On the Structure and Function of Tails in Snakes: Relative Length and Arboreality

Home , Ahaetulla dispar, Ahaetulla pulverulenta, Amblyodipsas polylepis, Atheris hispida, Boodontinae, Caudal luring

ON THE STRUCTURE AND FUNCTION OF TAILS IN SNAKES: RELATIVE LENGTH AND ARBOREALITY

COLEMAN MATTHEW SHEEHY III

A THESIS PRESENTED TO THE GRADUATE SCHOOL OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE UNIVERSITY OF FLORIDA 2006

Coleman Matthew Sheehy III

To the increased understanding, respect, and conservation of snakes worldwide

ACKNOWLEDGMENTS

I thank my committee members Harvey B. Lillywhite (chair), James Albert, and Max A.

Nickerson for their guidance and support. Harvey B. Lillywhite first inspired this work by suggesting a link between snake tails and the gravitational hypothesis. I thank Harvey B.

Lillywhite and Michael B. Harvey for providing unpublished snake length data, Florida Museum

of Natural History (FLMNH) curators F. Wayne King and Max A. Nickerson for access to the

Herpetology collection, Roy McDiarmid and George Zug at the United States National Museum

(USNM) for permission to use the Herpetology collection, and Steve Gotte at the USNM and

Kenney L. Krysko at the FLMNH for supplying data from the Herpetology collection databases.

I thank Michael B. Harvey, Laurie Vitt, James McCranie, Rom Whitaker, Bob Henderson, Bob

Powell, Blair Hedges, Ming Tu, Max A. Nickerson, Richard Sajdak, Bill Love, and John Rossi

for providing difficult to find snake natural history information.

I thank Michael B. Harvey and Ron Gutberlet for information on snake phylogenies,

Michael McCoy for assistance with various statistical programs and analyses, and Kent Vliet for

the use of a Macintosh computer. I thank Andres Lopez and Griffin Sheehy for help with

illustrating programs, Andres Lopez for help with phylogenetic programs, and Jason Neville for

computer assistance. I thank Glades Herp Inc. for permission to measure live snakes and,

perhaps more importantly, I am grateful to Russel L. Anderson, Sam D. Floyd and Ryan J. R.

McCleary for assistance in handling and measuring live snakes, many of which were large,

highly venomous, and uncooperative. In addition to my committee members, I thank Ryan J. R.

McCleary, David A. Wooten, Leslie Babonis, Chris Samuelson, Bruce Jayne, and Roy

McDiarmid for stimulating discussions regarding snake natural history and evolution. I thank

Griffin E. Sheehy and Andrea Martinez for all their patience, love and support. Finally, I want to

thank my parents Coleman M. Sheehy, Jr. and Ellen R. Sheehy for never failing to support and encourage a young boy’s endless passion for snakes. I could not have been more lucky.

TABLE OF CONTENTS page

ACKNOWLEDGMENTS ...... 4

LIST OF TABLES...... 8

LIST OF FIGURES ...... 9

ABSTRACT...... 10

CHAPTER

1 INTRODUCTION ...... 12

Gravitational Influence on Tail Morphology...... 13 Length Limitations...... 14 Relative Tail Length and Macrohabitat Use...... 15 Multiple Functions of Tail Use...... 17 Locomotion...... 17 Caudal Luring...... 20 Defense...... 21 Morphology and Reproduction...... 24 Sexual Dimorphism and Ontogenetic Shifts ...... 25

2 MATERIALS AND METHODS...... 27

Categorizing Climbing in Snakes: Gravitational Habitat ...... 27 Analyses...... 31 Frequency Distribution...... 31 Gravitational Habitat and Total Body Length...... 31 Gravitational Habitat and Tail Length...... 32 Constructing the Phylogeny ...... 32 Relative Tail-Length, Gravitational Habitat, and Phylogeny...... 34

3 RESULTS...... 48

Frequency Distribution ...... 48 Gravitational Habitat and Total Body Length ...... 48 Gravitational Habitat and Tail Length...... 49 Relative Tail-Length, Gravitational Habitat, and Phylogeny ...... 49

4 DISCUSSION...... 63

Relative Tail Length, Gravity, and Climbing in Snakes...... 63 Snake Tails and Defense: Speed and Pseudautotomy ...... 67

APPENDIX STENOTOPICALLY ARBOREAL SPECIES...... 71

LIST OF REFERENCES...... 73

BIOGRAPHICAL SKETCH ...... 85

LIST OF TABLES

Table page 2-1 Taxa and associated data sources for 227 snake species included in this study...... 36

2-2 Total variation in relative tail-lengths of 26 species of snakes...... 43

3-1 The 227 species included in this study ...... 50

A-1 Stenotopically arboreal species...... 71

LIST OF FIGURES

Figure page

2-1 Composite phylogeny of 227 snake taxa...... 44

3-1 Snake total length frequency distribution...... 56

3-2 Coefficients of variation of log10 transformed total length...... 58

3-3 Regression of log10 tail length on log10 total length...... 59

3-4 Analysis of covariance (ANCOVA) on corrected tail-length for 227 species of stenotopically arboreal...... 60

3-5 Analysis of covariance (ANCOVA) on corrected tail-length for 227 species of scansorial...... 61

3-6 Independent contrasts...... 62

4-1 Regression of absolute tail length on relative tail-length...... 70

Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science

ON THE STRUCTURE AND FUNCTION OF TAILS IN SNAKES: RELATIVE LENGTH AND ARBOREALITY

Coleman Matthew Sheehy III

December 2006

Chair: Harvey B. Lillywhite Major Department: Zoology

The pervasive effect of gravity on blood circulation is an important consequence for elongate animals such as snakes that utilize arboreal habitats. Upright postures create vertical gradients of hydrostatic pressures within circulatory vessels, and the magnitude of the pressure change is proportional to the total length of the blood column. In air, this potentially induces blood pooling and edema in dependent tissues and a decrease in the volume of blood reaching the head and vital organs of animals that are tall or elongate. Arboreal snakes exhibit a suite of behavioral, morphological, and physiological adaptations for countering the effects of gravity on blood circulation including relatively non-compliant tissue compartments in the tail.

Comparative studies involving arboreal, terrestrial, and aquatic species have demonstrated that blood pooling in dependent tissues of arboreal snakes can be tenfold lower than in terrestrial and aquatic species. In addition to non-compliant tail compartments, arboreal species appear to have longer tails relative to their non-climbing terrestrial and aquatic counterparts. However, the generality of tail length patterns related to arboreal habitats and gravity has not been previously studied in a broad range of taxa. Here I examine the hypothesis that there are constraints limiting the total length of arboreal snakes and that arboreal snakes

have relatively longer tails to help counter the effects of gravity while also helping to adjust total length to within the range of limitations.

I used macrohabitat and behavior to create four gravitational habitats to categorize the amount of climbing and, therefore, the amount of gravitational stress experienced: stenotopically arboreal, eurytopically arboreal/terrestrial, stenotopically terrestrial, and stenotopically aquatic.

The effects of sexual dimorphism, and ontogenetic shifts in allometry and habitat use, were avoided by using only adult females. Data were acquired from the literature, museum specimens, and live snakes. Frequency distributions and analysis of variance (ANOVA) were used to evaluate the assumption that total length limitations exist in stenotopically arboreal species. I tested for differences in relative tail-length (RTL) among the four gravitational habitats (227 species representing almost all snake families and subfamilies) by using analyses of covariance (ANCOVA). I tested for correlations between macrohabitat use and RTL within a phylogenetic framework by independent contrasts analyses after constructing a composite tree.

The RTL for the 227 species included in this study ranged from 1.1% (Rhinotyphlops episcopus) to 48.1% (Uromacer frenatus). The total length of stenotopically arboreal species appears to be constrained to between 50 and 200 cm, with few exceptions. The RTL between stenotopically arboreal and eurytopically arboreal/terrestrial species did not differ and were therefore combined into a single scansorial category. Scansorial species had RTLs on average two times longer than non-scansorial species. Snakes with relatively longer tails have a larger percent of dependent vessels contained within the tight integument of the tail and are thus more resistant to blood pooling experienced during climbing. Therefore, the relatively long tails of scansorial snakes can be regarded as one of a suite of characters likely to be adaptive responses to the cardiovascular constraints on blood circulation imposed by gravity.

CHAPTER 1 INTRODUCTION

Macrohabitat use is thought to strongly influence the evolution of vertebrate morphology

(Miles and Ricklefs 1984; Wikramanayake 1990; Lillywhite 1996; Martins, Araujo, Sawaya, and

Nunes 2001). Even in limbless and elongate vertebrates such as snakes, the evolution of

morphology is strongly influenced by the type of macrohabitat utilized (Vitt and Vangilder 1983;

Guyer and Donnelly 1990; Cadle and Greene 1993; Lillywhite and Henderson 2001; Martins et al. 2001). The roughly 3000 extant snake species have demonstrated a remarkable propensity for radiating into a wide variety of fossorial, arboreal, terrestrial, freshwater, and marine habitats in every part of the biosphere excluding only the deep sea and polar regions. This diverse ecological radiation, along with the loss of limbs, makes snakes excellent animals for investigating the effects of macrohabitat use on the evolution of morphology.

Arboreality has evolved numerous times independently among snakes, and several studies have identified various behavioral, morphological, and physiological characteristics associated with snakes in arboreal habitats (e.g., Johnson 1955; Marx and Rabb 1972; Henderson and

Binder 1980; Lillywhite 1993; Lillywhite and Henderson 2001; Martins et al. 2001). While it is

often difficult to demonstrate adaptation (e.g., Gould and Lewontin 1979; Bock 1980), the fact

that a phylogenetically diverse array of arboreal species share strikingly similar, if not identical,

morphological, behavioral, and physiological specializations supports the inference that these

traits are adaptive and, in many cases, the result of convergent evolution (Lillywhite 1996;

Lillywhite and Henderson 2001).

Studies investigating (directly or indirectly) snakes’ tails have included a wide range of

topics including cardiovascular adaptations (e.g., Lillywhite 1985, 1993, 2005; Lillywhite and

Henderson 2001), sexual dimorphism (e.g., Klauber 1943; King 1989; Shine 1993, 2000), mating

success (e.g., Shine et al. 2000), use in locomotion (e.g., Jayne 1988; Jayne and Bennett 1989), the evolution of vertebral elements (e.g., Johnson 1955; Lindell 1994; Shine 2000), defensive adaptations (e.g., Greene 1973, 1988; Arnold 1988; Mendelson 1991; Savage and Slowinski

1996), caudal luring (e.g., Greene 1997), development (Polly, Head, and Cohn 2001), and ecological correlations (e.g., Guyer and Donnelly 1990; Martins et al. 2001; Lobo, Pandav, and

Vasudevan 2004; Wüster, Duarte, and da Graça Salomão 2005; Wiens, Brandley, and Reeder

2006). However, the adaptive role of the tail in arboreal habitats is poorly understood. For example, the importance of the tail in snake locomotion (particularly in arboreal habitats) remains unclear (Jayne 1988; see below).

Gravitational Influence on Tail Morphology

An important consequence of utilizing complex, three-dimensional vertical habitats is the pervasive effect of gravity on blood circulation, which can be particularly pronounced in tall or long organisms such as giraffes and snakes (Lillywhite 1993,1996). Upright postures create vertical gradients of hydrostatic pressures within circulatory vessels. In air, this increases transmural pressures related to the absolute length of the fluid column, leading to a tendency for blood pooling and for fluid to filter from capillaries into surrounding tissue compartments resulting in edema in dependent tissues (Lillywhite 1985, 1993). As blood pooling and edema increase, the volume of blood reaching the heart decreases, thereby reducing the central blood pressure and consequently the amount of blood flow to the head and vital organs (Lillywhite

1993b, 1996, 2005; Lillywhite and Henderson 2001).

Arboreal snakes exhibit a suite of behavioral, morphological, and physiological adaptations for countering the effects of gravity on blood circulation including stereotypical body movements, small mass/length ratios, relatively anterior hearts, tightly applied integument, and relatively non-compliant tissue compartments in the tails (Lillywhite 1985, 1993; Lillywhite and

Henderson 2001). Comparative studies involving arboreal, terrestrial, and aquatic species demonstrate that blood pooling in dependent tissues of arboreal snakes during vertical posture is significantly less than in terrestrial and aquatic species, and these differences can approach tenfold (Lillywhite 1985, 1993; Lillywhite and Henderson 2001). The ability for arboreal snakes to defend against edema and blood pooling is almost certainly attributed to the aforementioned characters, one of which being relatively non-compliant tissue compartments in the tail

(Lillywhite and Henderson 2001; Lillywhite 2005). However, the magnitude of the compliance does not appear to be related to the length of the snake or its tail (Lillywhite 1993). There does, however, appear to be a relationship between tail length and macrohabitat use in that arboreal species generally have longer tails relative to their nonclimbing terrestrial and aquatic counterparts (see below). What then are the selective pressures responsible for the interspecific variation in tail length?

