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This book provides an up-to-date summary of the biology of snakes on a global basis. Eight chapters are devoted to general biology topics, including anatomy, feeding, venoms, predation and defense, social behavior, reproduction, evolution, and conservation; eight chapters survey the major snake groups, including blindsnakes, boas, colubrids, stiletto snakes, cobras, sea snakes, and vipers. Details of particular interest, such as coral snake mimicry and the evolution of the0 rattle, are highlighted as special topics. Chapter introductory essays are filled with anecdotes that will tempt nonspecialists to read on, while the book's wealth of comprehensive information will gratify herpeto-culturalists and professional biologists.
Greene's writing is clear, engaging, and full of appreciation for his subject. Michael and Patricia Fogden are known internationally for their outstanding work, and their stunning color photographs of snakes in their natural habitats are a brilliant complement to Greene's text. Here is a scientific book that provides accurate information in an accessible way to general readers, strongly advocates for a persecuted group of animals, encourages conservation--not just of snakes but of ecosystems--and credits science for enriching our lives. In helping readers explore the role of snakes in human experience, Greene and the Fogdens show how science and art can be mutual pathways to understanding.
ABOUT THE AUTHOR
Harry W. Greene is Professor in the Department of Ecology and Evolutionary Biology at Cornell University. He was formerly the Curator of Herpetology the Museum of Vertebrate Zoology, and Professor in the Department of Integrative Biology at the University of California, Berkeley, where he won the campuswide Distinguished Teaching Award in 1993. Michael and Patricia Fogden are acclaimed nature photographers whose work has appeared in such publications as Smithsonian and Natural History, and in books published by Time-Life, National Geographic, and Audubon. They live in Costa Rica.
Serpents have had a checkered history: They may have represented healing to the ancient Greeks and knowledge to the Incas, but for most folks they are appalling pictures of pure malevolence. It is Greene's mission to give the snake a public relations burnishing, to probe "the beauty and intrigue of these animals against the backdrop of science," and he does so in detail, with style, aided and abetted by some 200 glorious, how'd-they-catch-that photographs from the Fogden husband-and-wife team. There is plenty here to engage the dedicated snake fancier—on squamate hemipenises and undifferentiated maxillaries, behavioral ecology and biogeography. But Greene wisely enlivens his herpetological tale with stories from the field—dodging a viper's fangs as he reaches for its head, all the while knee deep in swamp muck—and fascinating sidebars on mimicry, blind snakes on the pheromone trail, snakes near extinction (such as the eastern Timber Rattlesnake), nomenclature (is it any wonder snakes get a bad rap with names like Death Adder, Black Halloween, and Eyelash Pitviper?)—tidbits that allow lay readers a chance to catch their breath. Greene closes with a call for snake conservation, in particular habitat protection, for many of these sedentary, finicky eaters are dependent upon unique, undisturbed landscapes that are currently under attack from developers.
Emerging from this work is a creature less to be reviled than to be admired, demonstrating extraordinary evolutionary adaptability, fabulous variety, and spectacular coloration.
in the "dream time" paintings of Australian aborigines, whereas rural people in the southeastern United States still refer to certain lizards with long, fragile tails as "glass snakes"—focusing on limblessness rather than the external ear openings and eyelids never found on true serpents. Even biologists portray snakes mainly in terms of locomotion and feeding, although two thousand years ago Aristotle hinted at the truth when he linked forked tongues with a "twofold pleasure from savours, their gustatory sensation being as it were doubled." Perhaps this key characteristic is largely overlooked because of human antipathy for all but the most obvious and appealing odors, as well as fuzzy notions about what exactly is a snake.
