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University of Nevada, Reno

Isolation at Work: Body Size Divergence between Reptiles of Nevada’s Pyramid Lake and Anaho Island

A thesis submitted in partial fulfillment of the requirements for the degree of

Bachelor of Science in Wildlife Ecology and Conservation and the Honors Program

Jade E. Keehn

Chris R. Feldman, Ph.D., Thesis Advisor Department of Biology

Nathan C. Nieto, Ph.D., Thesis Advisor Department of Agriculture, Nutrition, and Veterinary Sciences

May 2012

UNIVERSITY OF NEVADA THE HONORS PROGRAM RENO

We recommend that the thesis prepared under our supervision by

JADE E KEEHN

entitled

Isolation at Work: Body Size Divergence between Reptiles of Nevada’s Pyramid Lake and Anaho Island

be accepted in partial fulfillment of the requirements for the degree of

WILDLIFE ECOLOGY AND CONSERVATION, BACHELOR OF SCIENCE

______Chris R. Feldman, Ph.D., Thesis Advisor

______Nathan C. Nieto, Ph.D., Thesis Advisor

______Tamara Valentine, Ph.D., Director, Honors Program

May 2012

ABSTRACT

This Island Rule is a long-held tenet of biogeography which states that insular populations trend towards increased mean body size in small species and decreased mean body size in large species—a trend that has been inconsistent and even contradictory with reptile taxa. This study examines insular and mainland reptile populations of Aspidoscelis tigris tigris¸ Crotalus oreganus lutosus, Callisaurus draconoides myurus, Sceloporus uniformis, and Sceloporus occidentalis longipes to determine whether the Island Rule conforms with the observed size trends on Anaho Island in Pyramid Lake, Nevada. The selective influences of predation and resource abundance on body size are evaluated by comparing (1) the frequency of caudal autotomy to determine the influence of predation pressure and (2) head shape as a trait affected by the availability of prey resources.

Differences in head shape reveal patterns consistent with a shift to smaller prey in A. t. tigris as well as decreased head height for the C. o. lutosus, A. t. tigris, and C. d. myurus.

Differences in tail-regeneration frequencies are consistent with an altered pattern of predator-prey interaction for A. t. tigris and S. uniformis. Body size results on Anaho

Island contradict the Island Rule, with C. o. lutosus, A. t. tigris, and C. d. myurus males exhibiting smaller body sizes on the island while S. o. longipes and S. uniformis exhibit no size trend, perhaps as the result of a small sample size. Divergence in body size occurs on the island, in a direction that is consistent with the primary literature. This study supports the conclusion that Anaho Island harbors a community of reptiles that is distinct from the mainland in morphology and possibly in ecology and life-history evolution.

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ACKNOWLEDGMENTS

First and foremost, I would like to thank Drs. Chris R. Feldman and Nathan C.

Nieto for their help, their patience, and their unfaltering support. I would also like to thank Tony Bush for providing me with much needed enthusiasm and positivity when I could find none of my own.

This research would not have been possible without the contributions of the following individuals and organizations: The California Academy of Sciences, Museum of Vertebrate Zoology, University of Kansas Biodiversity Institute, and San Diego

Natural History Museum for providing access to specimens; Xavier Glaudas for generously allowing me to access his data; Drs. Dick Tracy and Chris Gienger for conducting valuable research that served as a strong foundation for this project; Donna

Withers of the USFWS, the Nevada Department of Wildlife, and the Pyramid Lake

Paiute Indian Tribe for allowing access to study sites and specimens; Peter Murphy for his insightful contributions to statistical analyses; the Honors Undergraduate Research

Award (HURA) for providing funding; and Honor’s Program Director Dr. Tamara

Valentine who inspires students every day to achieve more than what they think themselves capable of.

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TABLE OF CONTENTS

ABSTRACT ...... i ACKNOWLEDGEMENTS ...... ii TABLE OF CONTENTS ...... iii LIST OF TABLES ...... iv LIST OF FIGURES ...... v EPIGRAPH ...... vi INTRODUCTION ...... 1

THE ISLAND RULE ...... 1 NATURAL SELECTION: PREDATION PRESSURE ...... 3 NATURAL SELECTION: DIET ...... 5 STUDY SITE ...... 8 SPECIES OF INTEREST ...... 10 OBJECTIVES ...... 11 MATERIALS AND METHODS ...... 14

RESEARCH AREA ...... 14 MEASUREMENT METHODS ...... 14 DATA ANALYSIS ...... 16 RESULTS ...... 20

BODY SIZE ...... 20 TAIL-REGENERATION ...... 20 HEAD SIZE ...... 21 DISCUSSION ...... 22

BODY SIZE ...... 22 TAIL-REGENERATION ...... 22 HEAD SIZE ...... 24 FUTURE DIRECTIONS ...... 25 MANAGEMENT IMPLICATIONS ...... 25 WORKS CITED ...... 27 TABLES AND FIGURES ...... 34 APPENDIX 1 ...... 45

MUSEUM SPECIMENS ...... 45

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LIST OF TABLES

Table 1. Results from a Student’s T-test comparing body size between mainland and island individuals of the same sex and species. Average body size (SVL) on Anaho Island relative to Pyramid Lake is significantly different (bolded if P < 0.05) when mean body size of N individuals of differs between locations ...... 34 Table 2. Overall tail-regeneration frequencies, separated by species for the sexes of either location ...... 35 Table 3. Results from proportion tests and Fisher’s exact tests for pair-wise comparisons of locality and sex groups ...... 36 Table 4. Arrows show whether the “complex” MANOVA returned different proportions of head size relative to body size (using the independent variable location) between locations and independently for males (♂) and females (♀). Arrows indicate a trend towards smaller (down) or larger (up) variable size on Anaho Island relative to the Pyramid Lake mainland ...... 37

LIST OF FIGURES

Figure 1. Map of the Truckee River drainage basin and location of Pyramid Lake Indian Reservation ...... 38 Figure 2. USGS topographic map of Anaho Island (top) and horizontal view of Anaho Island (bottom, from Benson 2004) showing terraces when the lake level was 1,265 m (DT), 1,207 m (ET), and approximately 1,200 m (MT) ...... 39 Figure 3. Satellite image showing the geographic restrictions used to set the boundary for specimen collection locations, orange. Left: C. o. lutosus. Right: other squamates ...... 40 Figure 4. Illustrations modified from Powell et al. (2012, Figures 140, 232, 244, and 176) showing the landmarks used for head measurements ...... 41 Figure 5. Photographs of a normal (left) and regenerated (right) tail. Landmarks used to determine whether or not tail had been regenerated are identified including the fracture plane, normal scale rows, abnormal scale rows, and the original tail ...... 42 Figure 6. Body size frequency histogram (generated in Excel) for both male and female A. t. tigris. Mean body size differs between Anaho and Mainland samples ...... 43 Figure 7. Body size frequency histogram for both male and female C. o. lutosus. Mean body size differs between Anaho and Mainland samples...... 44

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EPIGRAPH

“To give an imaginary example from changes in progress on an island:- let the organization of a canine animal which preyed chiefly on rabbits, but sometimes on hares, become slightly plastic; let these same changes cause the number of rabbits very slowly to decrease, and the number of hares to increase; the effect of this would be that the fox or dog would be driven to try to catch more hares:…those individuals with the lightest forms, longest limbs, and best eyesight…would be slightly favoured, and would tend to live longer, and to survive…; they would also rear more young, which would tend to inherit these slight peculiarities. The less fleet ones would be rigidly destroyed. I can see no more reason to doubt that these causes in a thousand generations would produce a marked effect, and adapt the form of the fox or dog to the catching of hares instead of rabbits…”

– Darwin and Wallace 1858

INTRODUCTION THE ISLAND RULE

The unique adaptations of insular animals are a thought provoking topic in the study of biology. Insular giants and dwarfs drew attention from early researchers who attempted to find universal explanations for the intraspecific divergence of body size on islands (Foster 1964). Van Valen (1973) believed that body size divergence in island mammals followed a broad scale pattern, describing the emerging trend as the Island

Rule. This rule proposes that smaller species trend towards larger body size and large species trend towards smaller body size when isolated on islands (Van Valen 1973).