Length Limitations

Body size may be the most fundamental character of an organism, because nearly all aspects of an organism’s biology are correlated with this variable (Naganuma and Roughgarden

1990; Boback and Guyer 2003). The body sizes (i.e., total length) of snakes in general could be evolving toward an optimal length of 1.0 m (Boback and Guyer 2003), suggesting that selection and constraint might be influencing the total length of many snake species. However, the body size distribution is not obviously skewed in either direction, and idiosyncratic features of the natural history of snakes may be creating this distribution pattern (Boback and Guyer 2003).

Macrohabitat use likely imposes locomotor constraints upon snakes (Boback and Guyer 2003), and there is considerable evidence that arboreal snakes are limited in their use of habitat as a consequence of interactions between their morphology and the physical size of branches (see

Lillywhite and Henderson 2001, for a review on arboreal snake functional ecology). Arboreal

locomotion involves various combinations of undulatory, rectilinear, and concertina movements

along a complex and often unstable vertical three-dimensional substrate (Gans 1974; Edwards

1985; Lillywhite and Henderson 2001). Short snakes might not be able to adequately span gaps,

whereas large or heavy bodied snakes might not be supported by smaller branches (Henderson

and Nickerson 1976). Long snakes might be further limited physiologically by cardiovascular

constraints. Because foraging snakes must be able to span gaps between stems and branches and

approach prey without revealing their presence (Lillywhite and Henderson 2001), it is reasonable

to expect there are upper and lower limitations on total length in arboreal snake species.

Assuming there are length limitations imposed on snakes living in arboreal habitats, one

way snakes could have evolved total lengths within the acceptable range while still counteracting

blood pooling and assuring adequate blood flow to the head is by lengthening the tail relative to

the body since perivascular tissues are tighter in the tail than in the body cavity (Lillywhite

2005). Lengthening the tail relative to the body could potentially be achieved evolutionarily by

adding vertebrae to the tail or by elongating the caudal vertebrae themselves (Johnson 1955;

Shine 2000). Relative tail-length (RTL), which is the proportional ratio of tail length/total

length, is commonly used when performing interspecific comparisons in tail length to account

for total length differences (Klauber 1943). Relative tail-length in snakes appears to have low

intraspecific variation (i.e., it is a stable character), and this variation is further reduced when

investigating the sexes separately (Klauber 1943). Therefore, interspecific similarities and

differences in RTL are potentially useful sources of ecological and taxonomic information

(Klauber 1943).

Relative Tail-Length and Macrohabitat Use

Correlations between RTL and macrohabitat use have been suggested previously, but the

supporting data are weak or inconclusive. Klauber (1943) suggested that thick-bodied snakes

have relatively shorter tails than do thin-bodied snakes. Clark (1967) stated that fossorial habits seem to be accompanied by a shortening of the tail. Marx and Rabb (1972) investigated 962 species of 195 colubrid genera and found that the maximum number of subcaudal scales occurred in six species of snakes that were all arboreal (i.e., vine snakes). Because these six species are not all closely related, they concluded that these characteristics represent derived ecological specializations for arboreal habitats. King (1989) proposed that RTL in snakes is highly variable interspecifically and appears to be correlated with ecological factors. He also stated that other considerations such as mode of locomotion, habitat, and risk of predation, which while apparently correlated with tail length in lizards, have not been investigated in snakes.

Greene (1997) stated qualitatively that the tails of phylogenetically basal snakes

(scolecophidians) and most vipers are especially short, while the tails of many colubrids and elapids are longer. Martins et al. (2001) investigated 20 species of Bothrops and concluded that an increase in RTL occurred along with an increase in arboreality in some clades.

A strong method for assessing the influence of habitat use on the evolution of body form in snakes is to analyze monophyletic clades so that characters can be interpreted within an explicitly phylogenetic framework (Harvey and Pagel 1991; Martins et al. 2001). Although earlier studies have found a correlation between RTL and arboreality in snakes, most have not separated species by lineages and thus might be confounded by phylogenetic effects. Martins et al. (2001) addressed this issue using the monophyletic genus Bothrops, and their results corroborate previous studies. However, the study investigated only 20 species within a single clade, making the results difficult to apply to snakes in general. Similar studies using additional monophyletic groups are needed to determine whether this trend is widespread in snakes.

Herein, I investigate the relationship between tail length and macrohabitat use in arboreal species of snakes. The purposes of the present investigation are threefold. First, I evaluate the assumption that there are limitations imposed on the total length of arboreal species. Second, I test the hypothesis that arboreal species have relatively longer tails than nonclimbing species.

Third, I discuss the relationship between RTL and climbing within the context of gravitational adaptation, and hypothesize that additional selective pressures might be directing the evolution of relatively long tails in snakes.

Multiple Functions of Tail Use

Most vertebrate structures have multiple functions (Moon 2000), and snake tails are an excellent example. As a likely consequence of limblessness, several selective pressures are simultaneously acting on the tails of many snake species. For example, many juvenile pitvipers

(e.g., Agkistrodon piscivorus) use caudal luring to attract prey, but also vibrate their tails rapidly in defense when threatened. In order to understand the functional versatility, as well as possible constraints of complex vertebrate structures such as snake tails, information about how they are used in diverse environments and behaviors is required (Moon 2000).

Locomotion

Snakes likely use their tails to assist in locomotion (e.g., balance, propulsion, holding or climbing) (Klauber 1943); however, the extent to which this occurs is poorly understood (Jayne

1988; Lillywhite and Henderson 2001). Many fossorial species have short blunt tails (e.g., Eryx,

Sympholis lippiens, scolecophidians, and uropeltids), and some also have strongly keeled caudal scales (e.g., Sonora aemula and uropeltids). The apparent commonality of these characteristics among fossorial species suggests they are adaptations to fossorial habitats (e.g., locomotion and defense). However, in many cases the functional morphology is not well studied. Clark (1967) posits that the short tails of many fossorial snakes (i.e., scolecophidians) facilitate subterranean

locomotion by acting as an anchor against which the snake can push, since a long tail in this case

would likely bend and be unable to serve this purpose. However, Klauber (in Clark 1967)

suggests instead that burrowing would render the tail practically useless, and that the tails of

fossorial snakes are shortened secondarily due to non-use, rather than from direct selective pressures.

In a combination of experimental and correlative analyses, Jayne and Bennett (1989) demonstrated the difficulties in determining the effect of tail morphology on locomotor performance in terrestrial snakes. Jayne and Bennett demonstrated that losses ranging from

0.03% to 80.4% tail length had no significant effect on terrestrial locomotory performance in 52 garter snakes (Thamnophis sirtalis) with naturally incomplete tails. Locomotor performance was not affected by the experimental removal of the distal one third of the tail. The experimental removal of the distal two thirds of the tail only caused a small (4.5%) but significant average decrease in speed. However, the same study also found that burst speed in T. sirtalis performing terrestrial lateral undulation was fastest in individuals with intermediate relative tail-lengths.

Jayne and Bennett concluded that minor deviations from intermediate relative tail length do not affect locomotor performance among snakes. These results demonstrate that long tails can perhaps be slightly disadvantageous in terms of locomotor performance in T. sirtalis, and suggest that the long tails of some snake species are possibly due to other additional selective pressures.

For example, high incidence of tail loss is found in the genera Nerodia and Thamnophis suggesting tail loss from predation attempts (King 1987; Jayne and Bennett 1989; Mendelson

1991; see section below on tail loss). Furthermore, juvenile Nerodia harteri have been observed using their long tails to anchor themselves to rocks at the water’s edge while fishing (Rossi, pers.

comm.), whereas Nerodia sipedon has been observed using their tails to anchor themselves to

submerged sticks and rocks while fishing in currents (M. A. Nickerson pers. comm.; pers. obs).

Snake caudal vertebrae are complex, highly variable in size within individuals, and clearly distinguishable from the trunk vertebrae (Johnson 1955). Because the number of caudal vertebrae corresponds to the number of subcaudal scales by a ratio of 1:1 in most snake species, snakes with longer tails typically have more subcaudals and thus more caudal vertebrae than snakes with shorter tails (Ruthven and Thompson 1908; Gans and Taub 1965; Alexander and

Gans 1966; Voris 1975; Shine 2000). Differences in the relative size and number of caudal vertebrae suggest that the effectiveness of the tail in locomotory propulsion varies considerably among snake taxa (Jayne 1988). However, the consequences of caudal morphology likely vary with mode of locomotion (Jayne 1988). More research is needed to determine the extent of tail use in the various forms of snake locomotion.

The tails of most arboreal boids, viperids, and many colubrids are prehensile and assist in climbing and securing to branches (Lillywhite and Henderson 2001). Tree boas (Corallus) often wrap their prehensile tails around branches during prey capture and consumption (Henderson

2002; pers. obs.). Henderson (2002) observed tree boas (Corallus grenadensis) on Grenada hanging by their tails from vegetation, with the forepart of their bodies in typical ambush posture, presumably hunting for bats. I have observed similar hunting behavior in Corallus ruschenbergerii on Tobago and in Corallus caninus in captivity. However, there appears to be no correlation between long RTL and tail prehension for snakes in general (Lillywhite and

Henderson 2001).

Specializations in snake locomotion, such as highly efficient swimming and sidewinding, have likely evolved multiple times and employ tail use to varying degrees. Sea snakes and sea

kraits have evolved several adaptations to a marine existence, one of which being flattened, oarlike tails used for effective and rapid propulsion (Heatwole 1999). Yellow-bellied sea snakes

(Pelamis platurus) are well adapted to a pelagic existence and have subsequently lost the ability to crawl on land, spending their entire lives at sea (Greene 1997). Acrochordids have a muscle that shapes the skin of the body and tail into a keel while swimming (Heatwole 1999). However, not all marine snakes have oarlike tails. Some homalopsines have tails that are only slightly compressed, whereas natricines and other homalopsines have tails similar in size and shape to many terrestrial species (Heatwole 1999).

Sidewinding is often considered to be a specialized mode of locomotion (Jayne 1988).

However, it occurs in a surprisingly wide diversity of taxa including booid and colubroid snakes

(Gans and Mendelssohn 1972). Jayne (1988), in a study of snake locomotion, concluded that the tails of snakes are unlikely able to produce the movements and forces necessary for sidewinding and thus are likely contributing little during this form of locomotion.

Caudal Luring

Several snake species within the Boidae, Viperidae, Elapidae, and Colubridae use caudal luring to attract insectivorous prey by wiggling the often contrastingly colored tail tip (Sazima and Puorto 1993; Greene 1997). These taxa include Boa constrictor (Radcliffe, Chiszar, and

Smith 1980), Morelia viridis (Murphy, Carpenter, and Gillingham 1978), Calloselasma rhodostoma (Schuett 1984; Daltry, Wuster, and Thorpe 1998), Cerastes vipera (Heatwole and

Davison 1976), Daboia russelii (Henderson 1970), Agkistrodon (Neill 1948; Allen 1949;

Wharton 1960; Carpenter and Gillingham 1990), Crotalus (Kauffeld 1943), Hypnale (Whitaker and Captain 2004), Sistrurus (Jackson and Martin 1980; Rabatsky and Farrell 1996), Bothriopsis

(Greene and Campbell 1972), Bothrops (Sazima 1991), Acanthophis (Carpenter, Murphy and

Carpenter 1978; Chiszar, Boyer, Lee, Murphy, and Radcliffe 1990), Alsophis portoricensis (Leal

and Thomas 1994), Pantherophis obsoleta (Tiebout 1997), Tropidodryas striateceps (Sazima

and Puorto 1993), and Madagascarophis (W. Love pers. comm.). Caudal luring has been

reported primarily in juveniles (80% of the species known to caudal lure) to attract small,

visually oriented prey such as anurans and lizards into striking range (Neill 1960; Parellada and

Santos 2002). Cessation of this behavior often occurs within the first year or two with an

ontogenetic shift in diet towards larger endothermic prey items such as mammals and birds (Neill

1960; Jackson and Martin 1980; Daltry et al. 1998). However, in some species such as

Acanthophis antarcticus (Carpenter et al. 1978), Bothriopsis bilineata (Greene and Campbell

1972), Cerastes vipera (Heatwole and Davison 1976), and Sistrurus miliarius (Jackson and

Martin 1980), the behavior persists into adulthood. Persistence of caudal luring in these species has been attributed to the importance of insectivorous prey items in their adult diets (Jackson and

Martin 1980).

Defense

Snakes exhibit the most elaborate antipredator behaviors among reptiles (Greene 1988).

These behaviors range from generalized to specialized, and many involve the tail. Postcloacal scent glands are found in all snake species and exude an offensive odor (Whiting 1969). These noxious secretions likely enhance the effectiveness of cloacal discharge (fecal material) in deterring predators (Greene 1988).

Defensive tail displays are widespread in snakes; Greene (1973) identified 73 snake

species in at least six families known to perform unusually conspicuous tail displays.

