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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
by
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
RENO
THE HONORS PROGRAM
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
3i
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.
4ii
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.
5iii
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
6iv
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
7v
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
8vi
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
1
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.
14
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.
20
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).
22
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 tailregeneration 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.
25
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.
27
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100:47-64.
Stebbins RC. 2003. Peterson field guide to western reptiles and amphibians. 3rd ed. New
York (NY): Houghton Mifflin. 560 p.
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American Naturalist 112:545-555.
Tanner WW, Krogh JE. 1973. Ecology of Sceloporus magister at the Nevada test site,
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Truckee river map. Waterwired [Internet] [cited 2012 April 29]. Available from
http://aquadoc.typepad.com/.a/6a00d8341bf80a53ef00e554ecbc978833-320wi
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from
http://store.usgs.gov/b2c_usgs/usgs/maplocator/%28ctype=areaDetails&xcm=r3st
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33
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p.
34
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.
Species
Sex
C. d. myurus
C. d. myurus
S. o. longipes
S. uniformis
S. uniformis
A. t. tigris
A. t. tigris
C. o. lutosus
C. o. lutosus
♂
♀
1
Anaho
76.50
72.06
76.45
96.27
90.43
79.00
75.77
588.42
559.35
Mean Body Size2
N
Pyramid
14
81.20
16
72.70
29
74.01
37
97.43
7
89.36
16
83.87
22
82.39
38
766.75
20
674.64
N
25
179
209
51
39
89
70
53
25
P-value
(α=0.05)
0.0023
0.5835
0.1217
0.2291
0.5440
0.0003
0.0007
0.0000
0.0000
Anaho
Trend3
↓
—
—
—
—
↓
↓
↓
↓
♂♀
♂
♀
♂
♀
♂
♀
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 (—).
35
Table 2. Overall tail-regeneration frequencies, separated by species for the sexes of either
location.
Species
Subsample1
Sex
Location
A
A
P
P
A
A
P
P
A
A
P
P
A
A
P
P
2
N
TailRegeneration
Frequency
0.27
0.29
0.55
0.29
0.23
0.17
0.29
0.22
0.06
0.40
0.36
0.24
0.13
0.06
0.23
0.17
37
♂
7
♀
49
♂
38
♀
S. o. longipes
23
♂
6
♀
119
♂
70
♀
A. t. tigris
16
♂
20
♀
86
♂
63
♀
C. d. myurus
15
♂
16
♀
116
♂
69
♀
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.
S. uniformis
36
Table 3. Results from proportion tests and Fisher’s exact tests for pair-wise comparisons
of locality and sex groups.
Species1
S. uniformis
S. o. longipes
A. t. tigris
C. d. myurus
1
Regeneration Frequency
Comparison2
P♂
P♀
A♂
A♀
P♂
A♂
P♀
A♀
P♂
P♀
A♂
A♀
P♂
A♂
P♀
A♀
P♂
P♀
A♂
A♀
P♂
A♂
P♀
A♀
P♂
P♀
A♂
A♀
P♂
A♂
P♀
A♀
Test P-Value
Fishers Exact
Proportion3
0.16
0.03
1.00
1.00
0.11
0.02
1.00
1.00
0.62
0.49
1.00
1.00
0.80
0.68
1.00
1.00
0.30
0.16
0.12
0.05
0.07
0.04
0.30
0.26
0.47
0.45
1.00
0.95
0.74
0.59
0.46
0.47
Tests are performed intrapecifically, not interspecifically.
Abbreviations: Anaho Island (A) and Pyramid Lake (P) for either Males (♂) or Females (♀).
3
Significantly different tail-regeneration frequencies (P < 0.05) are bolded.
2
37
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
Variable
Length
Snout
Eye Width
Head Width
Eye Height
Head Height
C. o. lutosus
♂
♀
A. t. tigris
♂
♀
S. o. longipes
♂
♀
S. uniformis
♂
♀
C. d. myurus
♂
♀
—1
↓
↑
—
↓
—
—
↓
↓
↓
↓
↓
↓
—
—
↑
↓
—
↓
—
—
↑
—
↑
↑
—
↓
—
↓
↑
↑
↑
↓
↓
—
—
↑
—
—
↓
—
↓
↓
↓
↓
↓
↓
↓
—
↑
—
↑
—
—
—
—
—
—
—
—
—
—
—
—
—
↑
↑
↓
↓
—
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.
38
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.
39
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.
41
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.
42
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
Scale Rows
Regrown
Tail
Abnormal
Scale Rows
Normal Tail
Regenerated
Tail
43
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.