The lives of serpents are exquisitely permeated by chemical phenomena. If newborn Queen Snakes (Regina septemvittata) are experimentally offered diverse odor samples on cotton swabs, they attack the molecular signature of freshly molted crayfish (the sole item in their natural diet) and ignore all others. Black-tailed Rattlesnakes (Crotalus molossus) use the distinctive spoor of woodrats (Neotoma) to choose strategic ambush sites near the runways and nest entrances of their favored prey. A male Plains Gartersnake (Thamnophis radix) deftly follows females by assessing pheromone trails on vegetation, and tropical snakes presumably distinguish their own kind by odor from among the five or six dozen species in a rain forest. By contrast, fresh-baked bread and barbecue smoke offer us pleasant but uninspiring hints of a chemical worldview. The fragrances of Kelly's hair when I firstawake and of the desert after a thunderstorm are more impressive examples, flooding me with joy and hope before I consciously afford them meaning. And one hot afternoon, cruising mindlessly on a San Joaquin Valley freeway, my daydreams suddenly shifted from rattlesnakes to creamy tomato soup and crackers. Minutes later, passing a huge produce truck and still wondering why visions of childhood snacks had drifted in from nowhere, I realized I'd been traveling in the odor plume of an open load of tomatoes.
Early classifications of reptiles were based mainly on shapes and external structures as seen in museum specimens. Extensive attention to internal characteristics began in the 1800s with A.-M.-Constant Dumeril, a Parisian savant, and blossomed thereafter with studies of lungs, reproductive organs, and vertebrae by Edward D. Cope in the United States. Nevertheless, until the turn of the century even herpetologists still considered some elongate lizards "snakes" and called limbless amphibians "pseudophidians," or false snakes. A fairly stable arrangement consistent with fossils emerged only with the work of French paleontologist Robert Hoffstetter in the 1950s, and the composition of snakes as a group continued to depend on whether certain extinct forms were included. Lists of definitive characteristics have appeared in the past few decades, but most of us couldn't recognize a snake as a snake from "lateral closure of the braincase wall" and other such features!
Novel ways of studying snakes were paralleled over the last two centuries by shifts in the philosophy of biological classification, from imposing order on God's Universe to portraying evolutionary history. Consensus is emerging, influenced by new data and new viewpoints, and relationships among major lineages are increasingly clear. For example, the formal category "Serpentes" includes the most recent common ancestor of extant snakes and all descendants of that ancestor—a definition that emphasizes living, intact organisms (about which more is known) and avoids the problem of whether certain poorly preserved fossils really are "snakes." The oldest evolutionary divergence was between blindsnakes and other serpents, although those two groups are not as different as once thought. Most important, our current concept coincides with neither complete limblessness nor eating really large prey, a fact that would surprise many biologists. Both of those traits actually arose after the origin of snakes, and both also occur in other groups of vertebrates.
With accurate notions of their membership, we can more confidently characterize the evolutionary chronicle of serpents. They arose from nearly limbless lizards, and although some snakes have expansive mouths, others still have the relatively inflexible jaws that typified their common ancestor. In addition to serpentine locomotion and feeding specializations, the origin of snakes foreshadowed an increased reliance on chemical cues—and innovations at both ends! A highly mobile tongue carries molecules to a receptor organ in the roof of the mouth, and the tongue's deeply forked shape facilitates directional localization of an odor's source. Snakes use those structures to explore a chemical world perhaps analogous in complexity and subliminal nuance to the textures and colors we perceive visually. Furthermore, all serpents have paired glands in the tail base from which foul substances are smeared about during encounters with predators. Twin innovations thus underlie a spectacular array of locomotor, feeding, and social activities: forked tongues facilitate intensive searching for mates, places to hide, and food, while tail glands protect otherwise occupied snakes from their enemies. Understanding these and other chemically mediated responses is an exciting challenge for science; meanwhile, the everyday lives of serpents are more easily imagined when I remember Kelly's hair, desert thunderstorms, and that truckload of tomatoes.
Beyond coining scientific names (an activity known as taxonomy), phylogenetic systematics is a branch of biology that discerns the history of evolutionary divergence among organisms and categorizes them accordingly. Within that framework, herpetologists divide and subdivide the 2,700 species of snakes into manageable groups, making sense of diversity by searching for similarities and dissimilarities among them. Throughout this book the numbers in those groups are approximate, both because of uncertainties about the status of some species and because new kinds of snakes are discovered each year.