Characteristics of these displays include elevating (e.g., Eryx and Charina), tightly coiling (e.g.,

Diadophis and Farancia), or waving (e.g., Micrurus and Micruroides) the tail, which may be long or blunt, and brightly colored or drab. When threatened, Rhadinaea decorata often hides its head beneath coils while raising and wriggling its tail (Campbell 1998), whereas Oligodon

albocinctus and Sinomicrurus macclellandi flatten their bodies and curl up the end of their tails

(Whitaker and Captain 2004). Calliophis melanurus and C. nigrescens raise and coil their tails when disturbed (Whitaker and Captain 2004). Chilorhinopus butleri and C. gerardi hide their heads within coils and wave their tails in the air in defense (Spawls, Howell, Drewes, and Ashe

2002).

Tail length and thickness correlate with tail injury rate and defensive behaviors in the genera Eryx and Gongylophis (Greene 1973; R. Sajdak pers. comm.). Species exhibiting tail displays (e.g., E. jaculus, E. johnii, E. miliaris, and E. tataricus) have longer and thicker tails, small heads, and a relatively high frequency of tail injury. However, species that rely on a biting defense instead of tail displays (e.g., G. colubrinus, G. conicus, and possibly E. somalicus) have shorter, thinner tails, larger and more distinct heads, and a lower frequency of tail injury. These displays likely disorient potential predators and, in many species, serve as a decoy to divert attack from the head to the tail (Greene 1973).

Many species have tails with specialized external morphological characters used for defense. Several terrestrial and fossorial species (e.g., Carphophis, Contia tenuis, Farancia,

Oligodon affinis, and several typhlopids) possess a tail spine, which is pressed against an attacker

(Leonard and Stebbins 1999; Whitaker and Captain 2004). Juvenile Farancia abacura have also been observed using this tail spine to impale or “pop” tadpoles normally too large to be swallowed (Rossi 1992: 97). Uropeltids have enlarged, reinforced tail tips with specialized scale morphology that collect dirt to form protective plugs while burrowing (Gans 1976; Gans and

Baic 1977). Cutaneous photoreception, or dermal light sense, in the tail of the sea snake

Aipysurus laevis aides in concealment from visually oriented predators (Zimmerman and

Heatwole 1990). These sea snakes often hide in clumps of coral and use cutaneous

photoreception to avoid having their tails exposed to light, and thus vulnerable, during the

daytime.

The genera Crotalus and Sistrurus form the monophyletic group of approximately 31

species of New World pitvipers characterized by the presence of a rattle (Greene 1988). The

rattle is associated with a suite of anatomical, physiological, and behavioral specializations and is

generally accepted as being used primarily in defensive signaling (see Moon 2001, for summary

of rattle evolution). However, the evolution of this unique structure remains unresolved (Greene

1988; Moon 2001). A potential behavioral precursor to the rattle is tail vibrating, a defensive

behavior widespread in snakes where the tail is rapidly vibrated against loose surface debris to

produce a buzzing sound (Greene 1988).

Caudal pseudautotomy occurs in several snake species as a defensive strategy (Savage and

Slowinski 1996). However, this behavior has only been documented in snakes with relatively

long tails and is thought to be rare (Arnold 1988; Marco 2002). Enulius, Scaphiodontophis and

Urotheca possess morphological specializations that likely facilitate pseudautotomy such as

long, fragile tails with thick bases (Savage and Slowinski 1996). However, high incidence of tail

loss has also been observed in several other typically long-tailed genera such as Alsophis (Seidel

and Franz 1994), Amphiesma and Boiga (Whitaker and Captain 2004), Coluber (Marco 2002),

Coniophanes, Rhadinaea, Sibynophis and Thamnophis (Jayne and Bennett 1989; see Mendelson

1991, for review), Dendrophidion, (Duellman 1979), Drymobius (Mendelson 1991), Gastropyxis

(as Hapsidophrys), Grayia and Mehelya (Spawls et al. 2002), Nerodia (King 1987), Natriceteres

and Psammophis (Broadley 1987), Pliocercus (Smith and Chizar 1996), and Xenochrophis

(Ananeva and Orlov 1994), although these genera do not appear to possess the morphological

specializations for tail loss present in Enulius, Scaphiodontophis and Urotheca (Savage and

Slowinski 1996).

While both intervertebral pseudautotomy and intravertebral autotomy occur in lizards, only intervertebral pseudautotomy is known to occur in snakes (Arnold 1988; see Savage and

Slowinski 1996, for a review of terminology). Unlike many lizard species, pseudautotomy in snakes does not appear to be under neural control (Arnold 1988) and requires physical resistance, which is often facilitated by twisting or rotating the body in one direction until the tail snaps off

(Savage and Slowinski 1996; Marco 2002). However, reflex action often allows the segment of lost tail to continue thrashing, thus likely distracting the predator and allowing the snake to escape (Marco 2002; Savage 2002). Although caudal autotomy is a lepidosaurian synapomorphy, the ability to regenerate any portion of the tail has been lost in all snake species

(Pough et al. 2001).

Morphology and Reproduction

Peters (1964) defines the snake tail as the section of the body posterior to the cloaca. In males, the hemipenes and associated retractor muscles are located in the tail, while the testes

(and ovaries in females) are located within the body cavity. In both sexes of all species, the tail also contains a pair of scent glands (Whiting 1969). Male snakes typically use their tails during courtship to gain access to the female’s cloaca by performing a tail-search copulatory attempt

(TSCA) until the cloacas meet (Gillingham, Carpenter, and Murphy 1983). This TSCA is often preceded by various tail movements by the female, such as tail-whipping and tail-waving

(Carpenter and Ferguson 1977) and is followed by intromission and coitus (Gillingham et al.

1983). In most boids, courtship is facilitated by the use of two claw-like spurs, which are located on either side of the male’s cloaca. Male Madagascan tree boas (Sanzinia madagascariensis) use their spurs in combat bouts with other male conspecifics (Carpenter, Murphy, and Mitchell

1978). During these bouts, the males entwine their tails and vigorously flex the erected spurs

against the scales of the opponent while hanging from branches. Larger male garter snakes

(Thamnophis sirtalis) and European grass snakes (Natrix natrix) usually achieve more matings

apparently because they can physically displace the tails of smaller rival males by tail wrestling

(Luiselli 1996; Shine et al. 2000). Tail wrestling in this context may be widespread in snake

species that display “mating balls,” or mating aggregations where multiple males simultaneously

attempt copulation (Shine et al. 2000: F9).

Sexual Dimorphism and Ontogenetic Shifts

Although RTL is a stable character, sexual dimorphism in snake tail length is common

(Klauber 1943). Males typically have longer, more attenuate tails than females (King 1989;

Shine 1993). However, the degree of these differences varies interspecifically (King 1989; Shine

1993). King (1989) proposed three hypotheses that could help explain the existence of sexual dimorphism in tail length among snakes: (1) morphological constraint (the hemipenes and retractor muscles of males are located in the tail); (2) female reproductive output (a more posterior cloaca might increase body cavity volume and allow increased fecundity); and (3) male mating ability (longer tails in males may be advantageous during courtship). These predictions were tested using 56 colubrid genera, and the results supported both the morphological constraint and female reproductive output hypotheses (King 1989). Additional studies involving tail wrestling in several natricine species provide support for the male mating ability hypothesis

(Luiselli 1996; Shine et al. 2000). However, selection could act on more than one of these

hypotheses simultaneously.

Whereas RTL is stable among individuals of the same species, sex, and age, RTL is

nonetheless ontogenetically variable in most snake taxa (Klauber 1943). Therefore, the tail

proportions (allometry) of many species change as they grow. The majority of snake species

have relative tail-lengths that increase as they age (Klauber 1943); however, some species (e.g.,

Pituophis and Lampropeltis) have relative tail-lengths that become shorter (Klauber 1943).

Furthermore, some snake species demonstrate ontogenetic shifts in macrohabitat use, with one age class (e.g., juveniles or adults) found more frequently utilizing arboreal macrohabitats than another (Martins and Oliveira 1999). This behavioral shift has been well documented in several large boid species such as Python sebae (Spawls et al. 2002) and Boa constrictor (Campbell

1998), some colubrids such as Pseustes poecilonotus (Boos 2001), some viperids such as

Bothrops jararaca (Sazima 1992; Martins et al. 2001), and some elapids such as Ophiophagus hannah (R. Whitaker pers. comm.). Usually, juveniles are more arboreal than adults in those snake species known to exhibit behavioral shifts in habitat use. However, the opposite trend has been observed in Leptophis depressirostris (Nickerson, Sajdak, Henderson, and Ketcham 1978) and in some populations of Boa constrictor (Campbell 1998). Ontogenetic shifts involving arboreal macrohabitat use likely occur in many snake clades, but more detailed natural history information is needed to know the extent to which this is the case.

CHAPTER 2 MATERIALS AND METHODS

Categorizing Climbing in Snakes: Gravitational Habitat

Snakes occupy a wide variety of habitat types, and it is often useful to divide habitat usage into generalized categories when discussing snake community assemblages. Perhaps the most widely utilized categories for snake habitat use include fossorial, terrestrial, aquatic, semiaquatic, arboreal, and semiarboreal, or some subset of these (e.g., Johnson 1955; Shine 1983; Guyer and

Donnelly 1990; Dalrymple, Bernardino, Steiner, and Nodell 1991; Lindell 1994; Conant and

Collins 1998; Vidal, Kindl, Wong, and Hedges 2000).

However, as correctly noted by Johnson (1955), these categories can become inadequate when performing interspecific ecomorphological studies because patterns in habitat usage are often obscured. This is because these categories describe the habitat per se, and not the behaviors snakes exhibit while utilizing these habitats. For example, watersnakes in the genus

Nerodia typically live and obtain food near water (Conant and Collins 1998). Consequently, they are usually categorized as aquatic or semiaquatic (e.g., Vidal et al. 2000). However, many

Nerodia species spend a significant amount of time out of the water and off the ground climbing among branches to bask (Conant and Collins 1998). In fact, during parts of the year, some

Nerodia species can spend as much or more time above the ground in shrubs and trees than

Coluber constrictor, a snake typically categorized as semiarboreal (Mushinsky, Hebrard, and

Walley 1980; Plummer and Congdon 1994). Separating Nerodia and Coluber into distinct ecological categories (aquatic or semiaquatic versus semiarboreal) obscures these similarities in habitat usage. Similarly, categorizing both Nerodia and sea snakes such as the entirely pelagic

Pelamis platurus as aquatic is equally misleading. But in this case it is because the grouping suggests strong similarity in habitat usage when in actuality there is very little. Therefore, a

different system was needed to categorize climbing in snakes that combines habitat use with behavior, which I call gravitational habitat.

In order to categorize the amount of climbing, and therefore the amount of gravitational stress imposed, I divided gravitational habitat into four categories: stenotopically arboreal, eurytopically arboreal/terrestrial, stenotopically terrestrial, and stenotopically aquatic. These categories were based on adult habitat use information compiled from the literature and from personal observations. I define stenotopically arboreal species as those primarily living in arboreal habitats. These species are rarely found on the ground and should experience the greatest gravitational stress. Eurytopically arboreal/terrestrial species are often found on the ground, but regularly climb for reasons including hunting, escaping predators, and thermoregulation (e.g., Masticophis and Coluber). The stenotopically terrestrial category includes both terrestrial and fossorial species that rarely if ever climb and, thus, these species should experience relatively little gravitational stress. Some characteristically terrestrial species, or populations of species, do climb occasionally (e.g., Bitis arietans, B. armata, Bothrops asper,

Crotalus horridus, and Thamnophis sirtalis). However, I consider this behavior atypical and do not consider them eurytopically arboreal/terrestrial. I define stenotopically aquatic species as those primarily found in water. They typically exhibit one or more morphological specializations accepted as adaptations to aquatic habitats such as a flattened or oarlike tail, more dorsally positioned eyes and nostrils, salt excreting glands, and valvular nostrils (Heatwole,

1999). Laticaudines (genus Laticauda), the homalopsine snake Enhydris enhydris, and Helicops angulatus are included within this category because they are clearly adapted to an aquatic lifestyle and are usually found in water even though they occasionally sojourn onto land.

Stenotopically aquatic species should experience the least gravitational stress because the

surrounding water column acts as an “antigravity suit” (Lillywhite 1993: 561). Importantly, all categorical placements were based entirely on the ecology and behavior of each species and not on morphology.

Habitat use and other natural history information for each species were collated from the literature. Whereas many of these sources were various journal publications, a large amount of this information came from the following: Africa (Broadley and Cock 1975; Broadley 1983;

Branch 1998; Schmidt and Noble 1998; Spawls et al. 2002); Australia (Shine 1995); Central

America (Campbell 1998; Savage 2002); India (Whitaker and Captain 2004); Madagascar (Glaw and Vences 1994; Henkel and Schmidt 2000); North America (Smith and Brodie 1982; Conant and Collins 1998); South America (Murphy 1997; Boos 2001; Duellman 2005); and the West

Indies (Schwartz and Henderson 1991).

However, the natural history of some of the species included in this study is incompletely known, thereby making categorization difficult. For example, Alsophis antillensis and closely related Antillophis parvifrons are West Indian racers with relatively long tails (27.8% and 31.1% respectively). However, whether these species climb or not is unknown. Several other species of Alsophis are known to climb well, but because this information is not available for A. antillensis and A. parvifrons, I chose not to assume they climbed and thus categorized them as stenotopically terrestrial even though they may actually climb to some extent.