Many evolutionary mechanisms have been proposed for the Island Rule including resource limitation, competition, predation, and dispersal limitations (Lomolino 2005). In general, researchers have supported the idea that anomalous characteristics among island populations result from divergent selection regimes on mainland and island environments, which encompasses the mechanisms listed above (Pafilis et al. 2009a;

Palkovacs 2003; Shine 1987).

Genetic drift has also been proposed as a potential mechanism for divergence between populations (Lomolino 1983). Genetic drift is a random change in allele frequencies from one generation to the next, especially evident in small populations. Drift occurs when isolated populations experience reduced gene flow, which can also result in a genetically impoverished population (Pafilis et al. 2009a), or a random pattern of divergence among phenotypic traits. Drift cannot be excluded entirely from consideration as a mechanism of body size change; however, if multiple species have diverged from mainland relatives towards a predicted direction of change, drift can be discounted with 2 some certainty in favor of deterministic explanations such as varying degrees of dispersal ability among size classes or adaptive changes within a population (Meik et al. 2010).

The non-random association between body size and island area suggests that selective forces sensitive to island area might important to size divergence (Foster 1964; Meik et al. 2010).

Geographic factors such as the area of the island and the distance from the mainland may influence the magnitude of body size divergence (Meik et al. 2010), while interactions between local selective pressures determine the magnitude of body size change towards an optimum (Lomolino 2005). Body size directly impacts life-history traits including immigration potential, ecological interactions, and resource requirements

(Forsman 1991; King 1989; Lomolino 2005). Theory suggests that interspecific competition, predation, and parasitism are highly influential on large, proximate islands, while resource limitation and intraspecific competition influence populations on smaller islands (Lomolino 2005; Palkovacs 2003). Increased or decreased constraint on body size from selective differences in (1) predation pressure and (2) resource limitation are perhaps the two most relevant hypotheses for body size divergence in reptiles.

Squamates (lizards and snakes) are notorious for breaking the rules biogeography.

Reptiles exhibit the reverse of the well-supported Bergmann’s Rule, for example, which predicts increasing body size with increasing latitude or decreasing temperature (Ashton and Feldman 2003). It is not surprising, then, that scientific debate still exists over whether lizards and snakes conform to the Island Rule like other taxa such as mammals.

Boback and Guyer (2003) provided strong supporting evidence for the Island Rule in snakes, clarifying that dwarfism occurs in snakes larger than 1 meter (m) and gigantism 3 occurs in snakes smaller than 1 m. In general, researchers have found that gigantism is more common in iguanids, herbivorous reptiles, whiptails, tiger snakes, and tortoises, while dwarfism can be expected in rattlesnakes (Case 1978; Lomolino 2005; Soule

1966). Rattlesnakes contradict the proposed snake-wide trend toward an optimal body size of 1 m. In recent examinations of Crotalus mitchellii and C. viridis, both species exhibit dwarfism as the rule and not the exception, and both are on average less than 1 m in length (Ashton 2000; Meik et al. 2010), contradicting the predictions of the Island

Rule. On Anaho Island, the Great Basin Rattlesnake (C. o. lutosus) is thought to have diverged in body size with snakes on the island being smaller than those on the mainland

(Ashton 2000; Klauber 1956).

In lizards, conformity to the Island Rule is also lacking. A review by Meiri (2007) found that small lizards become smaller on islands while larger lizards increase in size.

This trend is particularly strong in carnivorous lizards, while results for omnivores and herbivores are not statistically significant. Here, I test the Island Rule in a local reptile community by examining body size variation between island and mainland populations. I then examine whether the island community shows evidence of selective differentiation resulting from resource competition or predation, as possible evolutionary mechanisms of divergence.

NATURAL SELECTION: PREDATION PRESSURE

Predation pressure is well supported in the literature as a causal mechanism for body size divergence (Crowell 1983; Tamarin 1978). Differences in body size might result from the release of a prey species from predation when a predator from the mainland is absent on the island. Selection could also occur if a novel or ecologically 4 different predator preferentially targets certain body size or age groups, causing a shift in mean body size (Lomolino 2005). On islands, the force of predation is expected to be less than on the mainland due to the presence of fewer predator species (Foster 1964;

MacArthur and Wilson 1967). Predator release should result in increased body size because the prey is less reliant on having a small body to hide from predators (Palkovac

2003; Werner and Gilliam 1984). While predator release has been studied in rodents, few studies have evaluated the effects of predation pressure on body size in reptiles

(Hasegawa 1994).

Comparing tail-regeneration frequencies between sites is one way to test whether the selective forces of predation differ. Caudal autotomy, the shedding of a tail along a breakage plane, is an often-used response to a predator attack by lizards (Cooper et al.

2004). The tail is shed, allowing the lizard to move away from the appendage and the predator is distracted from the fleeing lizard due to the wriggling movements of the free tail (Bateman and Fleming 2009). However, a higher incidence of tail-regeneration does not always imply that predation pressure is higher. Higher tail-regeneration frequency at one site over another can result from (1) more predation attempts due to either a greater susceptibility of a population to predation attacks or a higher density of predators, (2) a greater inefficiency of certain predators between sites, or a difference in the types or predators at a site, or (3) more frequent use of caudal autotomy as an escape mechanism between sites due to genetic divergence in ease of autotomy or selection for increased frequency of autotomy (Bateman and Fleming 2009; Pafilis et al. 2009b).

Regardless of the causal explanation for autotomic frequency, it is still valuable to look for differences in tail-regeneration frequencies to determine if some differences exist 5 in the ecology of predation between two sites. All of the three possible explanations above result from differences in predation pressure (as determined by the number, efficiency, and diversity of predators). Predation pressure corresponds with traits that influence tail-regeneration rates such as latency to autotomize and post-autotomic movements (Cooper et al. 2004), which indicates that tail-regeneration may be a trait responding to natural selection and the ecology of predation.

On a broad scale, showing that differences exist in selective forces between island and mainland communities lays a foundation for future investigations of how and why morphologic divergence might evolve. In this study, I examine the frequency of caudal autotomy to determine if differences in predation pressure, and thus selective forces, exist between island and mainland communities. I hypothesize that the frequency of caudal autotomy in lizards is higher on Anaho Island than on the mainland due to a higher density of predators (rattlesnakes) on the island (Klauber 1956). A recent study by Pafilis et al. (2009b) found that among multiple predator categories, the presence of snakes

(vipers) was significantly related to a higher ease (readiness to shed a tail when threatened) of autotomy. While rattlesnakes are predators of lizards on both the island and the mainland, rattlesnakes in high densities on Anaho are more likely to dine on lizards than on mice compared with their mainland counterparts, as few mice are found on the island (Glaudas et al. 2008). Thus, lizards should respond by evolving a high ease of autotomy, which is reflected by the rate of tail-regeneration (Pafilis et al. 2009b).

NATURAL SELECTION: DIET

Morphological and physiological variation can develop when species exploit different habitats and resources (Measey et al. 2011). Recent studies suggest that diet and 6 resource limitation occur in carnivorous lizards and snakes (Meik et al. 2010; Meiri

2007). Body size of islands species is hypothesized to decrease to account for lower resource levels (Palkovacs 2003). Likely, size differences result from differences in the relative abundances of certain prey types on islands (Pafilis et al. 2009a; Raia et al.

2010). These prey types include arthropods for smaller lizards and vertebrates for larger lizards and snakes (Case and Schwaner 1993).

More so than in other taxa, the body size of a viperid predator is closely linked to the size of its prey (Shine 1987, 1991). A snakes’ gape-limited feeding system of swallowing prey whole is responsible for this close association between predator size and prey size (Arnold 1993). On islands, body size differences in snakes are directly linked with mammal and reptile prey availability (Shine 1987). Where dwarf snakes occur, researchers find that relative abundances of smaller prey such as lizards exceed those of larger prey such as mammals (Case 1978; Meik et al. 2010; Shine 1987). Reduced prey availability is also associated with smaller gape size, such that dwarf rattlesnakes have shorter heads, resulting from a lower growth rate in relative head length (Meik et al.