This chapter introduces scientific nomenclature and common names. Even many biologists are unfamiliar with recent refinements, so some implications of phylogenetic systematics for understanding snakes are explained further in the Appendix. Here I also survey the major groups of snakes as background for the topics that follow, then summarize aspects of their general biology not covered elsewhere in the text.
SCIENTIFIC AND COMMON NAMES
For more than two hundred years biologists have used a binomial nomenclature pioneered by Carl von Linne, in which each species is known by a unique combination of italicized generic and specific names. The words themselves are derived from Latin or Greek or based on Latin endings. For example, the scientific name of the Western Rattlesnake is Crotalus viridis. Its species epithet, the second word, is Latin, meaning "green in color"; that species is one of thirty assigned to the genus Crotalus, based on the Greek word krotalon, meaning "a rattle." A formally named group of organisms, such as the genus Crotalus or the species Crotalus viridis, is called a "taxon." Subspecies, or geographical races within a species, have a third latinized name. In the first subspecies to be described, the subspecies name automatically repeats the species name: for example, the nominate subspecies of the Western Rattlesnake is Crotalus viridis viridis (Prairie Rattlesnake). In subsequently described subspecies a different name follows the specific name, as in Crotalus viridis cerberus (Arizona Black Rattlesnake). Genera and species often are abbreviated, as in C. v. viridis and C. v. cerberus. Definitions and some conceptual problems with species and subspecies are discussed in the Appendix.
Common names have no standing in biological nomenclature yet play an important role in communication among laypeople. I generally use English names in vogue for particular regions but follow personal preference in a few cases—I would as soon call a Black-headed Python (Aspidites melanocephalus) a "Teenage Pimple Serpent" as refer to colubrids of the genus Tantilla by their "standard" common name, blackhead snakes! I capitalize English names for plant and animal species (but not genera and other groups of species), to distinguish them from adjectives (e.g., dwarf, brown). In the interest of compactness, and with "rattlesnake" as a model, I combine words for groups of species (e.g., "seakraits" [Laticauda]), as opposed to single species (e.g., "Gopher Snake" [Pituophis catenifer]), but only when the root is one syllable with five or fewer letters and the modifier has no more than two syllables and six letters (e.g., "coralsnakes" versus "calico snakes" [Oxyrhopus]). English names for some higher taxa (e.g., "boas" for Boidae) are widely familiar, but I invented "dwarf pipesnakes" for Anomochilus; lacking popular alternatives, herpetologists call members of the largest snake family "colubrids" and refer to cobras and their relatives collectively as "elapids." Some laypeople find scientific names difficult, and many biologists are unfamiliar with common and scientific names outside their area of expertise, so I use English names whenever possible and provide scientific names for genera and species at the first mention in each introductory essay, text paragraph, special topic section, and photograph caption. Common and scientific names are cross-referenced in the Index.
SNAKES AND OTHER VERTEBRATES
In traditional Linnean taxonomy, groups above the species level (called "higher taxa") are assigned to ranked categories that supposedly represent older, more inclusive relationships. Genera are groups of similar, presumably related species (e.g., most rattlesnakes in Crotalus); families, denoted by the ending "-idae," are groups of similar, presumably related genera (e.g., cobras, seasnakes, and their relatives in Elapidae); orders are groups of similar, presumably related families (e.g., lizards and snakes in Squamata); and so on. Finer divisions in the ranked categories are sometimes used, most frequently subfamilies (denoted by the ending "-inae," as in Crotalinae for pitvipers, a subfamily within Viperidae). Tribes, denoted by the ending "-ini," are sometimes designated for groups of genera within subfamilies, (e.g., Sonorini for groundsnakes [Sonora] and their relatives within Colubrinae).