In order to avoid the confounding effects of sexual dimorphism and ontogenetic shifts in allometry and habitat use, only adult females were used for all aspects of this study except for the frequency distribution (see below). A snake was determined to be an adult if its total length was within, or very near, the published adult range for that species. Tail length data were collected from the literature, museum specimens, and live snakes (see Table 2-1 for species used in this

study and sources). Museum specimens were acquired from the Florida Museum of Natural

History (FLMNH) and National Museum of Natural History, Smithsonian (USNM). For

museum specimens, sex was determined by subcaudal incision. Species in which females are

known to possess well-developed hemipenis-like structures (e.g., Pseudoficimia and Gyalopium;

Hardy 1972; Smith and Brodie 1982) were not used in this study. Some Bothrops insularis

females have hemipenis-like structures (Hoge, Belluomini, Schreiber, and Penha 1961), and this

species was included in the study under the assumption that length data reported by Klauber

(1943) were from functional females. Klauber (1943) states that differential shrinkage between the tail and body can occur as a result of preservation, but that the amount is insignificant as long as the preservation methods are consistent. Live snakes were measured at Glades Herp Inc.,

Florida, and were probed to determine sex.

Snout-vent length (SVL) was measured from the tip of the snout to the posterior edge of the anal scale. Tail length was measured from the posterior edge of the anal scale to the tip of the tail, and only snakes with complete tails were used in this study. Snout-vent length and tail length were measured using either a meter stick (± 1.0 mm) or a caliper (± 0.1 mm). A string was used to follow the body contours of live snakes and rigid specimens and was subsequently measured with a meter stick. Length measurements were repeated on individuals up to ten times when possible and then averaged. I used mean SVL and tail lengths when those data were available from the literature or from multiple specimens, but otherwise I used data representing

single specimens. To verify the stability of relative tail-length (RTL), I gathered large samples of

data from the literature on the total variation in adult female RTL for 26 species (5 families, 9

subfamilies, 26 genera) and found the variation to be small (mean variation ± SE, 1% ± 0.3%,

95% C.I.) (Table 2-2). Furthermore, the RTL of museum specimens was checked to ensure the data were consistent with published adult lengths for that species.

Analyses

Frequency Distribution

Frequency distributions for total lengths were produced for each of the four gravitational habitat categories: stenotopically arboreal (n=75), eurytopically arboreal/terrestrial (n=74), stenotopically terrestrial (n=94), and stenotopically aquatic (n=35)(Table A-1). All categories comprise both Old and New World species. Data used for the frequency distributions were based on raw total lengths. Stenotopically arboreal species should spend the most time in arboreal habitats and, thus, were analyzed separately from eurytopically arboreal/terrestrial species. Furthermore, eurytopically arboreal/terrestrial species might not climb enough to have their lengths affected by such limitations.

Because there is much interspecific variation among snakes regarding which sex is longer

(Shine 1993), I used length measurements representing the longest adult total lengths regardless of sex. Maximum total lengths for each species were used when possible unless stated by the authors that the maximum size is extremely unusual. In that case, the next largest measurement was used. Maximum adult total length was used because whereas juvenile length is likely also under related selective pressures, they differ from adults in two important ways: (1) juveniles may utilize a different macrohabitat until adult size is reached or until a certain length is attained; and (2) juveniles are shorter and are thus less affected by gravitational stresses on blood circulation.

Gravitational Habitat and Total Body Length

To test for differences in mean total length among the four categories, I used an analysis of variance (ANOVA). To meet the assumption of normality, the length data were log10

transformed. Following the ANOVA, I compared the means among the four categories, using

Tukey’s Honestly Significant Difference test. Coefficients of variation (CV) were calculated and

used to compare variance among the four categories.

Gravitational Habitat and Tail Length

I tested for differences in tail length among 227 species within 138 genera, 12 families, and

18 subfamilies using an analysis of covariance (ANCOVA) with total length treated as a

covariate. Differences in tail length corrected for body length (corrected tail-length) were

inferred from comparisons of the Y-intercepts in the ANCOVA. Data in this and all subsequent

analyses were collected independently from those used in the frequency distribution described

above. Data were log10 transformed to meet the assumptions of linearity and normality before

performing the ANCOVA analyses. All statistical analyses were performed using the statistical

program package R (R Development Core Team 2006).

Constructing the Phylogeny

Phylogenies constructed by Lawson, Slowinski, Crother, and Burbrink (2005), Lawson,

Slowinski, and Burbrink (2004), and Vidal et al. (2000) were combined and used as a base

phylogeny, to which additional phylogenies from detailed studies were added (Fig. 2-1). When

possible, the trees chosen were those recommended by the authors. However, these were often

consensus trees and, as such, occasionally contained polytomies. Polytomy resolution was often

achieved by either using another tree in the same study with high bootstrap support, or by using a

tree from a different study. For different trees containing similar species but with conflicting

relationships, I used the tree with the strongest bootstrap support and, when available, the more extensive taxon sampling. However, phylogenetic relationships for some clades remain unresolved (e.g., Dipsas, Langaha, Leptodeira, Prosymna, and Psammophis), and uncertain relationships were in the end reflected as polytomies. Many of these polytomies contain

congeners categorized within the same gravitational habitat and, thus, are not likely to affect the

results (Fig 2-1). In some cases, I used species thought closely related to those in the composite tree to replace species for which no specimens or length data were available (e.g., Hydrops triangularis was replaced by H. caesurus; Xenoxybelis argenteus was replaced by X.

boulengeri).

The following studies were used to add taxa to the base phylogeny (Fig. 2-1). The

scolecophidian clade was replaced using the phylogeny of Vidal and Hedges (2002). The

phylogeny of Lenk, Kalyabina, Wink, and Joger (2001) was used for placement of true vipers

(Atheris, Bitis, Causus, Macrovipera and Vipera). The phylogeny of Malhotra and Thorpe

(2004) was used for Asian pitviper (Protobothrops, Trimeresurus, and Tropidolaemus) placement. The phylogeny of Parkinson, Campbell, and Chippindale (2002, in Gutberlet and

Harvey 2004) was used for New World pitviper relationships, and the phylogeny of Murphy, Fu,

Lathrop, Feltham, and Kovac (2002) was used for relationships within Crotalus. The phylogeny of Nagy, Joger, Wink, Glaw, and Vences (2003) was used for pseudoxyrhophine relationships.

The phylogeny of Kelly, Barker, and Villet (2003) was used for Dasypeltis and Dendrelaphis placement and psammophine relationships. The phylogeny of Alfaro and Arnold (2001) was used for thamnophiine relationships, and the phylogeny of De Quieroz, Lawson, and Lemos-

Espinal (2002) was used for relationships within Thamnophis. The phylogeny of Lawson et al.

(2005) was used for placement of the Homalopsinae, as well as the following genera: Ahaetulla,

Carphophis, Crotaphopeltis, Dinodon, Dipsadoboa, Drymarchon, Gonyosoma, Grayia,

Lycophidion, Masticophis, Mehelya, Natriceteres, Opheodrys, Prosymna, Philothamnus,

Phyllorynchus, Pseudaspis, Sonora, Spilotes, Telescopus, Thelotornis, Thrasops, and

Xenochrophis. The phylogeny of Utiger et al. (2002) was used for the placement of Arizona,

Elaphe, Lampropeltis, Pantherophis, and Pituophis. The phylogeny of Vidal et al. (2000) was

used for the placement of the following genera: Helicops, Hydrodynastes, Hydrops, Ialtris,

Oxyrhopus, and Pseudoeryx. The phylogeny of Kraus and Brown (1998) was used for the placement of the genera Chilomeniscus and Dispholidus. Subfamily designation followed that of the EMBL Reptile Database (Uetz 2006). However, recent phylogenetic analyses by Lawson et al. (2005) provide further evidence that considerable changes in these classifications need to occur in order to recognize monophyletic groups.

Relative Tail-Length, Gravitational Habitat, and Phylogeny

Interspecific comparative analyses can be confounded by pseudoreplication caused by phylogenetic relatedness among species samples (Price 1997). However, these effects can be partially resolved using independent contrasts (Felsenstein 1985). I assessed the relationship between RTL and macrohabitat use using the program Mesquite version 1.06 (Maddison and

Maddison 2005). Because there is no comprehensive phylogeny available for snakes, I constructed an estimate of relatedness by combining data from 14 recent molecular snake phylogenies into a composite tree containing 227 species within 138 genera, 12 families, and 18 subfamilies (Fig. 2-1). These data represent almost all snake families and subfamilies (see below). Branch lengths could not be estimated because the final phylogenetic tree was composed from a variety of sources. Independent contrasts were therefore generated with branch lengths assigned as either equal or with the assumption that the age of a clade is proportional to the number of species it contains using Grafen’s branch lengths (Grafen 1989; Maddison and

Maddison 2005). However, plots of standardized contrasts against the variance of untransformed contrasts showed strong significant correlations for Grafen’s, but not equal, branch lengths. As significant correlations violate a key assumption of independent contrast analysis (Diaz-Uriarte and Garland 1996), I used equal branch lengths only in the final analysis. Contrasts were

calculated between nodes for macrohabitat use and log10 transformed RTL, and relationships were examined between the variables by calculating regressions on these standardized contrasts using least-squared change optimization parsimony (Garland, Harvey, and Ives 1992; Grafen

1992).

Table 2-1. Taxa and associated data sources for 227 snake species included in this study. Family Subfamily Species Source

Acrochordidae Acrochordus granulatus Lillywhite unpubl. data

Aniliidae Anilius scytale UF62496

Atractaspididae Aparallactinae Amblyodipsas polylepis Broadley and Cock 1975 Amblyodipsas ventrimaculatus Broadley and Cock 1975 Aparallactus capensis Broadley and Cock 1975 Aparallactus guentheri Broadley and Cock 1975 Aparallactus lunulatus Broadley and Cock 1975 Xenocalamus mechowii Broadley and Cock 1975 Xenocalamus sabiensis Broadley and Cock 1975 Atractaspis bibronii Broadley and Cock 1975

Boidae Boinae Acrantophis dumerili Sheehy unpubl. data Boa constrictor Lillywhite unpubl. data Corallus caninus Lillywhite unpubl. data Corallus ruschenbergerii Sheehy unpubl. data Epicrates striatus Sheehy unpubl. data

Erycinae Charina trivirgata Klauber 1943 Gongylophis muelleri Sheehy unpubl. data

Pythoninae Morelia viridis Sheehy unpubl. data Python molurus Lillywhite unpubl. data Python regius Lillywhite unpubl. data Python sebae Broadley and Cock 1975

Colubridae Boodontinae Duberria lutrix Broadley and Cock 1975 Grayia smythii UF57047 Lamprophis fuliginosus Broadley and Cock 1975 Lamprophis lineatus Klauber 1943 Lycodonomorphus leleupi Broadley and Cock 1975 Lycophidion capense Broadley and Cock 1975 Lycophidion variegatum Broadley and Cock 1975 Mehelya capensis Schmidt and Noble 1998 Pseudaspis cana Broadley and Cock 1975

Table 2-1. Continued Family Subfamily Species Source Colubridae Colubrinae Ahaetulla nasuta Lillywhite unpubl. data Arizona elegans UF48734 Boiga blandingii UF69248 Boiga cynodon UF55217 Chilomeniscus stramineus Klauber 1943 Chironius carinatus UF34779 Coluber constrictor UF47855 Crotaphopeltis hotamboeia Broadley and Cock 1975 Dasypeltis fasciata UF61301 Dasypeltis medici Broadley and Cock 1975 Dasypeltis scabra Broadley and Cock 1975 Dendrelaphis pictus Lillywhite unpubl. data Dinodon rufozonatum Lillywhite unpubl. data Dinodon semicarinatum UF24089 Dipsadoboa aulica Broadley and Cock 1975 Dipsadoboa unicolor Schmidt and Noble 1998 Dispholidus typus Broadley and Cock 1975 Drymarchon corais UF83818 Elaphe radiata Lillywhite unpubl. data Gastropyxis smaragdina UF52721 Gonyosoma oxycephalum Lillywhite unpubl. data Lampropeltis getula Klauber 1943 Lampropeltis triangulum UF68828 Lycodon laoensis UF69087 Masticophis flagellum Klauber 1943 Masticophis lateralis Klauber 1943 Mastigodryas boddaerti UF91619 Opheodrys aestivus UF43623 Oxybelis fulgidus UF56396 Oxybelis aeneus Sheehy unpubl. data Pantherophis obsoleta Lillywhite unpubl. data Philothamnus dorsalis Schmidt and Noble 1998 Philothamnus irregularis Broadley and Cock 1975 Philothamnus semivariegatus Broadley and Cock 1975 Philothamnus angolensis UF53342 Philothamnus hoplogaster Broadley and Cock 1975 Phyllorynchus browni Klauber 1943 Phyllorynchus decurtatus Klauber 1943