20
18
16
14
12
10
8
6
4
2
0
Frequency
Anaho
SVL, mm
148
142
136
130
124
118
112
106
100
94
88
82
76
70
64
58
52
46
Frequency
Mainland
40
Frequency
Body Size Frequency Histogram: A. t. tigris
44
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
7
6
Frequency
Anaho
4
Mainland
Frequency
3
2
1
SVL, mm
956
932
908
884
860
836
812
788
764
740
716
692
668
644
620
596
572
548
524
0
500
Frequency
5
45
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
21456
21468
21481
40597
40609
40621
40637
40653
40667
40679
40691
40704
40722
40735
40747
40759
40771
40784
7319
21457
21469
21482
40598
40610
40623
40638
40654
40668
40680
40692
40705
40723
40736
40748
40760
40772
40785
7320
21458
21470
21483
40599
40611
40624
40639
40657
40669
40681
40693
40706
40724
40737
40749
40761
40773
40786
7321
21459
21471
21600
40600
40612
40625
40640
40658
40670
40682
40694
40709
40726
40738
40750
40762
40774
40877
7322
21460
21472
21601
40601
40613
40626
40642
40659
40671
40683
40695
40710
40727
40739
40751
40763
40775
7323
21461
21474
21602
40602
40614
40627
40643
40660
40672
40684
40696
40711
40728
40740
40752
40764
40777
21450
21462
21475
21603
40603
40615
40628
40645
40661
40673
40685
40697
40712
40729
40741
40753
40765
40778
21451
21463
21476
21604
40604
40616
40629
40646
40662
40674
40686
40698
40714
40730
40742
40754
40766
40779
21452
21464
21477
21605
40605
40617
40631
40648
40663
40675
40687
40699
40716
40731
40743
40755
40767
40780
21453
21465
21478
21606
40606
40618
40632
40649
40664
40676
40688
40700
40719
40732
40744
40756
40768
40781
21454
21466
21479
21607
40607
40619
40633
40650
40665
40677
40689
40701
40720
40733
40745
40757
40769
40782
21455
21467
21480
40596
40608
40620
40635
40652
40666
40678
40690
40703
40721
40734
40746
40758
40770
40783
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
6359
6371
7944
21578
21590
40539
40551
40563
6346
6360
7133
7945
21579
21591
40540
40552
40564
6347
6361
7134
7946
21580
21592
40541
40553
40565
6348
6362
7136
8054
21581
21593
40542
40554
40566
6351
6363
7137
8055
21582
21594
40543
40555
40567
6352
6364
7138
8056
21583
21595
40544
40556
40568
6353
6365
7139
8057
21584
21596
40545
40557
40569
6354
6366
7140
11240
21585
21609
40546
40558
40570
6355
6367
7141
11241
21586
22139
40547
40559
40571
6356
6368
7142
19210
21587
40536
40548
40560
40572
6357
6369
7300
19912
21588
40537
40549
40561
40573
6358
6370
7309
21577
21589
40538
40550
40562
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
6292
21513
21528
21540
40802
40814
5876
7306
21517
21529
21541
40803
40815
5877
8031
21518
21530
21542
40804
40816
5880
8032
21519
21531
21543
40805
40818
5881
17305
21520
21532
21544
40806
40819
5886
17306
21521
21533
22118
40807
40820
5887
17307
21522
21534
22121
40808
40821
5888
17308
21523
21535
23362
40809
40876
5889
17309
21524
21536
23368
40810
44152
5890
19911
21525
21537
40799
40811
44153
5892
19913
21526
21538
40800
40812
44154
6282
21512
21527
21539
40801
40813
120805
189667 189668 189669 189670 189671 189672 189674 189675 189676 189677 189678 189679
189680 198673 227929
S. o. longipes:
6265
6279
8062
23358
38025
40824
40836
40848
40860
6266
6280
8063
23359
38026
40825
40837
40849
40861
6267
6281
11212
23360
38027
40826
40838
40850
40862
6268
6287
11213
23361
38028
40827
40839
40851
40863
6269
6288
12470
23363
38029
40828
40840
40852
40864
6270
6289
17310
23364
38030
40829
40841
40853
40865
6271
6290
17311
23365
39648
40830
40842
40854
40875
6272
6298
17312
23366
39649
40831
40843
40855
44155
6274
8058
17313
23367
39650
40832
40844
40856
44156
6276
8059
22108
23369
39651
40833
40845
40857
14394
14406
14418
15946
16650
16663
29319
63460
14395
14407
14419
15947
16651
16664
36347
77821
14396
14408
14420
15948
16652
16665
36368
77822
14397
14409
14421
15949
16653
16667
39172
77823
14398
14410
14422
16642
16654
16668
40490
77824
14399
14411
14423
16643
16655
16669
40605
77825
14400
14412
14424
16644
16656
19945
40606
77826
6277
8060
23356
23370
40822
40834
40846
40858