In point of fact, traditional classifications often fail to portray evolutionary relationships, as illustrated by the following familiar ranked system:
The above scheme omits the origins of four limbs in the common ancestor of terrestrial vertebrates (there is no named group for all four classes), fails to signify the origin of the shelled egg within that group (there is no named group for mammals, "reptiles," and birds), and ignores the fact that crocodilians and birds are more closely related to each other than either of them is to any of the others—all highly significant events in vertebrate evolution!
By contrast, phylogenetic classifications express evolutionary divergences as equally indented sister taxa (i.e., those most recently sharing a common ancestor; more than two taxa are indented equally when their phylogenetic relationships are uncertain). Each set of descendant, equally indented taxa is referred to by the next higher, less indented name. For e amniotes are each other's closest relatives (they are sister taxa), collectively known as tetrapods; conversely, the oldest evolutionary divergence within tetrapods was between amphibians and their sister taxon, the amniotes. The historical relationships of snakes with other major groups of living terrestrial vertebrates can be retrieved from the following phylogenetic classification (Fig. 1 expresses these relationships as a phylogenetic tree or cladogram; Chapter 15 discusses relationships within Squamata in more detail):
Snakes have diverged from ancestral conditions of the larger taxa to which they pertain, sometimes strikingly so, but also reflect their heritage as members of those more inclusive groups. For example, snakes have a segmented vertebral column, one among many characteristics of Vertebrata (a larger group including Tetrapoda and various fish). They share numerous features typical of tetrapods yet for the most part lack the girdles and limbs used for locomotion by most other members of that group. Like amniotes but unlike amphibians, the first snakes laid shelled eggs with three embryonic membranes (including the amnion, hence the larger group's name), although now many squamates and most mammals are viviparous. Snakes share numerous anatomical characteristics with other reptiles (including birds), by which they all differ from mammals (the sister taxon of reptiles within Amniota).
Among living Reptilia, the sister taxon of Squamata is Sphenodontida, encompassing two species of New Zealand tuataras (Sphenodon); together squamates and tuataras are named Lepidosauria. All squamates share numerous derived characteristics, including paired copulatory organs in males. Traditionally the approximately 6,700 living species of Squamata have been divided into lizards (Suborder Lacertilia, often inappropriately called Sauria), amphisbaenians (Suborder Amphisbaenia; see p. 48), and snakes (Suborder Serpentes, sometimes called Ophidia). Phylogenetic systematists reject that arrangement because Lacertilia is not monophyletic; monitors (Varanidae), alligator lizards (Anguidae), and their relatives probably are more closely related to snakes than to other lizards, while whiptails (Teiidae) and their relatives might be more closely related to amphisbaenians than to some other lizards (see the Appendix for definitions of monophyly, paraphyly, and polyphyly). Actually, amphisbaenians and snakes are lizards in exactly the same sense that humans are primates, primates are mammals, and so forth.
CLASSIFICATION AND THE DIVERGENCE OF HIGHER SNAKE TAXA
The arrangement of major snake groups herein reflects well-supported evolutionary divergence and monophyletic relationships. Rather than name them all formally, I designate one group by a bracketed list of included taxa; to facilitate discussion, two sets of paraphyletic basal taxa are indicated (framed in quotes; Fig. 2 expresses these relationships as a phylogenetic tree):
Anomochilus (2 species of Indonesian dwarf pipesnakes) is structurally transitional between other alethinophidians and blindsnakes. Dwarf pipesnakes and five other small lineages of basal alethinophidians (once collectively called Anilioidea or anilioids) have undifferentiated or slightly enlarged ventral scales, stout jaws, and rather limited gapes. The other groups of living basal alethinophidians are Uropeltidae (9 genera, 46 species of shield-tailed snakes), Cylindrophis (9 species of Asian pipesnakes), Anilius scytale (Red Pipesnake), Xenopeltis (2 species of Asian sunbeam snakes), and Loxocemus bicolor (Neotropical Sunbeam Snake).