Table 2-1. Continued Family Subfamily Species Source Colubridae Colubrinae Pituophis catenifer Klauber 1943 Pituophis melanoleucus UF132981 Prosymna ambigua Schmidt and Noble 1998 Prosymna bivittata Broadley and Cock 1975 Prosymna stuhlmannii Broadley and Cock 1975 Prosymna sundevallii Broadley and Cock 1975 Sonora michoacanensis Klauber 1943 Spilotes pullatus UF56320 Stilosoma extenuatum Lillywhite unpubl. data Tantilla planiceps Klauber 1943 Tantilla relicta Lillywhite unpubl. data Tantilla hendersoni Stafford 2004 Tantilla melanocephala UF40711 Telescopus semiannulatus Broadley and Cock 1975 Thelotornis capensis Broadley and Cock 1975 Thrasops jacksonii UF52696

Dipsadinae Adelphicos quadrivirgatus Klauber 1943 Atractus depressiocellus Myers 2003 Atractus hostilitractus Myers 2003 Atractus clarki Myers 2003 Atractus darienensis Myers 2003 Carphophis amoenus UF43842 Diadophis punctatus UF56868 Dipsas catesbyi Harvey unpubl. data Dipsas indica Harvey unpubl. data Dipsas peruana Harvey unpubl. data Dipsas boettgeri Harvey unpubl. data Dipsas chaparensis Harvey unpubl. data Hypsiglena torquata Klauber 1943 Imantodes cenchoa UF11284 Leptodeira annulata Duellman 1958 Leptodeira septentrionalis Duellman 1958 Leptodeira frenata Duellman 1958 Leptodeira bakeri Duellman 1958 Leptodeira nigrofasciata Duellman 1958 Leptodeira maculata Duellman 1958 Leptodeira punctata Duellman 1958

Table 2-1. Continued Family Subfamily Species Source Colubridae Colubrinae Taeniophallus brevirostris Schargel et al. 2005 Thamnodynastes pallidus UF88631 Tretanorhinus variabilis UF119241

Homalopsinae Cerberus rynchops Lillywhite unpubl. data Enhydris enhydris Lillywhite unpubl. data

Natricinae Natriciteres olivacea Broadley and Cock 1975 Natrix natrix UF116535 Nerodia fasciata UF41022 Nerodia floridana UF109763 Nerodia sipedon UF63519 Nerodia taxispilota Lillywhite unpubl. data Nerodia rhombifer Lillywhite unpubl. data Regina alleni UF99998 Regina septemvittata UF68506 Seminatrix pygaea UF42444 Storeria dekayi Lillywhite unpubl. data Thamnophis hammondii Klauber 1943 Thamnophis ordinoides UF57050 Thamnophis sirtalis UF42468 Virginia valeriae UF54122 Xenochrophis flavipunctatus Lillywhite unpubl. data

Psammophiinae Psammophis biseriatus UF52841 Psammophis punctulatus UF52832 Psammophis sibilans Broadley and Cock 1975 Psammophis angolensis Broadley and Cock 1975 Psammophis brevirostris Broadley and Cock 1975 Psammophis crucifer Broadley and Cock 1975 Psammophis jallae Broadley and Cock 1975 Psammophylax tritaeniatus Broadley and Cock 1975 Rhamphiophis oxyrhynchus UF59339 Rhamphiophis rostratus Broadley and Cock 1975

Pseudoxyrhophiinae Dromicodryas bernieri USNM 499459 Ithycyphus miniatus USNM 149366

Table 2-1. Continued Family Subfamily Species Source Colubridae Pseudoxyrhophiinae Langaha pseudoalluaudi Domergue 1988 Langaha madagascariensis Guibé 1949 Langaha alluaudi Guibé 1949 Leioheterodon madagascariensis Sheehy unpubl. data Leioheterodon modestus Sheehy unpubl. data Micropisthodon ochraceus Domergue 1993

Xenodontinae Alsophis antillensis UF53983 Alsophis cantherigerus UF44287 Alsophis portoricensis UF57211 Alsophis vudii UF99946 Antillophis parvifrons UF23131 Arrhyton funereum UF113638 Clelia clelia UF34331 Darlingtonia haetiana UF55681 Drepanoides anomalus Dixon and Soini 1986 Erythrolamprus aesculapii UF115664 Farancia abacura Lillywhite unpubl. data Helicops angulatus UF88643 Heterodon nasicus UF56015 Heterodon platirhinos UF44172 Hydrodynastes gigas UF20576 Hydrops caesurus Scrocchi et al. 2005 Hypsirhynchus ferox UF60786 Ialtris dorsalis UF85307 Liophis typhlus UF32985 Oxyrhopus petola UF62069 Philodryas baroni Lillywhite unpubl. data Pseudoboa coronata UF117617 Pseudoeryx plicatilis UF86909 Siphlophis cervinus UF95759 Uromacer catesbyi UF23158 Uromacer frenatus UF23170 Uromacer oxyrhynchus UF23172 Xenodon severus UF87926 Xenoxybelis boulengeri Duellman 2005

Cylindrophiidae Cylindrophis ruffus UF51669

Table 2-1. Continued Family Subfamily Species Source Elapidae Elapinae Aspidelaps scutatus Broadley and Cock 1975 Bungarus fasciatus Sheehy unpubl. data Dendroaspis angusticeps Broadley and Cock 1975 Dendroaspis polylepis Broadley and Cock 1975 Dendroaspis viridis Sheehy unpubl. data Elapsoidea guentheri Broadley and Cock 1975 Elapsoidea semiannulata Broadley and Cock 1975 Elapsoidea sundevallii Broadley and Cock 1975 Elapsoidea nigra Klauber 1943 Hemachatus haemachatus Broadley and Cock 1975 Micrurus fulvius Lillywhite unpubl. data Naja melanoleuca Broadley and Cock 1975 Naja haje Broadley and Cock 1975 Naja mossambica Broadley and Cock 1975 Naja atra Lillywhite unpubl. data Naja kaouthia Lillywhite unpubl. data

Hydrophiinae Aipysurus laevis Lillywhite unpubl. data Emydocephalus annulatus Lillywhite unpubl. data Hydrophis melanocephalus Guinea 1981 Laticauda colubrina Guinea 1981 Notechis scutatus Lillywhite unpubl. data Pelamis platurus Lillywhite unpubl. data

Leptotyphlophidae Leptotyphlops alfredschmidti Lehr et al. 2002 Leptotyphlops macrops Broadley and Wallach 1996

Tropidophiidae Tropidophiinae Tropidophis morenoi Hedges et al. 2001 Tropidophis haetianus Sheehy unpubl. data

Typhlopidae Rhinotyphlops episcopus Franzen and Wallach 2002 Xenotyphlops grandidieri Wallach and Ineich 1996

Viperidae Crotalinae Agkistrodon contortrix Lillywhite unpubl. data Agkistrodon mokeson Klauber 1943 Agkistrodon piscivorus Lillywhite unpubl. data Atropoides nummifer Sheehy unpubl. data Bothriechis schlegelii Lillywhite unpubl. data

Table 2-1. Continued Family Subfamily Species Source Viperidae Crotalinae Bothrops insularis Klauber 1943 Crotalus atrox Lillywhite unpubl. data Crotalus horridus Lillywhite unpubl. data Crotalus ruber Lillywhite unpubl. data Crotalus cerastes Boundy and Balgooyen 1988 Protobothrops cornutus Herrmann et al. 2004 Trimeresurus gramineus Klauber 1943 Trimeresurus purpureomaculatus Lillywhite unpubl. data Trimeresurus albolabris Lillywhite unpubl. data Tropidolaemus wagleri Sheehy unpubl. data

Viperinae Atheris squamigera Klauber 1943 Atheris chlorechis Sheehy unpubl. data Bitis arietans Broadley and Cock 1975 Bitis atrops Broadley and Cock 1975 Bitis caudalis Broadley and Cock 1975 Bitis gabonica Lillywhite unpubl. data Bitis nasicornis Lillywhite unpubl. data Causus defilippii Broadley and Cock 1975 Causus rhombeatus Broadley and Cock 1975 Macrovipera mauritanica Sheehy unpubl. data Vipera xanthina Lillywhite unpubl. data

Xenopeltidae Xenopeltis unicolor UF50268

Table 2-2. Total variation in relative tail-lengths (RTL) of 26 species of snakes. The data are from adult females only and include species typically categorized as fossorial, terrestrial, semiarboreal and arboreal. In species where the RTL becomes shorter with age, the absolute value of the difference is shown. For sources (Sc), 1 = Broadley 1959; 2 = Klauber 1943. min max max - Family Subfamily Species n RTL RTL min Sc Atractaspididae Aparallactinae Amblyodipsas unicolor 13 0.06 0.07 1% 1 Boidae Erycinae Charina trivirgata 57 0.11 0.12 1% 2 Colubridae Boodontinae Duberria lutrix 10 0.10 0.12 2% 1 Lamprophis fuliginosus 34 0.11 0.13 2% 1 Pseudaspis cana 50.130.163%1 Colubrinae Arizona elegans 25 0.10 0.11 1% 2 Conopsis nasus 70 0.11 0.10 1% 2 Lampropeltis getula 249 0.11 0.10 1% 2 Masticophis flagellum 34 0.19 0.20 1% 2 Phyllorhynchus decurtatus 148 0.09 0.08 1% 2 Rhinocheilus lecontei 23 0.12 0.12 0% 2 Salvadora grahamiae 23 0.18 0.18 0% 2 Sonora michoacanensis 57 0.15 0.15 0% 2 Tantilla planiceps 15 0.15 0.18 3% 2 Dipsadinae Adelphicos quadrivirgatus 62 0.11 0.11 0% 2 Diadophis punctatus 183 0.13 0.14 1% 2 Geophis nasalis 87 0.11 0.13 2% 2 Hypsiglena torquata 30 0.12 0.12 0% 2 Natricinae Thamnophis hammondii 153 0.19 0.18 1% 2 Elapidae Elapinae Elapsoidea nigra 29 0.05 0.06 1% 2 Micrurus nigrocinctus 32 0.09 0.09 0% 2 Viperidae Crotalinae Bothrops insularis 94 0.11 0.11 0% 2 Trimeresurus gramineus 16 0.14 0.14 0% 2 Viperinae Atheris squamigera 25 0.12 0.13 1% 2 Bitis arietans 27 0.06 0.09 3% 1 Causus defilippii 22 0.05 0.07 2% 1

Figure 2-1. Composite phylogeny of 227 snake taxa. Species in gray boxes are stenotopically arboreal. Bolded branches denote eurytopically arboreal/terrestrial species. Asterisks denote stenotopically aquatic species. Bolded species exhibit pseudautotomy. Remaining unmarked species are stenotopically terrestrial.

Figure 2-1. Continued

CHAPTER 3 RESULTS

Frequency Distribution

The frequency distribution of raw total lengths for all four gravitational habitat categories is shown in Fig. 3-1. The frequency distribution mean (mm), median, mode and standard deviation within each of the four categories were: stenotopically arboreal (1212, 1050, 1050,

506.5), eurytopically arboreal/terrestrial (1644, 1215, 1680, 1103.6), stenotopically terrestrial

(855.5, 652, 480, 557.7), and stenotopically aquatic (1105, 1000, 1000, 530). Stenotopically arboreal total lengths had the lowest standard deviation, whereas the eurytopically arboreal/terrestrial total lengths had the greatest by more than twofold. Slightly more than half

(52%) of the stenotopically arboreal species were between 60-120 cm total length, and 93.5% were between 50-200 cm total length. There were no stenotopically arboreal species shorter than

50 cm, four species between 201-240 cm (in order of increasing length: Dendroaspis viridis,

Boiga cynodon, Boiga forsteini, and Gonyosoma oxycephalum), and only one species (Leptophis ahaetulla) longer than 240 cm. Several non-stenotopically arboreal snake species have total lengths < 50 cm and > 200 cm (Fig. 3-1).

Gravitational Habitat and Total Body Length

There were differences in total length between the four gravitational habitat categories (P <

0.0001, df = 3, F = 19.433, Fig. 3-1). Mean total length was longer in stenotopically arboreal species than in stenotopically terrestrial species (P < 0.00001), longer in eurytopically arboreal/terrestrial species than in stenotopically terrestrial species (P < 0.00001), and longer in stenotopically aquatic species than in stenotopically terrestrial species (P = 0.0015). However, I did not find a difference in mean total length between stenotopically arboreal and eurytopically arboreal/terrestrial species (P = 0.32), between stenotopically arboreal and stenotopically aquatic

species (P = 0.96), or between eurytopically arboreal/terrestrial and stenotopically aquatic

species (P = 0.24).

There were differences in the variance among the four categories (Fig. 3-2). The

coefficients of variation in order of increasing value are: stenotopically arboreal (CV = 0.011),

stenotopically aquatic (CV = 0.014), eurytopically arboreal/terrestrial (CV = 0.023), and

stenotopically terrestrial (CV = 0.027).