2010). This research supports the prediction that a dietary shift from mammals to reptiles would results in decreased body size (Meik et al. 2010; Shine 1991).

On Anaho Island, rattlesnakes are thought to be smaller than their mainland counterparts (Ashton 2000; Klauber 1956). Recent survey efforts found that very few mammals exist on the island; this limited mammalian prey base is unlikely to support

Anaho’s high density of Great Basin rattlesnakes (C. Gienger, unpublished data).

Because Great Basin rattlesnakes feed predominantly on lizards when young and on 7 mammals as large adults (Glaudas et al. 2008), it is predictable that a dietary shift could account for observable differences in body size.

Combining these observations with the literature on island and mainland snake size relative to prey size (Boback 2006; Marcio et al. 1999; Schwaner 1985), I hypothesize that size differences between communities result from dietary shifts from mammals to lizards. Snakes will be smaller on the island because they are exploiting smaller-bodied prey. Because head size is highly correlated with body size and has been suggested as the selective target for diet-related size divergence (Meik et al. 2010), I predict that island snakes will also have heads that are smaller than their mainland counterparts (Boback 2006).

Size trends in lizards, as in snakes, are highly correlated with prey resource availability (Case and Schwaner 1993; Forsman and Lindell 1993; Verwaijen et al.

2002). As in snakes, a lizard’s gape size or head size determines the size of prey that can be consumed (Verwaijen et al. 2002). Lizards with larger heads can exert a stronger bite force: harder-shelled invertebrates can be consumed leading to a greater diversity of potential prey items in the diet (Herrel et al. 1999). A narrow prey base correlates with small-headed lizards and a wide prey base correlates with large head size (Case and

Schwaner 1993). A strong correlation also exists between maximum prey size and large head size that affects the ability to exploit large or hard prey (Measey et al. 2011). Head length and jaw dimensions were best at predicting bite force (Herrel et al. 2010), confirming that longer head lengths are associated with a stronger bite force, which is needed to consume larger prey. 8

According to the Island Biogeography Theory, prey abundance should decrease on islands relative to the mainland as a result of the species-area relationship (MacArthur and Wilson 1967). There is also a higher potential on islands for extinction of local populations, resulting from environmental stochasticity and lower immigration rates

(MacArthur and Wilson 1967). To deal with fewer prey resources, species are expected to develop wider prey bases on islands, broadening their dietary niche to account for the lack of traditional prey items in the island environment (Gravel et al. 2011).

If prey abundance is less on islands than on mainlands (Case 1978; Foster 1964;

MacArthur and Wilson 1967), lizards on Anaho Island should increase the diversity of prey that they consume to counter the absence of traditional prey items. Because the ability to exploit prey depends on gape size (Herrel et al. 1999), I hypothesize that on

Anaho Island, lizards will respond to a narrower prey base by increasing their gape size in relation to body size. I would not expect a concurrent increase in body size if prey is limiting because increased body size would result in a disproportionate increase in metabolic needs that are not matched by increased prey availability.

STUDY SITE

Pyramid Lake is located in north-western Nevada in Washoe County. The lake and surrounding area are designated as an Indian Reservation of the Pyramid Lake Piute

Tribe (Figure 1). Roughly 1 km from the eastern shoreline, Anaho Island (a federal wildlife refuge designated in 1940 and administered by the USFWS) stands 1,334 m tall and covers 247 acres (Figure 2), hosting an active colony of breeding American white pelicans, Pelecanus erythrorhynchos (Benson 2004; Murphy and Tracy 2005). Anaho

Island is unique in that not only does it have a nutrient enriched ecosystem resulting from 9 high seabird densities (Markwell and Daugherty 2002) but may also have a higher density of rattlesnakes than the Pyramid lake mainland (Klauber 1956).

Present day Pyramid Lake is a remnant of the pluvial Lake Lahontan, which covered much of north-western Nevada from 45,000 to 16,500 years before present

(YBP) (Benson and Thompson 1987). This lake reached its maximum elevation of 1,330 m in elevation approximately 13,500 YBP (Benson and Thompson 1987). Organic deposits were radio-carbon dated to age the erosion of the upper terraces of Anaho Island, placing the emergence of the island from the lake at between 10,850 and 9,600 YBP

(Benson et al. 1992).

When the lake elevation was approximately 1,220 m (Benson et al. 1992), water levels were in the process of receding, causing the erosion of the upper terraces and tufa formations of Anaho Island (Figure 2). Lake levels exceeded the highest terraces on

Anaho prior to this period of recession, signifying that land-bound macrofauna on the island have been isolated for at most 10,850 years. The colonization process could have occurred either by passage across a land bridge or through migrants crossing the open water. A land bridge seems more likely, given that multiple vertebrate taxa have colonized the island and that the island is within close proximity to the eastern shore of the lake (Figure 2).

Island environments provide excellent opportunities to study evolution in action.

Boundaries to migration such as lakes and oceans restrict gene flow, resulting in geographically proximal mainland and island populations that, in some cases, exhibit a striking amount of divergence in life history traits—for example gigantism in C. mitchellii on the Ángel de la Guarda island (Meik et al. 2010), or the presence of 10 flightless rails on islands but not on mainlands (Fraser et al. 1992). As in the previous examples, there may be little gene flow between the reptile populations on Anaho Island and the Pyramid Lake mainland. Gene flow acts through immigration and emigration, mixing the gene pools of neighboring populations. Without gene flow, each population can evolve distinctive characteristics that potentially influence fitness.

SPECIES OF INTEREST

This study focused on five reptile species. All species are present both on Anaho

Island and on the Pyramid Lake mainland. Nomenclature is taken from the most recent version (May 2011) of the list of official standard English and scientific names as maintained by the Society for the Study of Amphibians and Reptiles (Crother 2008).

Crotalus oreganus lutosus, Great Basin Rattlesnake, Klauber 1930:

Family: Viperidae. The Great Basin rattlesnake is a subspecies of the Pacific

rattlesnake (Ashton and de Queiroz 2001). It averages 65.3 (female) and 73.9

(male) cm snout-to-vent length (SVL) (Glaudas et al. 2008). Across its range, the

Pacific rattlesnake is highly variable in life-history characteristics such as body

size, sexual dimorphism, and coloration (Ashton and de Queiroz 2001). As a

viperid, it is a sit-and-wait predator that ingests its prey head-first (Greene 1992).

Diet is predominantly mammal-based, but also includes squamates and birds with

less frequency (Glaudas et al. 2008).

Callisaurus draconoides myurus, Northern Zebra-tailed Lizard, Richardson 1915:

Family: Phrynosomatidae. This slim-bodied lizard is typically 63 - 101 mm SVL

(Stebbins 2003). It is found in washes and open areas and its diet consists of 11

spiders, insects (grasshoppers, beetles, caterpillars, robberflies, and others), and

occasionally plants or other lizards (Stebbins 2003).

Sceloporus occidentalis longipes, Western Fence Lizard, Baird 1859:

Family: Phrynosomatidae. As one of the most commonly encountered lizards of

the west, the western fence lizard occupies many habitat types including human

dominated landscapes. Its SVL averages from 57 - 89 mm and its diet consists

principally of insects and spiders (Stebbins 2003).

Sceloporus uniformis, Yellow-backed Spiny Lizard, Phelan and Brattstrom 1955:

Family: Phrynosomatidae. This lizard (raised to the species level from a

subspecies of S. magister in Schulte et al., 2006) is both larger and stockier than

S. occidentalis with a typical SVL of 82 - 142 mm (Stebbins 2003). It frequents

arid and semiarid shrublands, hiding in crevices and small burrows. Insects

(larvae, ants, beetles, grasshoppers, termites, and caterpillars), spiders, centipedes,

buds, flowers, berries, and leaves compose its diet (Stebbins 2003).