6278
8061
23357
38024
40823
40835
40847
40859
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
14403
14415
15943
16647
16660
19948
40609
14392
14404
14416
15944
16648
16661
21447
40610
14393
14405
14417
15945
16649
16662
24455
63459
14401
14413
15936
16645
16657
19946
40607
14402
14414
15937
16646
16658
19947
40608
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
21490
21502
24557
36097
40503
40617
20372
21491
21503
24558
36098
40504
40618
20373
21492
21504
24559
36099
40505
40619
20374
21493
21505
24560
36100
40506
42079
20375 20376 20377 20378 20477
21494 21495 21496 21497 21498
24549 24550 24551 24552 24553
36089 36090 36091 36092 36093
36123 36134 40497 40498 40499
40507 40508 40509 40510 40511
162360 162361 187587 228226
20478
21499
24554
36094
40500
40512
20620
21500
24555
36095
40501
40615
20621
21501
24556
36096
40502
40616
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
12813
14667
24491
36040
51684
77852
7529
14656
14924
24492
36355
51686
77853
7530
14657
14925
24493
36356
51690
77854
7531
14658
14926
24494
36357
51691
77855
7532
14659
15956
24495
36372
51692
77856
11175
14660
17101
24496
36373
51694
77857
11179
14661
17102
25209
36374
51696
77858
11181
14662
17112
36035
50956
51697
77859
12806
14663
17114
36036
50957
51699
77860
12810
14664
20471
36037
51680
51700
77861
12811
14665
21458
36038
51681
75820
12812
14666
21465
36039
51682
77851
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
22791
36638
38376
93792
7866
31859
36639
39042
7868
31860
36642
39060
7870
31861
36643
39064
7875
36151
36644
39245
11363
36371
36650
39248
20646
36372
36651
39271
21630
36374
36654
39273
21633
36375
36655
64209
21639
36447
37990
91624
21642
36627
38374
92263
21643
36634
38375
93788
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
48
5. UNR:
C. d. myurus:
7740 7741 7742
7752 7753 7754
7764
Gienger et al. 2008:
CADR-11
CADR-22
CADR-33
CADR-44
CADRB-12
7743
7755
7744
7756
7745
7757
7746
7758
7747
7759
7748
7760
7749
7761
7750
7762
7751
7763
CADR-12
CADR-23
CADR-34
CADR-45
CADRB-3
CADR-13
CADR-24
CADR-35
CADR-51
CADRB-4
CADR-14
CADR-25
CADR-41
CADR-52
CADRB-5
CADR-15
CADR-31
CADR-42
CADRB-10
CADR-21
CADR-32
CADR-43
CADRB-11
5050 6542
7234
7797
7863
7864
7871
7872
7873
7874
17133 21619
21623 21637
38969 39246
21638
39253
21640
39270
36628
39272
36631
39587
36635
43393
36640
69600
36641
69601
36649
93785
38696 38966
202967
C. o. lutosus:
Gienger et al. 2008:
CRLU-8
CRLU-9
CRLU-22
CRLU-23
CRLU-29
CRLU-30
CRLU-13
CRLU-24
CRLU-31
CRLU-17
CRLU-25
CRLU-19
CRLU-26
CRLU-21
CRLU-28
7768
7769
7770
7771
7772
7773
7774
7775
7776
7813 7814 7815 7816
7826 7827 7828 7829
7839 7840 7841 7842
Gienger et al. 2008:
SCMA-11
SCMA-111
SCMA-12
SCMA-121
SCMA-13
SCMA-131
SCMA-14
SCMA-141
SCMA-15
SCMA-151
SCMA-21
SCMA-211
SCMA-22
SCMA-221
SCMA-23
SCMA-231
SCMA-24
SCMA-241
SCMA-25
SCMA-251
SCMA-301 SCMA-302
SCMA-31
SCMA-310
SCMA-315 SCMA-32
SCMA-324 SCMA-325
SCMA-42
SCMA-43
7817
7830
7819
7831
7820
7832
7821
7833
7822
7834
7823
7835
7824
7836
7825
7837
A. t. tigris:
7765 7766
7777
7767
S. uniformis:
SCMA-112
SCMA-122
SCMA-132
SCMA-142
SCMA-152
SCMA-212
SCMA-222
SCMA-232
SCMA-242
SCMA-252
SCMA-302b
SCMA-311
SCMA-320
SCMA-33
SCMA-44
SCMA-113
SCMA-123
SCMA-133
SCMA-143
SCMA-153
SCMA-213
SCMA-223
SCMA-233
SCMA-243
SCMA-253
SCMA-303
SCMA-312
SCMA-321
SCMA-34
SCMA-45
SCMA-114
SCMA-124
SCMA-134
SCMA-144
SCMA-154
SCMA-214
SCMA-224
SCMA-234
SCMA-244
SCMA-254
SCMA-304
SCMA-313
SCMA-322
SCMA-35
SCMA-115
SCMA-125
SCMA-135
SCMA-145
SCMA-155
SCMA-215
SCMA-225
SCMA-235
SCMA-245
SCMA-255
SCMA-305
SCMA-314
SCMA-323
SCMA-41
7783
7795
7785
7838
7787
7789
S. o. longipes:
7779 7780 7781
7791 7792 7793
Gienger et al. 2008:
7782
7794
7784
7796
7786
7788
7790
49
SCOC-003
SCOC-115
SCOC-125
SCOC-23
SCOC-34
SCOC-45
SCOC-11
SCOC-120
SCOC-126
SCOC-24
SCOC-35
SCOC-111
SCOC-121
SCOC-127
SCOC-25
SCOC-41
SCOC-112
SCOC-122
SCOC-128
SCOC-31
SCOC-42
SCOC-113
SCOC-123
SCOC-21
SCOC-32
SCOC-43
SCOC-114
SCOC-124
SCOC-22
SCOC-33
SCOC-44