Gravitational Habitat and Tail Length

Perhaps not surprisingly, tail length is correlated with total length (r2 = 0.65, P < 0.0001, n

= 277, Fig. 3-3). Because I did not find a difference in corrected tail-length between

stenotopically arboreal and eurytopically arboreal/terrestrial species (P = 0.30, Fig. 3-4), I

combined these categories into a single scansorial category (Fig. 3-5). The scansorial species

had corrected tail-lengths on average 1.9 times longer than the two non-scansorial categories (P

< 0.0001) (Fig. 3-5). However, I did not find a difference in corrected tail-length between stenotopically terrestrial and stenotopically aquatic species (P = 0.94, Fig. 3-4). The relative tail- lengths for the 227 species included in this study ranged from 1.1% (Rhinotyphlops episcopus) to

48.1% (Uromacer frenatus) (Table 3-1).

Relative Tail-Length, Gravitational Habitat, and Phylogeny

The analysis of covariance (ANCOVA) results supported using the scansorial gravitational habitat category for the independent contrast analyses instead of the separate analyses of the stenotopically and eurytopically arboreal/terrestrial categories. After accounting for the effect of phylogeny on the data, I found a significant relationship between independent contrasts of

2 scansorial macrohabitat use and log10 transformed RTL (r = 0.31, P < 0.0001, Fig. 3-6).

Table 3-1. The 227 species included in this study in order of decreasing relative tail-length (RTL), and with associated categorizations used in analyses. Range (Rg), OW = Old World, NW = New World. Gravitational habitat (Gh), 3 = stenotopically arboreal; 2 = eurytopically arboreal/terrestrial; 1 = stenotopically terrestrial; 0 = stenotopically aquatic. Family Subamily Species RTL Rg Gh Colubridae Xenodontinae Uromacer frenatus 0.481 NW 3 Colubridae Xenodontinae Uromacer catesbyi 0.455 NW 3 Colubridae Xenodontinae Uromacer oxyrhynchus 0.440 NW 3 Colubridae Pseudoxyrhophiinae Langaha alluaudi 0.427 OW 3 Colubridae Pseudoxyrhophiinae Micropisthodon ochraceus 0.414 OW 3 Colubridae Pseudoxyrhophiinae Langaha pseudoalluaudi 0.403 OW 3 Colubridae Xenodontinae Xenoxybelis boulengeri 0.386 NW 3 Colubridae Colubrinae Gastropyxis smaragdina 0.383 OW 3 Colubridae Colubrinae Oxybelis aeneus 0.380 NW 3 Colubridae Psammophiinae Psammophis punctulatus 0.377 OW 2 Colubridae Xenodontinae Antillophis parvifrons 0.371 NW 2 Colubridae Pseudoxyrhophiinae Langaha madagascariensis 0.368 OW 3 Colubridae Colubrinae Thelotornis capensis 0.365 OW 3 Colubridae Colubrinae Opheodrys aestivus 0.355 NW 3 Colubridae Psammophiinae Psammophis biseriatus 0.352 OW 2 Colubridae Xenodontinae Helicops angulatus 0.340 NW 0 Colubridae Colubrinae Ahaetulla nasuta 0.333 OW 3 Colubridae Psammophiinae Psammophis brevirostris 0.333 OW 2 Colubridae Colubrinae Philothamnus semivariegatus 0.325 OW 3 Colubridae Colubrinae Chironius carinatus 0.320 NW 2 Colubridae Colubrinae Oxybelis fulgidus 0.319 NW 3 Colubridae Pseudoxyrhophiinae Ithycyphus miniatus 0.315 OW 3 Colubridae Xenodontinae Alsophis vudii 0.312 NW 2 Colubridae Xenodontinae Arrhyton funereum 0.311 NW 1 Colubridae Psammophiinae Rhamphiophis oxyrhynchus 0.308 OW 2 Colubridae Dipsadinae Imantodes cenchoa 0.306 NW 3 Colubridae Colubrinae Philothamnus angolensis 0.302 OW 3 Colubridae Xenodontinae Alsophis portoricensis 0.302 NW 2 Colubridae Colubrinae Dendrelaphis pictus 0.300 OW 3 Colubridae Colubrinae Masticophis lateralis 0.298 NW 2 Colubridae Psammophiinae Psammophis angolensis 0.296 OW 1 Colubridae Colubrinae Philothamnus irregularis 0.295 OW 3 Colubridae Xenodontinae Alsophis cantherigerus 0.293 NW 2 Colubridae Psammophiinae Psammophis jallae 0.293 OW 2 Colubridae Xenodontinae Ialtris dorsalis 0.293 NW 1 Colubridae Colubrinae Mastigodryas boddaerti 0.288 NW 2 Colubridae Psammophiinae Rhamphiophis rostratus 0.285 OW 2 Colubridae Dipsadinae Leptodeira punctata 0.283 NW 2 Colubridae Psammophiinae Psammophis sibilans 0.280 OW 2 Colubridae Colubrinae Spilotes pullatus 0.279 NW 2

Table 3-1. Continued Family Subamily Species RTL Rg Gh Colubridae Natricinae Xenochrophis flavipunctatus 0.278 OW 1 Colubridae Xenodontinae Alsophis antillensis 0.278 NW 1 Colubridae Boodontinae Grayia smythii 0.277 OW 1 Colubridae Colubrinae Dispholidus typus 0.276 OW 3 Colubridae Colubrinae Thrasops jacksonii 0.275 OW 3 Colubridae Colubrinae Philothamnus hoplogaster 0.275 OW 2 Colubridae Colubrinae Masticophis flagellum 0.269 NW 2 Elapidae Elapinae Dendroaspis viridis 0.260 OW 3 Elapidae Elapinae Dendroaspis angusticeps 0.258 OW 3 Colubridae Dipsadinae Dipsas catesbyi 0.257 NW 3 Colubridae Xenodontinae Philodryas baroni 0.256 NW 3 Colubridae Dipsadinae Dipsas boettgeri 0.256 NW 3 Colubridae Colubrinae Philothamnus dorsalis 0.255 OW 3 Colubridae Colubrinae Coluber constrictor 0.250 NW 2 Colubridae Dipsadinae Dipsas chaparensis 0.248 NW 3 Colubridae Natricinae Nerodia taxispilota 0.247 NW 2 Colubridae Dipsadinae Dipsas bucephala 0.245 NW 3 Colubridae Natricinae Nerodia fasciata 0.240 NW 2 Colubridae Pseudoxyrhophiinae Dromicodryas bernieri 0.240 OW 1 Colubridae Natricinae Regina septemvittata 0.239 NW 2 Colubridae Colubrinae Tantilla hendersoni 0.239 NW 1 Colubridae Colubrinae Gonyosoma oxycephalum 0.236 OW 3 Colubridae Natricinae Thamnophis ordinoides 0.234 NW 1 Colubridae Xenodontinae Drepanoides anomalus 0.232 NW 1 Colubridae Xenodontinae Hypsirhynchus ferox 0.230 NW 1 Colubridae Colubrinae Boiga cynodon 0.229 OW 3 Colubridae Dipsadinae Dipsas peruana 0.229 NW 3 Colubridae Natricinae Thamnophis hammondii 0.229 NW 1 Colubridae Dipsadinae Thamnodynastes pallidus 0.228 NW 2 Colubridae Natricinae Natriciteres olivacea 0.228 OW 1 Colubridae Natricinae Nerodia rhombifer 0.227 NW 2 Colubridae Colubrinae Dipsadoboa aulica 0.226 OW 3 Colubridae Dipsadinae Leptodeira bakeri 0.226 NW 2 Colubridae Colubrinae Boiga blandingii 0.226 OW 3 Colubridae Natricinae Nerodia floridana 0.224 NW 2 Colubridae Dipsadinae Leptodeira annulata 0.224 NW 3 Colubridae Natricinae Nerodia sipedon 0.224 NW 2 Colubridae Xenodontinae Darlingtonia haetiana 0.223 NW 1 Colubridae Xenodontinae Siphlophis cervinus 0.222 NW 3 Colubridae Psammophiinae Psammophis crucifer 0.220 OW 1 Colubridae Dipsadinae Leptodeira septentrionalis 0.219 NW 2 Colubridae Natricinae Thamnophis sirtalis 0.217 NW 1 Colubridae Natricinae Regina alleni 0.215 NW 1 Colubridae Colubrinae Dinodon semicarinatum 0.214 OW 2 Colubridae Colubrinae Tantilla planiceps 0.211 NW 1

Table 3-1. Continued Family Subamily Species RTL Rg Gh Colubridae Dipsadinae Leptodeira frenata 0.209 NW 2 Colubridae Natricinae Storeria dekayi 0.208 NW 1 Boidae Boinae Corallus ruschenbergerii 0.207 NW 3 Colubridae Psammophiinae Psammophylax tritaeniatus 0.207 OW 1 Colubridae Colubrinae Tantilla relicta 0.203 NW 1 Colubridae Dipsadinae Diadophis punctatus 0.203 NW 1 Colubridae Dipsadinae Leptodeira maculata 0.202 NW 2 Elapidae Elapinae Dendroaspis polylepis 0.199 OW 2 Colubridae Xenodontinae Pseudoboa coronata 0.199 NW 1 Colubridae Xenodontinae Clelia clelia 0.198 NW 1 Atractaspididae Aparallactinae Aparallactus lunulatus 0.198 OW 1 Colubridae Dipsadinae Tretanorhinus variabilis 0.197 NW 1 Colubridae Pseudoxyrhophiinae Leioheterodon modestus 0.196 OW 1 Colubridae Colubrinae Tantilla melanocephala 0.195 NW 1 Colubridae Dipsadinae Taeniophallus brevirostris 0.194 NW 1 Colubridae Xenodontinae Oxyrhopus petola 0.193 NW 2 Colubridae Homalopsinae Enhydris enhydris 0.192 OW 0 Atractaspididae Aparallactinae Aparallactus capensis 0.190 OW 1 Colubridae Boodontinae Lycodonomorphus leleupi 0.189 OW 1 Atractaspididae Aparallactinae Aparallactus guentheri 0.188 OW 1 Colubridae Natricinae Natrix natrix 0.188 OW 2 Colubridae Colubrinae Dipsadoboa unicolor 0.187 OW 2 Colubridae Dipsadinae Leptodeira nigrofasciata 0.186 NW 2 Colubridae Colubrinae Elaphe radiata 0.184 OW 2 Viperidae Crotalinae Protobothrops cornutus 0.184 OW 3 Colubridae Colubrinae Sonora michoacanensis 0.181 NW 1 Colubridae Colubrinae Dinodon rufozonatum 0.179 OW 2 Colubridae Xenodontinae Liophis typhlus 0.177 NW 2 Colubridae Colubrinae Dasypeltis medici 0.174 OW 2 Elapidae Hydrophiinae Notechis scutatus 0.173 OW 2 Elapidae Elapinae Naja melanoleuca 0.168 OW 2 Colubridae Homalopsinae Cerberus rynchops 0.165 OW 1 Colubridae Colubrinae Lycodon laoensis 0.164 OW 2 Viperidae Crotalinae Trimeresurus gramineus 0.162 OW 3 Colubridae Pseudoxyrhophiinae Leioheterodon madagascariensis 0.160 OW 1 Colubridae Natricinae Seminatrix pygaea 0.160 NW 1 Colubridae Xenodontinae Heterodon platirhinos 0.160 NW 1 Elapidae Elapinae Naja mossambica 0.159 OW 2 Elapidae Elapinae Naja haje 0.158 OW 2 Viperidae Crotalinae Agkistrodon piscivorus 0.157 NW 1 Colubridae Xenodontinae Hydrops caesurus 0.157 NW 1 Viperidae Crotalinae Bothriechis schlegelii 0.157 NW 3 Boidae Boinae Corallus caninus 0.156 NW 3 Viperidae Crotalinae Trimeresurus purpureomaculatus 0.156 OW 3 Colubridae Colubrinae Lampropeltis triangulum 0.151 NW 1