Aspidoscelis tigris tigris, Great Basin Whiptail, Baird and Girard 1852:

Family: Teiidae. Typically, this predatory lizard ranges from 60 - 127 mm SVL

(Stebbins 2003). Its diet consists of insects (larvae, termites, grasshoppers, and

beetles), spiders, scorpions, and sometimes other lizards (Stebbins 2003) and it is

commonly found in sparsely vegetated habitats.

OBJECTIVES

This study aims to compare Anaho Island and the Pyramid Lake mainland under the predictions of the Island Rule. Following the predictions of Meiri (2007) and Meik et al. (2010), I hypothesize that snakes and lizards should be smaller on Ahano Island than 12 they are on the mainland, contrary to the size trends proposed by the Island Rule. I predict that that S. o. longipes and C. d. myurus will be smaller on Anaho Island, being small-bodied species among lizard taxa. I hypothesize that S. uniformis and A. t. tigris will trend towards smaller size or will not exhibit size divergence between island and mainland populations (average snout-to-vent length values for S. uniformis and A. t. tigris are less than the average SVL among 87 lizard populations of 40 species, 122 mm, calculated from supplemental material provided by Meiri 2007).

Research on Anaho Island has yet to address the relative impacts of selective forces on divergence between populations. Diet and predation pressure correlate with body-size divergence in island communities (Palkovacs 2003), and predictions that would result from either of these forces are tested as a means of examining whether either selective force exists. If predation pressure is acting as a selective force on Anaho Island, then I would expect to see differences in the frequencies of caudal autotomy between localities.

If diet is influencing lizards on Anaho Island, I expect a larger head size relative to body size in island lizards resulting from a broader dietary niche (Gravel et al. 2011).

Gape size is the selective target for size changes in snakes (Meik et al. 2010) and lizards

(Case and Schwaner 1993), and if fewer prey are available, lizards should have responded by increasing their gape size to make room for larger muscles capable of crushing hard-bodied prey items, expanding the number of potential prey items to include more invertebrates (Case and Schwaner 1993). If a switch has occurred from mammals to non-mammalian prey items, rattlesnakes should require smaller gapes and should have narrow head sizes (Meik et al. 2010). 13

This study examines body size of reptiles on Anaho Island and expands upon an unpublished study by Gienger et al. (2008). Where Gienger et al. (2008) was field-based, resulting in sample sizes that are restricted to what could be found by a limited number of researchers in a relatively short time period, this study reviews morphology by examining a large collection of museum specimens. The use of museum specimens allows for a review of body size divergence over multiple generations of collected specimens, rather than the shorter time period of a field study. In addition, this study examines males and females separately. This method was not used in Gienger et al. (2008), which might have introduced conflicting variation for species in which the sexes are dimorphic, particularly if sexual dimorphism is not at the same magnitude on the mainland and the island

(Forsman 1991). Lastly, this study increases the sample size within each species for body size comparisons, ensuring that the number of individuals examined in each species is sufficient to discern significant size trends. The analyses in this thesis will be used to answer the broader management question of whether Anaho Island hosts a reptile community that is distinct from the mainland.

MATERIALS AND METHODS

RESEARCH AREA

Preserved lizards (C. d. myurus, S. o. longipes, S. uniformis, and A. t. tigris) and snakes (C. o. lutosus) were located from Anaho Island and the vicinity of Pyramid Lake by searching through the HerpNet Database. This database catalogues all of the preserved specimens of the Class Reptilia available for researchers in the United States. The geographic cutoffs used to exclude specimens not proximate to Pyramid Lake were delineated arbitrarily, taking into consideration the boundaries of the Great Basin Desert.

Polygons for lizards and snakes (Figure 3) differed in size: the rattlesnake polygon was larger because rattlesnakes are predators that exist at a lower density than lizards and a larger shape polygon was needed to obtain similar sample sizes among lizards and snakes.

MEASUREMENT METHODS

Over 1,200 specimens were acquired from 5 museums (Appendix 1). Specimens were stored in 70% ethanol and were processed at the University of Nevada, Reno and at the Museum of Vertebrate Zoology in Berkley, CA. Size measurements were taken for each specimen using digital calipers and meter sticks. Snout-to-vent length

(SVL), which measures the snake or lizard from the tip of the nose to the start of the vent, was used as a measure of body size (Stebbins 2003). For snakes, individuals were uncoiled and pressed against an 18” wooden circle using a string to measure SVL. Head dimensions were taken which included (1) Head Width (HW): at the widest part of the head for C. o. lutosus; at the top of the tympanic membrane for lizard species, (2) Eye

Width (EW): at the widest part of the supraoculars for C. o. lutosus; at the posterior base 15 of the supraoculars on the outer edge for lizard species, (3) Head Length (HL): from the tip of the rostral scale to the far extent of the lower jaw bone, (4) Head Height (HH): not taken for C. o. lutosus; at the tallest part of the skull for lizards, (5) Eye Height (EH): from the top of the outer supraocular scale edge to the lower extent of the upper labials beneath the center of the eye, (6) Snout Width (SW): at the rostral scale located between the prefrontal and internasal scales in A. t. tigrus; at the nostrils for all other species (not measured in S. uniformis). These measurements are shown in Figure 4.

Approximately 200 specimens were added to the data set from data collected by

Gienger et al. (2008). These data include species, sex, locality, tail-regeneration, and

SVL information, used for the body size and predation pressure analyses. Sex was determined by the presence (male) or absence (female) of enlarged post-anal scales in lizards (Pietruszka 1981). For C. o. lutosus, sex was not discernible using external traits.

However, many of the snakes had been sexed by Glaudas et al. (2009), who provided the information needed.

In addition to recording museum of origin, species, individual identification number, SVL, sex, locality (island or mainland), and the head dimensions above, I examined specimens for tail damage. Tails were scored as damaged if the tail had regrown which is distinguished by a fracture plane, abnormal scale rows, abnormal coloration, or a different thickness on the regrown portion of the tail (Figure 5). Tails were scored as undamaged if they did not have any obvious abnormalities. Tails were not scored if the tail was not whole or with the specimen. For C. o. lutosus, tail length (from the vent to the last scale row) was measured because tail-length relative to body length 16 differs for males and females and can be used with some consistency to predict the sex of a specimen (Klauber 1956).

DATA ANALYSIS

Only adults were included in this study. The smallest SVL values at sexual maturity were taken from the literature for each species. In cases where more than one study reported a minimum SVL value, the shortest reported SVL was used. This excluded

C. d. myurus males less than 67 mm and females less than 63 mm (Pianka and Parker

1972); S. uniformis males less than 89 mm and females less than 81 mm (Tanner and

Krogh 1973); S. o. longipes males less than 55 mm and females less than 59 mm

(Goldberg 1974); and A. t. tigris males less than 70 mm and females less than 63 mm

(Parker 1972).

Body Size

Body size distribution was compared for each locality and each species using

SVL values. For C. o. lutosus, unknown sexes were assigned as male or female based on the following process: SVL/tail-length ratios were calculated for 43 known females, 88 known males, and 29 unknown sexes. Individuals were arranged along a continuum of low (male) to high (female) SVL/tail-length ratios. Along the continuum, a cutoff point was established at 13.82 mm (93% of females were larger than this value so unknowns smaller than 13.82 mm were assigned as male) and 14.5 mm (93% of males were smaller than this value so unknowns larger than 13.82 mm were assigned as female). Then, a cutoff value of 14.16 mm was established as the average of the two prior cutoff values with remaining unknowns above and below this value being assigned as female and male, 17 respectively. This left a final sex ratio of 0.57, which was not statistically different

(proportion test) from the original ratio of known males to females (P = 0.6263).

Each locality sample was checked for normality visually with a frequency histogram and statistically with an F-test. Before performing a Student’s T-test (tests for significant difference in means between samples), an F-test was used to find out whether the variances were equal or unequal between two samples. If unequal, a Student’s T-test for Unequal Variances was performed instead of a Student’s T-test for Equal Variances.

