuous motion. Grasshoppers thus were detected primarily through their response to this minor disturbance. While searchers walked, they visually scanned the ground for the presence of grasshoppers. No longer than five minutes were spent on a quadrat. There were an average of 7 shrubs per quadrat on hardpan, 35 shrubs per quadrat on sandy flats and 40 shrubs per quadrat on dunes. For every grasshopper, the date, time and mesohabitat were recorded, along with life stage (nymph or adult) of the grasshopper. Analysis of Variance – Repeated measures (ANOVAR) was used to investigate differences in grasshopper abundance among mesohabitats and time periods, with time period as the within-subject factor and mesohabitat as the between-subjects factor because the number of grasshoppers seen in each survey were not independent values. Within each of the 3 transects of each mesohabitat type, every plant was identified to species, and its height and maximum and minimum diameter (viewed from above) measured. These data were used to calculate plant volume by species in each mesohabitat and in the study plot as a whole for comparison of mesohabitat use by grasshoppers and G. wislizenii. 25

Environmental Temperatures From June 27 to July 14, the air temperature 2m above the ground surface (Ta) was recorded about twelve times a day (range 5-25). The temperature of the horizontal surface of the sand in direct sunlight (Tss) was recorded about nine times a day (range 3-19). The temperature of the sand surface in “deep” shade (Tssh) was also measured intermittently. The Ta was measured using a rapid registering thin-bulb mercury thermometer. The thermometer was waved rapidly, shaded by hand from 20cm above; the reading reached thermal equilibrium within 5 seconds. The temperature reading was watched for about 30 seconds, and an approximate modal temperature recorded. In fairly still conditions, temperature fluctuated by a few tenths of a degree during this thirty-second period, but during windy conditions, temperature variation of as much as a few degrees Celsius could occur. This variation was small relative to the 20oC change in Ta throughout the day. Tss and Tssh were measured with a digital thermocouple thermometer, using a standard technique of lightly running the copper-constantan sensor across the flat sand at an approximate depth of one millimeter, barely covering the sensor with the uppermost surface substrate. Temperature measurements for each day were plotted against time of day and fitted with a second order polynomial regression line. The weather was stable throughout the study (no rain or strong winds or substantial cloud cover on any day). Also, for those days on which the number of measurements permitted a reasonable estimate of daily temperature change, the line equations for Ta and Tss varied little among days. Therefore, the data for all days were combined in one figure and polynomial lines of regression for Ta, Tss and Tssh plotted (Figure 2).

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70.0 Tss Tssh

60.0

T at 2m

Temperature (oC)

50.0 40.0 30.0 20.0 10.0 0.0 5:00

7:00

9:00

11:00

13:00 15:00 Time of day

17:00

19:00

21:00

Figure 2. Hourly changes in the temperature of the surface of the sand in full sun (Tss), temperature of the surface of the sand in deep shade (Tssh) and air temperature 2m above the ground (T at 2m) between June 27 and July 14, 2003, and the second order polynomial line of regression fitted to each. Sample sizes are: Tss = 110, Tssh = 88, T at 2m = 253. The regression line for Tss is y = –483.16(x)2 + 566.62(x) – 106.53 (R2=0.856, p