Table 3-1. Continued Family Subamily Species RTL Rg Gh Viperidae Viperinae Atheris chlorechis 0.151 OW 3 Viperidae Crotalinae Trimeresurus albolabris 0.151 OW 3 Colubridae Colubrinae Pantherophis obsoleta 0.150 NW 2 Colubridae Boodontinae Pseudaspis cana 0.150 OW 1 Viperidae Crotalinae Tropidolaemus wagleri 0.149 OW 3 Colubridae Colubrinae Telescopus semiannulatus 0.148 OW 2 Elapidae Elapinae Hemachatus haemachatus 0.148 OW 1 Colubridae Dipsadinae Hypsiglena torquata 0.147 NW 1 Elapidae Elapinae Naja kaouthia 0.146 OW 1 Viperidae Viperinae Atheris squamigera 0.144 OW 3 Elapidae Hydrophiinae Emydocephalus annulatus 0.144 OW 0 Colubridae Colubrinae Drymarchon corais 0.143 NW 2 Colubridae Colubrinae Arizona elegans 0.143 NW 1 Colubridae Colubrinae Prosymna ambigua 0.143 OW 1 Elapidae Elapinae Naja atra 0.141 OW 1 Elapidae Elapinae Aspidelaps scutatus 0.136 OW 1 Colubridae Colubrinae Pituophis catenifer 0.135 NW 1 Elapidae Hydrophiinae Aipysurus laevis 0.134 OW 0 Colubridae Natricinae Virginia valeriae 0.134 NW 1 Colubridae Dipsadinae Carphophis amoenus 0.133 NW 1 Boidae Erycinae Charina trivirgata 0.133 NW 1 Colubridae Colubrinae Lampropeltis getula 0.131 NW 1 Colubridae Boodontinae Mehelya capensis 0.130 OW 2 Colubridae Boodontinae Lamprophis fuliginosus 0.130 OW 1 Tropidophiidae Tropidophiinae Tropidophis morenoi 0.129 NW 1 Colubridae Xenodontinae Pseudoeryx plicatilis 0.129 NW 1 Viperidae Crotalinae Bothrops insularis 0.128 NW 2 Colubridae Xenodontinae Xenodon severus 0.127 NW 1 Tropidophiidae Tropidophiinae Tropidophis haetianus 0.127 NW 2 Colubridae Xenodontinae Hydrodynastes gigas 0.126 NW 1 Boidae Boinae Epicrates striatus 0.125 NW 2 Colubridae Xenodontinae Heterodon nasicus 0.125 NW 1 Colubridae Boodontinae Lamprophis lineatus 0.123 OW 1 Colubridae Colubrinae Chilomeniscus stramineus 0.123 NW 1 Boidae Pythoninae Python molurus 0.122 OW 2 Colubridae Colubrinae Dasypeltis fasciata 0.122 OW 2 Colubridae Colubrinae Crotaphopeltis hotamboeia 0.121 OW 1 Colubridae Colubrinae Dasypeltis scabra 0.120 OW 2 Colubridae Dipsadinae Atractus clarki 0.116 NW 1 Viperidae Viperinae Vipera xanthina 0.115 OW 1 Viperidae Viperinae Macrovipera mauritanica 0.114 OW 1 Colubridae Boodontinae Duberria lutrix 0.113 OW 1 Colubridae Xenodontinae Erythrolamprus aesculapii 0.111 NW 1 Viperidae Crotalinae Agkistrodon contortrix 0.110 NW 1 Colubridae Dipsadinae Atractus hostilitractus 0.107 NW 1

Table 3-1. Continued Family Subamily Species RTL Rg Gh Colubridae Boodontinae Lycophidion variegatum 0.105 OW 1 Boidae Pythoninae Python sebae 0.104 OW 2 Elapidae Hydrophiinae Pelamis platurus 0.104 OW 0 Colubridae Colubrinae Prosymna stuhlmannii 0.103 OW 1 Colubridae Dipsadinae Atractus depressiocellus 0.103 NW 1 Colubridae Xenodontinae Farancia abacura 0.102 NW 1 Boidae Pythoninae Morelia viridis 0.102 OW 3 Xenopeltidae Xenopeltis unicolor 0.100 OW 1 Acrochordidae Acrochordus granulatus 0.099 OW 0 Elapidae Elapinae Elapsoidea sundevallii 0.099 OW 1 Colubridae Colubrinae Phyllorynchus decurtatus 0.097 NW 1 Colubridae Boodontinae Lycophidion capense 0.096 OW 1 Elapidae Hydrophiinae Laticauda colubrina 0.096 OW 0 Viperidae Viperinae Causus rhombeatus 0.096 OW 1 Colubridae Dipsadinae Atractus darienensis 0.095 NW 1 Elapidae Hydrophiinae Hydrophis melanocephalus 0.093 OW 0 Boidae Boinae Boa constrictor 0.090 NW 2 Colubridae Colubrinae Pituophis melanoleucus 0.090 NW 1 Viperidae Crotalinae Atropoides nummifer 0.088 NW 1 Elapidae Elapinae Bungarus fasciatus 0.085 OW 1 Colubridae Colubrinae Prosymna sundevallii 0.085 OW 1 Leptotyphlophidae Leptotyphlops macrops 0.082 OW 1 Colubridae Colubrinae Phyllorynchus browni 0.081 NW 1 Viperidae Crotalinae Crotalus ruber 0.080 NW 1 Viperidae Viperinae Bitis nasicornis 0.080 OW 1 Colubridae Colubrinae Prosymna bivittata 0.080 OW 1 Viperidae Crotalinae Crotalus horridus 0.076 NW 1 Elapidae Elapinae Micrurus fulvius 0.075 NW 1 Viperidae Viperinae Bitis arietans 0.075 OW 1 Elapidae Elapinae Elapsoidea guentheri 0.075 OW 1 Viperidae Crotalinae Crotalus atrox 0.073 NW 1 Colubridae Colubrinae Stilosoma extenuatum 0.073 NW 1 Boidae Boinae Acrantophis dumerili 0.071 OW 1 Atractaspididae Aparallactinae Xenocalamus sabiensis 0.069 OW 1 Atractaspididae Aparallactinae Amblyodipsas ventrimaculatus 0.068 OW 1 Boidae Pythoninae Python regius 0.066 OW 1 Boidae Erycinae Gongylophis muelleri 0.064 OW 1 Atractaspididae Aparallactinae Amblyodipsas polylepis 0.064 OW 1 Elapidae Elapinae Elapsoidea nigra 0.064 OW 1 Viperidae Viperinae Bitis gabonica 0.063 OW 1 Viperidae Crotalinae Crotalus cerastes 0.063 NW 1 Viperidae Viperinae Bitis caudalis 0.063 OW 1 Viperidae Viperinae Bitis atrops 0.062 OW 1 Atractaspididae Aparallactinae Xenocalamus mechowii 0.060 OW 1 Viperidae Viperinae Causus defilippii 0.060 OW 1

Table 3-1. Continued Family Subamily Species RTL Rg Gh Elapidae Elapinae Elapsoidea semiannulata 0.055 OW 1 Atractaspididae Atractaspidinae Atractaspis bibronii 0.052 OW 1 Aniliidae Anilius scytale 0.044 NW 1 Leptotyphlophidae Leptotyphlops alfredschmidti 0.042 NW 1 Typhlopidae Xenotyphlops grandidieri 0.035 OW 1 Cylindrophiidae Cylindrophis ruffus 0.017 OW 1 Typhlopidae Rhinotyphlops episcopus 0.011 OW 1

16 A 14 12 10 8 6 umber of Species N 4 2 0 40 80 120 160 200 240 280 Total Length (cm)

30 B 25

umber of Species 10 N 5

0 40 100 200 300 400 500 600 700 800 900 Total Length (cm)

Figure 3-1. Snake total length frequency distribution. A) Stenotopically arboreal species. B) Eurytopically arboreal/terrestrial species. C) Stenotopically terrestrial species. D) Stenotopically aquatic species.

30 C 25

umber of Species 10 N

0 20 60 100 140 180 220 260 Total Length (cm)

10 9 D 8 7 6 5 4 umber of Species

N 3 2 1 0 40 80 120 160 200 240 280 Total Length (cm)

Figure 3-1. Continued

0.030

n 0.025

0.020

0.015 0.010

Coefficient of Variatio Coefficient 0.005

0.000 Stenotopically Eurytopically Stenotopically Stenotopically Arboreal Arb/Terr Terrestrial Aquatic Gravitational Habitat

Figure 3-2. Coefficients of variation of log10 transformed total length among the four gravitational habitats.

Log(Tail Length) 0.5 1.0 1.5 2.0 2.5

2.2 2.4 2.6 2.8 3.0 3.2 3.4 3.6

Log(Total Length)

2 Figure 3-3. Regression of log10 tail length on log10 total length for 227 snake species (r = 0.65; P < 0.0001).

Log(Tail Length) 0.51.01.52.02.5

2.2 2.4 2.6 2.8 3.0 3.2 3.4 3.6

Log(Total Length)

Figure 3-4. Analysis of covariance (ANCOVA) on corrected tail-length for 227 species of stenotopically arboreal (upper dotted line, open triangles), eurytopically arboreal/terrestrial (lower dotted line, solid circles), stenotopically terrestrial, and stenotopically aquatic (overlapping solid lines, solid circles and open circles respectively) snakes.

Log(Tail Length) 0.5 1.0 1.5 2.0 2.5

2.2 2.4 2.6 2.8 3.0 3.2 3.4 3.6

Log(Total Length)

Figure 3-5. Analysis of covariance (ANCOVA) on corrected tail-length for 227 species of scansorial (dotted line, open triangles), and stenotopically terrestrial and aquatic (overlapping solid lines, solid circles and open squares respectively) snakes.

2.5

1.5

1 Macrohabitat use

0.5

0 -1.75 -1.5 -1.25 -1 -0.75 -0.5 -0.25 Log RTL

Figure 3-6. Independent contrasts of macrohabitat use and log10 transformed relative tail-length (RTL; r2 = 0.31, P < 0.0001). For macrohabitat use, 0 = stenotopically aquatic; 1 = stenotopically terrestrial; 2 = scansorial.

CHAPTER 4 DISCUSSION

Relative Tail-Length, Gravity, and Climbing in Snakes

Gravity is a pervasive force that clearly provides acute challenges to blood circulation in terrestrial vertebrates. These challenges are particularly pronounced in elongate vertebrates such as snakes utilizing complex three-dimensional vertical habitats (Lillywhite 1996). Thus, the ability to regulate blood circulation in vertical habitats or upright postures potentially imposes important constraints on the behavior and morphology of scansorial snake species. Overcoming these cardiovascular constraints has likely resulted in the evolution of novel morphological adaptations as species radiated from terrestrial into arboreal habitats.

A likely consequence of limblessness in snakes is an increase in the selective pressures imposed on various aspects of the body and tail (Polly et al. 2001). This is particularly true in species adapted to the extreme challenges associated with arboreal environments (Lillywhite

1996; Lillywhite and Henderson 2001). Therefore, differences in body and tail characteristics should exist among snake species inhabiting different macrohabitats and, thus, experiencing different selective pressures.

One such morphological change likely involves the total length of stenotopically arboreal species. The distribution frequency of total length for adult stenotopically arboreal species suggests there are constraints limiting total length to between 50 and 200 cm, with few exceptions. There were no stenotopically arboreal species with total lengths < 50 cm as adults.

Because gradients of intravascular and transmural pressures increase with absolute vertical length of a blood column, relatively short species are not strongly affected by the cardiovascular constraints imposed by gravity. Carotid blood flow in the stenotopically terrestrial viper

Agkistrodon piscivorus was less impaired by tilting in smaller than in larger individuals

(Lillywhite and Smits, 1992). Furthermore, Lillywhite and Smits (1992) suggest that gravity

induced cardiovascular constraints on blood circulation limit the total length of arboreal vipers to

about 1 m. For snakes in general, my results indicate that constraints limit total length in adult stenotopically arboreal species to > 50 cm, and that these constraints are not likely cardiovascular.

Insofar as gravity would not seem to be a factor at smaller body size, species < 50 cm may have lesser ability to adequately span gaps, which might result in ecological constraints such as increased vulnerability to predation or decreased hunting success. Because several of the arboreal species included in the distribution frequency have closely related terrestrial species with total lengths < 50 cm (e.g., Trimeresurus), the comparative data support the inference that there are lower limitations on the total length of stenotopically arboreal snakes to > 50 cm.

Similarly, there were few stenotopically arboreal snake species (n = 5) with total lengths >

200 cm suggesting upper level constraints on the total length of these species. The four species between 201-240 cm (in order of increasing length: Dendroaspis viridis, Boiga cynodon, Boiga forsteini, and Gonyosoma oxycephalum) all have relatively long tails, with three having relative

tail-lengths between 23-26% (no length data available for Boiga forsteini, although its relative

tail-length (RTL) should be within this range as well). Only one species (Leptophis ahaetulla)

slightly exceeded 240 cm in total length (247.5 cm), and it also has a relatively long tail (39% of

total length). Snakes > 200 cm are perhaps also negatively influenced by ecological constraints

in complex vertical three-dimensional habitats. Their relatively large mass (particularly in boids)

might restrict movements to thicker branches.

The variance in total length among eurytopically arboreal/terrestrial species was more than

twofold greater than that of stenotopically arboreal species. In fact, the stenotopically arboreal

species had the lowest variance in total length of all four categories. These results further suggest there are constraints limiting total length of stenotopically arboreal species, particularly because I did not find differences in either the mean total length or the mean corrected tail-length between stenotopically and eurytopically arboreal/terrestrial species.

Corrected tail-length of scansorial species was on average 1.9 times longer than that of non-scansorial species (Fig. 3-5). Lengthening the tail relative to the body increases the relative length of blood vessels that are surrounded by tight (low compliance) tissues. This helps to mitigate posterior blood pooling and thereby facilitates blood flow to the heart, brain, and vital organs during the upright positions experienced during climbing (Lillywhite and Gallagher 1985;

Lillywhite 2005). Therefore, the long tails of scansorial snakes can be regarded as one of a suite of characters likely to be adaptive responses to the cardiovascular constraints on blood circulation imposed by gravity (Lillywhite 1987; Lillywhite 2005).