Data were compiled in Excel (2011) and analyzed in R (RDCT 2011).

When comparing SVL between island and mainland species, sexes were treated independently to control for sexual-size dimorphism (Forsman 1991) except for S. o longipes. In this species, a T-test of SVL between males and females from similar localities found no significant difference; island and mainland body size was compared with sexes pooled. For every other species, a T-test determined that body size varied significantly between the sexes and data were not pooled between the sexes.

Tail-Regeneration

Within each locality, the frequency of tail-regeneration for each species was calculated. Data were compiled in Excel (2011) and analyzed in R (RDCT 2011). The proportion of tail-regeneration within the population between females and males was compared first with a Fisher’s Exact Test and a proportion’s test. If regeneration proportions were significantly different (P-value ≤ 0.05) in either test, males and females were analyses separately. After examining differences between sexes, I conducted a final

Fisher’s Exact Test and proportion’s test to compare regeneration frequencies for each 18 species between the island and mainland. The null expectation is that regeneration frequencies will not vary between locations.

Head Size

All morphometric data were z-transformed with sexes and species separated and localities pooled. This transformation standardizes quantitative data by converting it into multiples of standard deviations around the mean of 0, which allows measurements with varying standard deviation sizes to be compared together (Zar 1999). To determine whether head proportions varied between Anaho Island and Pyramid Lake populations, two Multivariate Analysis of Variance (MANOVA) tests were performed for each sex using SAS version 9.2 (SAS 2008). The first was termed a “simple” MANOVA with the dependent variables: HL, HW, EW, HH, EH, and SW (except for SW in S. uniformis) as a function of the independent variable location (Anaho or Pyramid). A second, called a

“complex” MANOVA was performed that modeled the dependent variables: HL, HW,

EW, HH, EH, and SW (excluding SW for S. uniformis and including tail-length (TL) for

C. o. lutosus), and compared samples as a function of the independent variables location,

SVL, and the interaction between location and SVL (location*SVL). This approach standardizes each head variable by the body length (SVL) of an individual, and therefore adjusts for body size.

The null expectation is that Anaho and Mainland species will show no significant difference (P > 0.05) in the dependent variable when examining the location or the location*SVL independent variables, and that samples will always show significant differences when examining the SVL independent variable. If the P-value is significant for the Anaho variable, then the mean of the dependent variable differs as a function of 19 the location. If the P-value for Anaho*SVL is significant, then there is a relationship between SVL and the head shape variable that differs between the island and mainland. If the P-value for SVL is significant, then the dependent variable varies with body size, which is expected for all individuals and head size measures should show a positive correlation with body size measures.

RESULTS

BODY SIZE

Average body size was smaller for Anaho Island males and females of A. t. tigris

(Figure 6) and C. o. lutsus (Figure 7), and males but not females of C. d. myurus. Male mean body size estimates for Anaho and Pyramid were 588.42 and 766.75, 79.00 and

83.87, and 76.50 and 81.20 respectively for C. o. lutsus, A. t. tigris, and C. d myurus.

Female mean body size estimates for Anaho and Pyramid were 559.35 and 674.64, and

75.77 and 82.39 respectively for C. o. lutsus, and A. t. tigris. S. o. longipes and S. uniformis did not differ in body size between locations. Males were larger than females for both locations for all species, except for S. o. longipes in which the sexes were not statically different (Table 1).

TAIL-REGENERATION FREQUENCY

Tail-regeneration frequencies are shown in Table 2. The regeneration frequency in each species was 0.19, 0.30, 0.38, and 0.26 for C. d. myurus, A. t. tigris, S. uniformis, and S. o. longipes, respectively. When separated into regeneration frequencies for Anaho

Island and for Pyramid Lake, frequencies are 0.09 and 0.21, 0.25 and 0.31, 0.27 and 0.44,

0.21 and 0.27 for C. d. myurus, A. t. tigris, S. uniformis, and S. o longipes, respectively.

In all species, tail-regeneration frequencies are lower on Anaho Island than on Pyramid

Lake but not significantly so in most species (P > 0.05, Table 3).

There was a trend between tail-regeneration frequency and sex: males have higher frequencies than females in six of eight comparisons between the two locations for four species (Table 2). These differences, however, are only significant for S. uniformis from 21

Pyramid Lake (P = 0.0263, proportion test) and nearly significant for A. t. tigris from

Anaho Island (P = 0.053, proportion test).

HEAD SIZE

Head dimensions in the simple MANOVA models show a significant difference when comparing localities (Wilks' Lambda Test P-value < 0.05) for all species and sexes examined, except for male (P = 0.11) and female (P = 0.59) S. o. longipes and male (P =

0.14) and female (P = 0.34) S. uniformis. Complex MANOVA models showed significant differences for shape variables between locations for A. t. tigris females, S. uniformis males, and C. d. myurus males and females; with SVL for all sexes of all species; and with the interaction of SVL and location for C. o. lutosus males and A. t. tigris males.

The majority of head variables showed no discernible direction of trend (larger or smaller size in Anaho individuals relative to Pyramid individuals, Table 4). In A. t. tigris, it is notable that all head shape variables show a trend towards decreased size in Anaho specimens. In females, HL, HW, EW and HH were significantly different (P < 0.05), SW showed a strong trend (0.06 < P < 0.15), and EW showed a trend (0.16 < P < 0.49). In males, HL, SW, EW, EH, and HH show a trend for decreased size, while HW shows a strong trend for decreased size. Another interesting result is that EH and HH decrease for all species that show a trend. In C. d. myurus, EW and HW increase for both sexes

(significantly for HW in females).

DISCUSSION

BODY SIZE

These results do not support the Island Rule predictions that smaller animals grow larger to monopolize resources and enhance metabolic efficiency, while larger animals grow smaller to reduce resource requirements and increase reproduction (Meiri et al.

2008). No trend is evident in S. uniformis or S. occidentalis, while C. o. lutosus, C. d. myurus (males), and A. t. tigris become smaller on the island, in agreement with the original research hypothesis that rattlesnakes and lizards will exhibit dwarfism on islands.

As other researchers have also concluded, the generality of the Island Rule does not apply to reptiles as well as it does in other taxa (Meiri et al. 2011). However, the explanation for non-conformity of lizards with the Island Rule remains unclear.

This study supports the conclusion that the Island Rule is not a rule, but rather an artifact of comparing relatively unrelated groups that show finer-scale (i.e. genus, family, or order level) patterns when responding to insularity (Meiri 2007, 2008; Meiri et al.

2004, 2006, 2008, 2011; Raia et al. 2010; but see Lomolino 2005). As with selection in non-island environments, taxa-specific adaptations are more likely to result from the interplay of an organism’s biology and the particular abiotic factors at play, rather than universal patterns like the Island Rule.

TAIL-REGENERATION

Tail-regeneration frequencies were not significantly different between localities for all species; however, males of S. uniformis and A. t. tigris did show significantly higher regeneration frequencies on the mainland. For these species, differences in the frequencies of caudal autotomy support the hypothesis that the ecology of predation 23 differs between locations. Additional support is provided by the fact that all species trend towards lower regeneration frequencies on the island (providing evidence for an adaptive change rather than a result of genetic drift). This suggests that predation pressure might be less on the island; however, a causal explanation for regeneration frequency should not be identified without additional information on predator-prey dynamics.

One challenge in interpreting these results is that this test can only provide indirect support for the hypothesis. A difference in tail-regeneration frequencies, as an indirect measure of predation, does not explicitly identify if predation itself differs.

Other interpretations such as competition cannot be ruled out. This test does not conclusively refute the null hypothesis that predation does not differ between islands; it only identifies that predation is a possible factor influencing body size. A more detailed study that examined latency to shed a tail and predator efficiency and intensity would allow for more concrete conclusions regarding the strength of predation as a selective force for body size (Bateman and Fleming 2009). More individuals should be examined to determine if the trend towards lower regeneration frequencies among all species is significant or a result of small sample size.