Basal macrostomatans (formerly called Booidea or booids) have moderately enlarged ventral scales and lighter, more mobile jaw elements than basal alethinophidians; in these and some other aspects, they are transitional between the latter and caenophidians. Basal macrostomatans include Bolyeriidae (2 genera, 2 species of Round Island boas) and Tropidophiidae (4 genera, 20 species of dwarf boas), as well as the better known Boidae (8 genera, 40 species of boas, sand boas, and their relatives), and Pythonidae (8 genera, 24 species of pythons). I informally refer to basal alethinophidians, basal macrostomatans, and Acrochordidae together as basal snakes. Although highly specialized for aquatic life, Australasian filesnakes are phylogenetically and structurally transitional between basal macrostomatans and the Colubroidea; together Acrochordidae and Colubroidea are grouped as Caenophidia and informally called "advanced snakes."
Colubroidea encompass Atractaspididae (14 genera, 65 species of stiletto snakes [Atractaspis] and their associates), Colubridae (290 genera, almost 1,700 species of colubrids), Elapidae (63 genera, 272 species of cobras and their relatives), and Viperidae (30 genera, 230 species of vipers and pitvipers). Colubroids share modifications of the skull, such that the maxillary bones are freed from their primitive role for ingestion and available for other specializations. Venomous seakraits and seasnakes (ca. 15 genera and 55 species) sometimes are collectively separated as the Hydrophiidae, but that taxon includes at least two independent invasions of the marine environment by Australasian elapids and thus is polyphyletic.
The timing of major events in snake evolution is not well understood, owing in part to a relatively poor fossil record. It is discussed in more detail in Chapters 8 and 15, but here is a general outline: The group originated in the Mesozoic era, more than 65 million years ago (mya). Within the Cenozoic era that followed (up to the present), advanced snakes probably arose at least as long ago as the Oligocene epoch (35-25 mya). Numerous modern snake genera are known from the Miocene epoch (25-5 mya) and more recent deposits.
Snake heads vary from chunky to elongate and pointed; snakes' trunks may be cylindrical, tapered at each end, or compressed laterally or dorsoventrally. Some scolecophidians and basal snakes have rudimentary pelvic girdles and external hind limbs, but most serpents lack those structures. No snake has even traces of a pectoral girdle or front limbs. The musculoskeletal system of snakes is discussed later with respect to roles in locomotion (Chapter 2) and feeding (Chapter 3). In this book snake size usually is described in terms of the total length (snout-to-vent plus tail) of an average adult.
The internal anatomy of serpents resembles that of other vertebrates, but the viscera are modified to fit a tubular body. Major organs usually are staggered linearly and more elongate than in other squamates; in some snakes one member of a pair of organs is reduced or absent (see p. 49). Most basal snakes have two well-developed lungs, but in blindsnakes and colubroids the left lung is greatly reduced or lost. The right lung extends through much of a snake's body cavity and ends in a sacklike air storage area, especially well developed in seasnakes. A snake's esophagus extends from the mouth almost to midbody and is not sharply differentiated from the stomach; a pyloric valve separates the latter from a looped or coiled small intestine, which in turn empties into a short, straight, large intestine. The liver is elongate and bilobed. Paired kidneys and gonads (ovaries or testes) are staggered beside the midline in the posterior part of the body. There is no urinary bladder. Typically the right ovary is farther toward the head and the right oviduct is longer than the left. Some blindsnakes, some black-headed snakes (Tantilla), and at least one atractaspidid (Polemon notatus) have a single ovary or oviduct, the loss of one member of the pair probably associated with streamlined bodies in these slender, fossorial creatures. As in other reptiles (including birds), the cloaca is a common chamber that separately receives products of the kidneys, large intestine, and reproductive tracts; it opens through the vent.
Like other squamates, male snakes have paired copulatory organs (see Chapter 6 for other differences between the sexes). Each organ is called a hemipenis (literally, "half-penis"), a name that reflects an ancient, erroneous belief that the two grooved structures were pressed together to form a single mammal-like apparatus. Each squamate hemipenis is in fact a blind, inverted cylinder that can be everted through the vent by a combination of hydraulic pressure (from blood sinuses in the organ) and muscle action. Semen travels along a surface channel (the sulcus spermaticus, or sperm groove) into the female's cloaca, and a retractor muscle and reduced blood pressure invert the organ after mating. Hemipenes are stored in the base of the tail when not in use, giving the tails of male snakes a characteristically stouter shape and greater length than those of females.