Relative tail-length is positively correlated with absolute tail-length (Fig. 4-1) and likely more important in countering the effects of gravity than absolute tail-length. Snakes with relatively longer tails have a larger percent of dependent vessels contained within the tight integument of the tail and are thus more resistant to dependent transmural pressures experienced during climbing.

I did not find a difference in RTL between stenotopically and eurytopically arboreal/terrestrial species (Fig. 3-4). There are two possible explanations for this. (1) Even though eurytopically arboreal/terrestrial species climb less frequently than stenotopically arboreal species, they still need adaptations to counter the effects of gravity on blood circulation.

This is the most likely explanation, and it could help explain why many eurytopic species that periodically climb (e.g., Coluber constrictor and Masticophis flagellum) have relatively long

tails, but lack prehensile tails. (2) Stenotopically arboreal species might have evolved from

eurytopically arboreal/terrestrial species. Henderson and Binder (1980) proposed this hypothesis

in a review of the ecology and behavior of vine snakes. However, the composite tree in this

study does not support this hypothesis due to lack of resolution (Fig. 2-1). The tree shows two

instances where stenotopically arboreal species likely evolved from eurytopically

arboreal/terrestrial ancestors, and at least four instances where eurytopically arboreal/terrestrial species likely evolved from stenotopically arboreal ancestors (Fig. 2-1). However, there are at

least three instances in which the ancestral state is unclear. Analyses using better resolved

phylogenies at the generic and species level for multiple clades are necessary to thoroughly test this hypothesis.

The relative tail-lengths for the stenotopically aquatic species (9.3% to 19.2%) fall well

within the range for the stenotopically terrestrial species (1.1% to 38.3%). This is likely because the tails of stenotopically aquatic species are affected by the unique selective pressures associated with an essentially weightless environment. In most aquatic environments, the tails do not function in countering the effects of gravity on blood circulation, but rather in propulsion.

Consequently, these species should be expected to have relative tail-lengths long enough to effectively propel the snake through water, yet short enough to minimize drag. Therefore, similarity in RTL between stenotopically aquatic and stenotopically terrestrial species is likely the result of entirely different selective pressures.

Several patterns emerged from the data regarding RTL at the family level. First, the

Viperidae in general have relatively short body lengths, absolute tail lengths, and relative tail- lengths, and these characteristics appear to be retained in arboreal species (Lillywhite and Smits

1992). The results from this study support these observations, with the highest RTL value for an

arboreal viperid in this study being 18.4% for Protobothrops cornutus (Table 3-1). However,

even though vipers tend to be relatively short, Martins et al. (2001) demonstrate that RTL

increases with increasing arboreality in the genus Bothrops. This trend for increased RTL in

scansorial species is further supported by the 25 viperid species included in this study, and it

likely characterizes viperids in general. Similarly, the 11 boid species used in this study tended

to have relatively short tails, although many species are relatively long bodied. The highest RTL

value for a stenotopically arboreal boid was 16.2% for Corallus ruschenbergerii (Table 3-1).

The species with the longest relative tail-lengths were clearly members of the family Colubridae.

The 87 species with the longest RTL values were all colubrids (ranging from 20.8% - 48.1%),

with the only exception of two arboreal elapids (Dendroaspis viridis and Dendroaspis angusticeps) with RTL values of 26.0% and 25.8% respectively (Table 3-1). Although

Dendroaspis polylepis is fast moving and an agile climber, it is primarily terrestrial and has a shorter RTL (19.9%) than its strictly arboreal congeners even though they attain similar total lengths (Branch 1998).

Snake Tails and Defense: Speed and Pseudautotomy

In addition to scansorial species, relatively long tails were also noted in several non- scansorial species characterized by defensive tail loss (pseudautotomy) and/or using speed as a primary means of capturing prey and escaping predators (e.g., Darlingtonia, Drepanoides, and

Thamnophis). In fact, many of these species had RTL values similar to many scansorial species

(RTLs of 29 species included in this study were between 20% and 34%).

Included within this group of species that use their tails to escape predators are species that often swim, but evidence suggests that relatively long tails are not particularly advantageous for either rapid terrestrial locomotion or swimming (Jayne 1988; Jayne and Bennett 1989). Jayne

(1988) found that RTL in Nerodia and Elaphe were about equally effective for swimming,

suggesting the relatively long tails of natricines are not an adaptation for swimming. However, of the 29 species of stenotopically terrestrial species with relatively long tails included in this study, at least 19 are known from the literature to lose their tails in defense. While the relative frequency of tail loss in wild populations cannot always be accurately determined from museum specimens alone due to potential collection bias (Arnold 1988; Jayne and Bennett 1989), these results certainly warrant further investigation.

Many long-tailed terrestrial species are also active, diurnal predators that rely on speed to procure prey (Greene 1997). However, if fast moving terrestrial snakes possess adaptations for speed, and long RTL is not required for speed, then alternative selective pressures are likely responsible for maintaining long tails in these species. Furthermore, because many of these species are known to possess stub tails (Greene 1997), it is reasonable to infer that the long tails of these terrestrial species might be a mechanism for defense. Many of these species rely on speed for escaping predators, and quickly fleeing increases the likelihood of a predatory attempt being directed to the tail instead of the body (Greene 1973). A long tail can subsequently break allowing the snake to escape.

Guyer and Donnelly (1990) used length-mass relationships to divide a Costa Rican snake assemblage of 27 species into four distinct morphological groups and found that, among 603 individuals, the highest frequencies of tail breaks occurred in the leaf litter and terrestrial categories (mean = 0.19 and 0.08 respectively) with the arboreal and semiarboreal categories having the lowest (mean = 0.01 and 0.0 respectively). In fact, the leaf-litter habitat was characterized by having long RTL and high frequency of tail loss (e.g., Coniophanes,

Dendrophidion, Pliocercus, Rhadinaea, and Scaphiodontophis) and, thus, highlighting the apparent prevalence of pseudautotomy in many terrestrial snake species within a single

assemblage. Additional studies of snake assemblages in other areas would be of considerable

use in determining the frequency of pseudautotomy among snake assemblages in diverse ecosystems.

The current dogma regarding pseudautotomy suggests it is a rare phenomenon in snakes

(Arnold 1988; Marco 2002). However, the paucity of information on this topic renders such a

conclusion premature. As more natural history data become available, the number of snake

species observed exhibiting relatively high frequencies of tail loss in wild populations continues

to increase. The sum of these findings suggests that pseudautotomy in snakes is possibly more

common than presently thought and potentially important in understanding the evolution of

relatively long tails in many terrestrial snake species.

However, different functions of tail length need not be mutually exclusive. It is likely that

the long RTL of many eurytopically arboreal/terrestrial species (e.g., Coluber constrictor) serve

the dual purposes of aiding in defense by pseudautotomy, while also countering the effects of

gravity during climbing. Further studies comparing tail characteristics of scansorial and

terrestrial species (e.g., prehension, tail length, presence of fracture planes, size of caudal

vertebra, and muscle mass) would be of considerable interest and I intend to pursue these ideas

in a later study.

0.000

-0.500

-1.000 (RTL) 10

Log -1.500

-2.000

-2.500 0.00 0.50 1.00 1.50 2.00 2.50 3.00

Log10 (absolute tail-length)

Figure 4-1. Regression of absolute tail length on relative tail-length (RTL) for 227 snake species (r2 = 0.64, P < 0.0001).

APPENDIX A STENOTOPICALLY ARBOREAL SPECIES

Table A-1. Stenotopically arboreal species (4 families, 10 subfamilies, 34 genera, 77 species) used for total length frequency distributions; NW = New World, OW = Old World. Family Subfamily Species Rang e Boidae Boinae Corallus annulatus NW Corallus caninus NW Corallus ruschenbergerii NW Pythoninae Morelia viridis OW Colubridae Colubrinae Ahaetulla dispar OW Ahaetulla nasuta OW Ahaetulla prasina OW Ahaetulla pulverulenta OW Boiga cynodon OW Boiga blandingii OW Boiga cyanea OW Boiga forsteini OW Boiga multifasciata OW Boiga ocellata OW Chrysopelea ornata OW Chrysopelea paradisi OW Dendrelaphis cyanochloris OW Dendrelaphis pictus OW Dipsadoboa aulica OW Dispholidus typus OW Drymobius margaritiferus NW Elaphe frenata OW Elaphe prasina OW Gastropyxis smaragdina OW Gonyosoma oxycephalum OW Leptophis ahaetulla NW Leptophis depressirostris NW Opheodrys aestivus NW Oxybelis aeneus NW Oxybelis fulgidus NW Philothamnus angolensis OW Philothamnus dorsalis OW Philothamnus hoplogaster OW Philothamnus irregularis OW Philothamnus semivariegatus OW Thelotornis capensis OW Thelotornis kirtlandii OW Thrasops jacksonii OW Dipsadinae Dipsas boettgeri NW Dipsas catesbyi NW Dipsas chaparensis NW Dipsas indica NW

Table A-1 Continued Family Subfamily Species Rg Colubridae Dipsadinae Dipsas peruana NW Imantodes cenchoa NW Imantodes inornatus NW Leptodeira annulata NW Leptodeira septentrionalis NW Sibon nebulata NW Sibon sartorii NW Psammophiinae Psammophis biseriatus OW Pseudoxyrhophiinae Langaha alluaudi OW Langaha madagascariensis OW Langaha pseudoalluaudi OW Micropisthodon ochraceus OW Stenophis gaimardi OW Stenophis granuliceps OW Xenodontinae Philodryas baroni NW Siphlophis cervinus NW Uromacer catesbyi NW Uromacer frenatus NW Uromacer oxyrhynchus NW Elapidae Elapinae Dendroaspis angusticeps OW Dendroaspis viridis OW Viperidae Crotalinae Bothriechis schlegelii NW Trimeresurus cornutus OW Trimeresurus erythrurus OW Trimeresurus gramineus OW Trimeresurus macrolepis OW Trimeresurus malabaricus OW Trimeresurus medoensis OW Trimeresurus purpureomaculatus OW Tropidolaemus wagleri OW Viperinae Atheris chlorechis OW Atheris hispida OW Atheris nitschei OW Atheris rungweensis OW Atheris squamigera OW

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BIOGRAPHICAL SKETCH

Coleman Sheehy has always had a passionate curiosity about the natural world. Growing up in Richmond, Virginia, his earliest interests centered around dinosaurs, but these interests quickly expanded to include living reptiles and amphibians and, in particular, snakes. Thanks to an encouraging and supportive family, Coleman’s basement, while growing up, was constantly filled with native wildlife he collected on local field excursions. Most of these animals were reptiles and amphibians and it was during these years that Coleman honed many of the observational and field skills that would become such an important aspect of his academic career.

After acquiring his General Education Diploma (GED), Coleman was invited to work at

James River Park in Richmond, where his responsibilities included leading interpretative hikes and float trips through miles of undeveloped, island-dotted habitat along the James River. He also gave hundreds of educational programs focused on introducing the public of all ages to the fascinating reptiles and amphibians native to Virginia and to the importance of their conservation.

Coleman later began working at a local pet store specializing in exotic reptiles and amphibians and, after several years, became general manager of the primary store in Richmond.

It was during this time that Coleman realized many of the problems associated with the pet trade and he sought to resolve many of these by initiating captive breeding programs and by only purchasing or trading captive bred animals. Also during this time, Coleman saved enough money to fund a month-long trip exploring Madagascar. It was during this trip that he met two prominent American herpetologists (Drs. Ronald Nussbaum and Christopher Raxworthy) who strongly influenced his career path. The experience left Coleman with the realization that he could incorporate his love of herpetology and traveling into a successful career through

academia. Coleman subsequently enrolled at J. Sargeant Reynolds Community College in

Virginia and graduated summa cum laude with an Associate in Science in the year 2000. He

then transferred to the University of Florida, where he graduated magna cum laude with a bachelor’s degree in zoology and a minor in wildlife ecology and conservation in 2002.

Coleman has traveled to Madagascar, Honduras, South Africa, Tobago, the Bahamas,

Colombia, Brazil, and Taiwan as well as many states within the US. While working on his master’s, Coleman taught the laboratories for many classes, including Herpetology, the Natural

History of Amphibians and Reptiles, Vertebrate Zoology, Functional Vertebrate Anatomy,

Ecology, Advanced Island Biogeography, and Introductory Biology. He has worked in the herpetology collections of the Florida Museum of Natural History and the Transvaal Museum in

South Africa, and he has presented several talks at scientific meetings. He has also published regularly in peer-reviewed journals since 2001 and, to date, has ten publications including the

description of a new species of frog from Bolivia.

Coleman has been accepted into a Ph.D. program at the University of Texas at Arlington,

where he will pursue his interests in snake systematics, evolutional biology, ecomorphology, and

functional morphology by studying several groups of Central and South American snakes. His

long-term goal is to secure a tenured position in a Museum or University, where he can conduct

research and teach in the areas of herpetology and vertebrate evolution, while also actively promoting the conservation of wildlife worldwide.