Interestingly, mainland S. uniformis and island A. t. tigris differed in tail- regeneration frequencies between males and females. Most studies suggest no difference between males and females in tail-regeneration frequencies (Vinegar 1975; Lin et al.

2006; but see Vitt 1981). A possible interpretation is that males, as the more visible sex, have higher tail-regeneration frequencies because they are more-frequently the target of predation attempts. A higher degree of intraspecific competition and aggression in males could also lead to these results, and a more detailed study of competition in island males 24 might yield interesting results regarding the influence of competition on tail regeneration frequency and the potential for competition to influence body size in aggressive males

(Palkovacs 2003).

HEAD-SIZE

There were few discernible patterns in head shape variables between locations, with the exception of two patterns that deserve further consideration. A. t. tigris is smaller on Anaho Island for both sexes for all examined head shape variables, even after accounting for its smaller body size on Anaho Island (location MANOVA model). A smaller head size in A. t. tigris contradicts my prediction that head size should increase on Anaho Island. This species should be examined for differences in diet and resource selection between the island and mainland such as specialization on a new prey type, as head size and bite force relate to the potential prey spectrum of a lizard (Herrel et al.

2001). Genetic drift and founding effects are other possible interpretations: founding individuals of this species could have been smaller-headed, or a higher percentage of small-headed lizards might have experienced increased reproductive success as the result of another trait.

The second trend is that for all species examined, HH was smaller (except when no trend was evident) although reduced height was only statistically significant in A. t. tigris and C. d. myurus. EH was not a consistent variable, as many specimens exhibited shrunken tissue to varying degree around the eye. HH, however, was measured with consistent landmarks across specimens. It would be interesting to examine whether HH correlates with any adaptation for processing or acquiring prey.

FUTURE DIRECTIONS

My evidence supports the conclusion that isolation or insularity of a population does not result in a universal pattern of size evolution (Meiri et al. 2008). While I do not suggest refuting all large scale patterns in body size evolution (such as the influence of island size and distance from the mainland on the magnitude of body size change), I do suggest a stronger consideration for the influence of site-specific selective influences such as predation, resource abundance, and competition.

A study of the selective target of predation pressure would be an exciting avenue for future analysis. Selection might not act directly on body size (i.e. predators preferentially choosing one size extreme) but indirectly by altering mortality rates and life-history traits such as age and size of individuals at maturity (Palkovacs 2003).

In C. o. lutosus, future studies of genetic as well as morphologic variation would provide more concrete evidence of differentiation between island and mainland populations. Any additional studies should attempt to determine how frequently new colonists or migrants arrive to the island as a way to determine the actual degree of isolation for rattlesnakes and other species. Behavioral trials to evaluate aggressive behavior could be used to infer predation pressure for island rattlesnakes.

MANAGEMENT IMPLICATIONS

This study demonstrates that Anaho Island harbors a community of reptiles that is distinct from the mainland in morphology and possibly in ecology and life-history evolution. Diversity in form has accumulated relatively quickly in the 10,000 years since the formation of Anaho Island, and the evolutionary history and potential of this island population should be considered in the development of management goals. The Anaho 26

Island community is of particular interest in light of changing climate conditions (e.g. precipitation, temperature) which might threaten water levels in Pyramid Lake, in conjunction with increasing demands for water from the growing Reno urban area.

(Murphy and Tracy 2005). If water levels decrease substantially, a land bridge could result between the island and the lake shore, reestablishing gene flow between previously isolated lizard populations.

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TABLES AND FIGURES

Table 1. Results from a Student’s T-test comparing body size between mainland and island individuals of the same sex and species. Average body size (SVL) on Anaho Island relative to Pyramid Lake is significantly different (bolded if P < 0.05) when mean body size of N individuals of differs between locations. Mean Body Size2 Species Sex P-value Anaho Anaho N Pyramid N (α=0.05) Trend3 C. d. myurus ♂ 76.50 14 81.20 25 0.0023 ↓ C. d. myurus ♀ 72.06 16 72.70 179 0.5835 — S. o. longipes ♂♀1 76.45 29 74.01 209 0.1217 — S. uniformis ♂ 96.27 37 97.43 51 0.2291 — S. uniformis ♀ 90.43 7 89.36 39 0.5440 — A. t. tigris ♂ 79.00 16 83.87 89 0.0003 ↓ A. t. tigris ♀ 75.77 22 82.39 70 0.0007 ↓ C. o. lutosus ♂ 588.42 38 766.75 53 0.0000 ↓ C. o. lutosus ♀ 559.35 20 674.64 25 0.0000 ↓ 1 Sexes are pooled in S. o. longipes because a Student's T-test found no significant difference in body size between sexes; in all other species, sexes (male ♂, and female ♀,) were significantly different. 2 N = sample size. 3 Arrows show smaller (↓) or larger (↑) mean body size in island relative to mainland specimens, except when the trend is insignificant (—).

Table 2. Overall tail-regeneration frequencies, separated by species for the sexes of either location. Tail- Subsample1 Species N2 Regeneration Sex Location Frequency S. uniformis ♂ A 37 0.27 ♀ A 7 0.29 ♂ P 49 0.55 ♀ P 38 0.29 S . o. longipes ♂ A 23 0.23 ♀ A 6 0.17 ♂ P 119 0.29 ♀ P 70 0.22 A . t. tigris ♂ A 16 0.06 ♀ A 20 0.40 ♂ P 86 0.36 ♀ P 63 0.24 C . d. myurus ♂ A 15 0.13 ♀ A 16 0.06 ♂ P 116 0.23 ♀ P 69 0.17 1 Abbreviations: Anaho Island (A) and Pyramid Lake (P) for either Males (♂) or Females (♀). 2 N indicates sample size, the number of individuals examined for each subsample.

Table 3. Results from proportion tests and Fisher’s exact tests for pair-wise comparisons of locality and sex groups. Species1 Regeneration Frequency Test P-Value Comparison2 Fishers Exact Proportion3 S. uniformis P♂ P♀ 0.16 0.03 A♂ A♀ 1.00 1.00 P♂ A♂ 0.11 0.02 P♀ A♀ 1.00 1.00 S. o. longipes P♂ P♀ 0.62 0.49 A♂ A♀ 1.00 1.00 P♂ A♂ 0.80 0.68 P♀ A♀ 1.00 1.00 A. t. tigris P♂ P♀ 0.30 0.16 A♂ A♀ 0.12 0.05 P♂ A♂ 0.07 0.04 P♀ A♀ 0.30 0.26 C. d. myurus P♂ P♀ 0.47 0.45 A♂ A♀ 1.00 0.95 P♂ A♂ 0.74 0.59 P♀ A♀ 0.46 0.47 1 Tests are performed intrapecifically, not interspecifically. 2 Abbreviations: Anaho Island (A) and Pyramid Lake (P) for either Males (♂) or Females (♀). 3 Significantly different tail-regeneration frequencies (P < 0.05) are bolded.

Table 4. Arrows show whether the “complex” MANOVA returned different proportions of head size relative to body size (using the independent variable location) between locations and independently for males (♂) and females (♀). Arrows indicate a trend towards smaller (down) or larger (up) variable size on Anaho Island relative to the Pyramid Lake mainland.

Dependent C. o. lutosus A. t. tigris S. o. longipes S. uniformis C. d. myurus Variable ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ ♂ ♀ 1 Length — — ↓ ↓ — ↑ ↑ — ↓ — Snout ↓ ↑ ↓ ↓ ↑ — — — ↑ — Eye Width ↑ — ↓ ↓ ↓ ↑ ↑ — ↑ ↑ Head Width — — ↓ ↓ — — ↑ — ↑ ↑ Eye Height ↓ ↓ ↓ ↓ ↓ — — — ↓ ↓ Head Height — — ↓ ↓ — — ↓ — ↓ ↓ Tail Length — ↓ — — — — — — — — 1 —: Variable not estimated or P-values greater than .50; black arrow indicates a trend in variable length with a P–value between 0.49 and 0.16; orange arrow indicates a strong trend in variable length with a P–value between 0.15 and 0.06; red arrow indicates a significant trend in variable length on Anaho relative to the mainland with a P–value between 0.05 and 0.00.