The biological role of double hemipenes remains intriguing. Each copulatory organ receives sperm from only the testis on its side of the body. Common Kingsnakes (Lampropeltis getula) alternate the right and left hemipenes during successive copulations; Ottoman Vipers (Vipera xanthina) attempt to insert whichever organ is adjacent to a female's vent. Perhaps the squamate arrangement permits frequent copulation while ensuring recovery time for the alternating reproductive tracts. Hemipenes usually vary among species and higher taxa in shape (e.g., simple versus forked), ornamentation (e.g., presence or absence of spines, papillae, etc.), and size. As might be expected, the urogenital anatomy of males and females differs similarly in shape between two species of tree pitvipers (Trimeresurus); inexplicably, hemipenes and female cloacae each vary among populations of the Variable Reedsnake (Calamaria lumbricoidea), but not in ways that make sense in terms of their functional relationships with each other.
Cloacal scent glands are unique to and characteristic of all snakes, a fact that suggests they might have played an important role in the origin and successful radiation of the group. These glands are paired pouches, opening from the tail base into the posterior edge of the cloaca; their typically foul-smelling contents are ejected by muscles and probably deter predators. Some blindsnakes have an additional tail gland of unknown function.
THE INTEGUMENT, COLORATION, AND ECDYSIS
Snake skin resembles that of most other reptiles, in that its scales are folded and thickened portions of the outermost layers, the dermis and epidermis. Each scale consists of an outer surface, an inner surface, a hinge zone where folding occurs, and a thin free margin that usually overlaps adjacent scales—all easily seen on a freshly shed skin. Snake scales are smooth or have longitudinal ridges (known as keels), and they usually overlap other scales posteriorly. Small pits and tubercles are sometimes visible with the naked eye, especially on the head, and the scale surfaces also are marked by microscopic ridges, tubercles, and other structures that differ among species and higher taxa.
Boas, pythons, and many vipers have small, irregularly arranged head scales, in contrast to the large, symmetrical head scales (also known as plates or shields) of most advanced snakes. Moving from front to back over the head, these large scales are the rostral (covering the snout), internasals (usually paired, behind the rostral), prefrontals (usually paired, behind the internasals), supraoculars (often fragmented, just over the eyes), frontal (between the supraoculars), and parietals (paired, behind the frontal). Supralabial (upper) and infralabial (lower) lip scales border the mouths of snakes on each side. Behind each nasal scale (including or adjacent to the nostril) are loreal or preocular scales, or both, and behind each eye, between the supralabials and parietals, are postocular and temporal scales. On the underside of the head, an anterior mental scale generally is followed by large, paired chin shields and smaller gular scales. Most snakes have a longitudinal mental groove between rows of chin scales, but a few groups lack this expansion pleat (e.g., blindsnakes, dwarf pipesnakes [Anomochilus], and some colubroids that feed on slimy invertebrates).
Dorsal body scales typically overlap in diagonal, usually odd-numbered rows; these range from a dozen or so (e.g., ten in Tiger Ratsnake [Spilotes pullatus], thirteen in Asian coralsnakes [Calliophis]) to more than ninety in some seasnakes. In burrowers and other slender species, row counts of dorsal scales are low and relatively constant along the body, whereas in stocky serpents with tapered anterior and posterior parts the numbers are high at midbody and decrease at each end. Males of the Short Seasnake (Lapemis curtus) have spinelike, juxtaposed dorsal scales, and mid-dorsal scales of the bizarre Javan Mudsnake (Xenodermis javanicus) are large, non-overlapping knobs. Most snakes have enlarged, transverse ventral scales, but blindsnakes, most basal alethinophidians, and some seasnakes have scales that are uniform in size throughout the body. Ventral scale counts range from fewer than a hundred (e.g., in some African slug-eaters [Duberria]) to more than five hundred in some seasnakes. In most snakes a transversely enlarged anal scale covers the cloacal opening, marking the boundary between body and tail. Snakes with differentiated ventral scales also have enlarged subcaudal scales under the tail, often paired; these number from fewer than ten (e.g., in some reedsnakes [Calamaria]) to more than two hundred (e.g., in some wolfsnakes [Lycodon]).