Figure 1. Map of the Truckee River drainage basin and location of Pyramid Lake Indian Reservation1.

Anaho Island

1 Truckee river map. Waterwired [Internet] [cited 2012 April 29]. Available from http://aquadoc.typepad.com/.a/6a00d8341bf80a53ef00e554ecbc978833-320wi.

Figure 2. USGS topographic map of Anaho Island1 (top) and horizontal view of Anaho Island (bottom, from Benson 20042) showing terraces when the lake level was 1,265 m (DT), 1,207 m (ET), and approximately 1,200 m (MT).

2000 ft.

1 The USGS store: map locator and downloader [Internet] [cited 2012 April 29]. Available from http://store.usgs.gov/b2c_usgs/usgs/maplocator/%28ctype=areaDetails&xcm=r3standards tanda_prd&carea=%24ROOT&layout=6_1_61_48&uiarea=2%29/.do. 2 Benson LV. 2004. The tufas of Pyramid Lake, Nevada. U.S. Geological Survey Circular 1267. 14 p. 40

Figure 3. Satellite image showing the geographic restrictions used to set the boundary for specimen collection locations, orange1. Left: C. o. lutosus. Right: Other squamates.

1 Herpnet [Internet] [cited 2012 April 29]. Available from http://www.herpnet2.org/search.aspx.

Figure 4. Illustrations modified from Powell et al. 20121 (Figures 140, 232, 244, and 176) showing the landmarks used for head measurements.

1 Powell R, Collins JT, Hooper ED. 2012. Key to the herpetofauna of the continental United States and Canada. 2nd ed. Lawrence (KS): University Press of Kansas. 160 p.

Figure 5. Photographs of a normal (left) and regenerated (right) tail. Landmarks used to determine whether or not tail had been regenerated are identified including the fracture plane, normal scale rows, abnormal scale rows, and the original tail.

Original Tail

Fracture

Plane

Normal Regrown Scale Rows Tail

Abnormal Scale Rows

Normal Tail Regenerated Tail

Figure 6. Body size frequency histogram (generated in Excel) for both male and female A. t. tigris. Mean body size differs between Anaho and Mainland samples.

Body Size Frequency Histogram: A. t. tigris

20 18 16

14 12 10

8 FrequencyAnaho Frequency 6 FrequencyMainland 4 2

40 46 52 58 64 70 76 82 88 94

136 100 106 112 118 124 130 142 148 SVL, mm

Figure 7. Body size frequency histogram for both male and female C. o. lutosus. Mean body size differs between Anaho and Mainland samples. Body Size Frequency Histogram: C. o. lutosus

4 FrequencyAnaho FrequencyMainland

3 Frequency 2

620 932 500 524 548 572 596 644 668 692 716 740 764 788 812 836 860 884 908 956 SVL, mm

APPENDIX 1 MUSEUM SPECIMENS

Data were obtained from records held in the following institutions and accessed through the HerpNET data portal (http://www.herpnet.org) in December, 2011: California Academy of Sciences [CAS], San Francisco, CA; Museum of Vertebrate Zoology [MVZ], University of California, Berkeley, CA; University of Kansas Biodiversity Institute [KU], Lawrence, KS; San Diego Natural History Museum [SDNHM], San Diego, CA.

1. CAS: C. d. myurus: 7318 7319 7320 7321 7322 7323 21450 21451 21452 21453 21454 21455 21456 21457 21458 21459 21460 21461 21462 21463 21464 21465 21466 21467 21468 21469 21470 21471 21472 21474 21475 21476 21477 21478 21479 21480 21481 21482 21483 21600 21601 21602 21603 21604 21605 21606 21607 40596 40597 40598 40599 40600 40601 40602 40603 40604 40605 40606 40607 40608 40609 40610 40611 40612 40613 40614 40615 40616 40617 40618 40619 40620 40621 40623 40624 40625 40626 40627 40628 40629 40631 40632 40633 40635 40637 40638 40639 40640 40642 40643 40645 40646 40648 40649 40650 40652 40653 40654 40657 40658 40659 40660 40661 40662 40663 40664 40665 40666 40667 40668 40669 40670 40671 40672 40673 40674 40675 40676 40677 40678 40679 40680 40681 40682 40683 40684 40685 40686 40687 40688 40689 40690 40691 40692 40693 40694 40695 40696 40697 40698 40699 40700 40701 40703 40704 40705 40706 40709 40710 40711 40712 40714 40716 40719 40720 40721 40722 40723 40724 40726 40727 40728 40729 40730 40731 40732 40733 40734 40735 40736 40737 40738 40739 40740 40741 40742 40743 40744 40745 40746 40747 40748 40749 40750 40751 40752 40753 40754 40755 40756 40757 40758 40759 40760 40761 40762 40763 40764 40765 40766 40767 40768 40769 40770 40771 40772 40773 40774 40775 40777 40778 40779 40780 40781 40782 40783 40784 40785 40786 40877

C. o. lutosus: 7862 7865 7869 7876 15961 21620 21621 21622 21625 21626 21627 21628 21629 21632 21634 21636 21641 21645 36629 36630 36632 36633 36636 36637 36646 36647 36652 36653 39041 39252 39269 39593 69599 78073 84516 93787 98551

A. t. tigris: 5830 6346 6347 6348 6351 6352 6353 6354 6355 6356 6357 6358 6359 6360 6361 6362 6363 6364 6365 6366 6367 6368 6369 6370 6371 7133 7134 7136 7137 7138 7139 7140 7141 7142 7300 7309 7944 7945 7946 8054 8055 8056 8057 11240 11241 19210 19912 21577 21578 21579 21580 21581 21582 21583 21584 21585 21586 21587 21588 21589 21590 21591 21592 21593 21594 21595 21596 21609 22139 40536 40537 40538 40539 40540 40541 40542 40543 40544 40545 40546 40547 40548 40549 40550 40551 40552 40553 40554 40555 40556 40557 40558 40559 40560 40561 40562 40563 40564 40565 40566 40567 40568 40569 40570 40571 40572 40573 40574 46

40575 40576 40577 40578 40579 40580 40581 40582 40583 40584 40585 40586 40587 40588 40589 40590 40591 40592 40593 40594 40595 195829 223552 223553

S. uniformis: 5874 5876 5877 5880 5881 5886 5887 5888 5889 5890 5892 6282 6292 7306 8031 8032 17305 17306 17307 17308 17309 19911 19913 21512 21513 21517 21518 21519 21520 21521 21522 21523 21524 21525 21526 21527 21528 21529 21530 21531 21532 21533 21534 21535 21536 21537 21538 21539 21540 21541 21542 21543 21544 22118 22121 23362 23368 40799 40800 40801 40802 40803 40804 40805 40806 40807 40808 40809 40810 40811 40812 40813 40814 40815 40816 40818 40819 40820 40821 40876 44152 44153 44154 120805 189667 189668 189669 189670 189671 189672 189674 189675 189676 189677 189678 189679 189680 198673 227929

S. o. longipes: 6265 6266 6267 6268 6269 6270 6271 6272 6274 6276 6277 6278 6279 6280 6281 6287 6288 6289 6290 6298 8058 8059 8060 8061 8062 8063 11212 11213 12470 17310 17311 17312 17313 22108 23356 23357 23358 23359 23360 23361 23363 23364 23365 23366 23367 23369 23370 38024 38025 38026 38027 38028 38029 38030 39648 39649 39650 39651 40822 40823 40824 40825 40826 40827 40828 40829 40830 40831 40832 40833 40834 40835 40836 40837 40838 40839 40840 40841 40842 40843 40844 40845 40846 40847 40848 40849 40850 40851 40852 40853 40854 40855 40856 40857 40858 40859 40860 40861 40862 40863 40864 40865 40875 44155 44156 120801 120802 120803 120804 132406 132407 132408 189453 189454 189455 189456 189457 189458 189459 189460 189461 202940 202941 202945 202946 202947 202948 202949 202956 202958 202959 202960 202961 202962 202975 229261 247438 249482 249483 249488

2. KU: C. o. lutosus: 43743 201282 202966

3. MVZ: C. d. myurus: 14391 14392 14393 14394 14395 14396 14397 14398 14399 14400 14401 14402 14403 14404 14405 14406 14407 14408 14409 14410 14411 14412 14413 14414 14415 14416 14417 14418 14419 14420 14421 14422 14423 14424 15936 15937 15943 15944 15945 15946 15947 15948 15949 16642 16643 16644 16645 16646 16647 16648 16649 16650 16651 16652 16653 16654 16655 16656 16657 16658 16660 16661 16662 16663 16664 16665 16667 16668 16669 19945 19946 19947 19948 21447 24455 29319 36347 36368 39172 40490 40605 40606 40607 40608 40609 40610 63459 63460 77821 77822 77823 77824 77825 77826

C. o. lutosus: 7867 21624 21631 36373 36645 36648 64210 81791 202955

A. t. tigris: 11340 14427 14428 14429 16679 16680 16681 16682 18457 18458 20353 20354 20355 20357 20358 20360 20361 20362 20363 20364 20366 20367 20369 20370 47

20371 20372 20373 20374 20375 20376 20377 20378 20477 20478 20620 20621 21490 21491 21492 21493 21494 21495 21496 21497 21498 21499 21500 21501 21502 21503 21504 21505 24549 24550 24551 24552 24553 24554 24555 24556 24557 24558 24559 24560 36089 36090 36091 36092 36093 36094 36095 36096 36097 36098 36099 36100 36123 36134 40497 40498 40499 40500 40501 40502 40503 40504 40505 40506 40507 40508 40509 40510 40511 40512 40615 40616 40617 40618 40619 42079 162360 162361 187587 228226

S. uniformis: 14364 14425 14426 15955 16677 20080 20081 20082 20083 20084 20085 23714 24484 29325 32076 32077 32078 32079 32080 32081 32083 32084 32085 35990 35994 40492 40493 40494 40495 40496 40612 40613 40614 42078 77839 162077 162078 180308 180309 180310 187512 228018

S. o. longipes: 7528 7529 7530 7531 7532 11175 11179 11181 12806 12810 12811 12812 12813 14656 14657 14658 14659 14660 14661 14662 14663 14664 14665 14666 14667 14924 14925 14926 15956 17101 17102 17112 17114 20471 21458 21465 24491 24492 24493 24494 24495 24496 25209 36035 36036 36037 36038 36039 36040 36355 36356 36357 36372 36373 36374 50956 50957 51680 51681 51682 51684 51686 51690 51691 51692 51694 51696 51697 51699 51700 75820 77851 77852 77853 77854 77855 77856 77857 77858 77859 77860 77861 116661 210303 210304 210305 210307 229066 229067 233482 252086 252087 252088 252089 252090 252092 252093 252094 252095 252096 252097 252098 252099 252100 252101 252102 252103 252104 252105 252106 252107 252108 252109 252110 252111 252112 252113 252114 252115

4. SDNHM: C. d. myurus: 36383 36384 36684 36685 36686 38678 38679 38680 38681 38682

C. o. lutosus: 7861 7866 7868 7870 7875 11363 20646 21630 21633 21639 21642 21643 22791 31859 31860 31861 36151 36371 36372 36374 36375 36447 36627 36634 36638 36639 36642 36643 36644 36650 36651 36654 36655 37990 38374 38375 38376 39042 39060 39064 39245 39248 39271 39273 64209 91624 92263 93788 93792 202965 202974

A. t. tigris: 38693 38694 38695

S. uniformis: 27811 27812 27813 36378 36379 36380 36381 38326 38327 38683 38684 38685 38686

S. o. longipes: 27815 28915 28916 28917 28918 28919 28920 28921 28922 36382

5. UNR: C. d. myurus: 7740 7741 7742 7743 7744 7745 7746 7747 7748 7749 7750 7751 7752 7753 7754 7755 7756 7757 7758 7759 7760 7761 7762 7763 7764 Gienger et al. 2008: CADR-11 CADR-12 CADR-13 CADR-14 CADR-15 CADR-21 CADR-22 CADR-23 CADR-24 CADR-25 CADR-31 CADR-32 CADR-33 CADR-34 CADR-35 CADR-41 CADR-42 CADR-43 CADR-44 CADR-45 CADR-51 CADR-52 CADRB-10 CADRB-11 CADRB-12 CADRB-3 CADRB-4 CADRB-5

C. o. lutosus: 5050 6542 7234 7797 7863 7864 7871 7872 7873 7874 17133 21619 21623 21637 21638 21640 36628 36631 36635 36640 36641 36649 38696 38966 38969 39246 39253 39270 39272 39587 43393 69600 69601 93785 202967 Gienger et al. 2008: CRLU-8 CRLU-9 CRLU-13 CRLU-17 CRLU-19 CRLU-21 CRLU-22 CRLU-23 CRLU-24 CRLU-25 CRLU-26 CRLU-28 CRLU-29 CRLU-30 CRLU-31

A. t. tigris: 7765 7766 7767 7768 7769 7770 7771 7772 7773 7774 7775 7776 7777

S. uniformis: 7813 7814 7815 7816 7817 7819 7820 7821 7822 7823 7824 7825 7826 7827 7828 7829 7830 7831 7832 7833 7834 7835 7836 7837 7839 7840 7841 7842 Gienger et al. 2008: SCMA-11 SCMA-111 SCMA-112 SCMA-113 SCMA-114 SCMA-115 SCMA-12 SCMA-121 SCMA-122 SCMA-123 SCMA-124 SCMA-125 SCMA-13 SCMA-131 SCMA-132 SCMA-133 SCMA-134 SCMA-135 SCMA-14 SCMA-141 SCMA-142 SCMA-143 SCMA-144 SCMA-145 SCMA-15 SCMA-151 SCMA-152 SCMA-153 SCMA-154 SCMA-155 SCMA-21 SCMA-211 SCMA-212 SCMA-213 SCMA-214 SCMA-215 SCMA-22 SCMA-221 SCMA-222 SCMA-223 SCMA-224 SCMA-225 SCMA-23 SCMA-231 SCMA-232 SCMA-233 SCMA-234 SCMA-235 SCMA-24 SCMA-241 SCMA-242 SCMA-243 SCMA-244 SCMA-245 SCMA-25 SCMA-251 SCMA-252 SCMA-253 SCMA-254 SCMA-255 SCMA-301 SCMA-302 SCMA-302b SCMA-303 SCMA-304 SCMA-305 SCMA-31 SCMA-310 SCMA-311 SCMA-312 SCMA-313 SCMA-314 SCMA-315 SCMA-32 SCMA-320 SCMA-321 SCMA-322 SCMA-323 SCMA-324 SCMA-325 SCMA-33 SCMA-34 SCMA-35 SCMA-41 SCMA-42 SCMA-43 SCMA-44 SCMA-45

S. o. longipes: 7779 7780 7781 7782 7783 7784 7785 7786 7787 7788 7789 7790 7791 7792 7793 7794 7795 7796 7838 Gienger et al. 2008: 49

SCOC-003 SCOC-11 SCOC-111 SCOC-112 SCOC-113 SCOC-114 SCOC-115 SCOC-120 SCOC-121 SCOC-122 SCOC-123 SCOC-124 SCOC-125 SCOC-126 SCOC-127 SCOC-128 SCOC-21 SCOC-22 SCOC-23 SCOC-24 SCOC-25 SCOC-31 SCOC-32 SCOC-33 SCOC-34 SCOC-35 SCOC-41 SCOC-42 SCOC-43 SCOC-44 SCOC-45