Many lizards have crests, casques, and other fancy ornamentations, whereas—perhaps because they would impede locomotion—elaborations of the skin are rare in snakes. Scaly appendages occur on the snouts or over the eyes of some arboreal serpents (e.g., Madagascan Vinesnakes [Langaha nasuta; photos, pp. 124, 125]; also various vipers) and of the aquatic Tentacled Snake (Erpeton tentaculatus; photo, p. 183). Some snakes dig with an enlarged rostral scale, designed like a plow or spade (photo, p. 43). A few species have spikelike tail scales that also might aid in burrowing, and the modified tail tips of some others produce noise during antipredator displays.
Most snake skin colors result from pigments, although Asian sunbeam snakes (Xenopeltis) and some other species have microscopic structures that make their scales iridescent. Some boas, colubrids, and vipers become lighter at night and darken during the day. With age, melanin deposits in the skin often obscure the bright patterns of juvenile snakes; examples of such ontogenetic color shifts include several pitvipers and colubrids that are blotched or bright red as juveniles, then uniformly dark-colored as adults. Color changes sometimes vary geographically within a species, perhaps associated with changes in habitat and defensive responses: As adults, Black Ratsnakes (Elaphe o. obsoleta) are uniformly dark and Yellow Ratsnakes (E. o. quadrivittata) have black stripes on a light background, whereas all juveniles of that species are light brown or gray with a dorsal pattern of dark blotches. Adult Western Rattlesnakes (Crotalus viridis) are contrastingly blotched like their young over most of the range of that species, but some full-grown Arizona Black Rattlesnakes (C. v. cerberus) are sooty black with small golden flecks.
Adult color patterns are constant in most snake species, at least within a population. Well-known polymorphisms, however, include striped versus banded Common Kingsnakes (Lampropeltis getula); striped, banded, and unicolored Prairie Groundsnakes (Sonora semiannulata); and red versus gray or brown estuarine species in Asia (Dog-faced Watersnake [Cerberus rynchops]) and the United States (Salt Marsh Watersnake [Nerodia clarkii]). Although popular with hobbyists, free-living snakes with truly aberrant colors and patterns are easily visible to predators and thus rare. At least in Brazil, most naturally occurring albino snakes are either nocturnal or burrowers, therefore less likely to be seen by enemies, or are venomous and thus especially capable of defense.
Molting (shedding, ecdysis) in reptiles results from cyclical changes in the underlying skin structure; the end result—a shiny new skin—might facilitate growth, renew tissue abraded during locomotion or otherwise damaged, remove ectoparasites, and maximize chemical communication. Most squamates molt in small, ragged pieces over a period of days or weeks, but alligator lizards, amphisbaenians, and snakes typically shed their skins in one piece. Intervals between ecdysis range from a few weeks to several months and vary with temperature, health, growth, and feeding. For several days prior to molting the eyes are clouded gray or blue by fluid between the old and newly formed spectacles; snakes in that condition are usually inactive and sometimes remain hidden. Among those I found "in the blue," a Northern Cat-eyed Snake (Leptodeira septentrionalis) was hidden in a bromeliad, two Terciopelos (Bothrops asper) remained in burrows, several Bushmasters (Lachesis muta) were coiled on the forest floor, and a Lowland Bush Viper (Atheris squamiger) was resting on a branch.
A shedding snake rubs supralabial and infralabial scales free from the mouth's margin, then crawls forward; as a result of the inside-out nature of this process, the tail of the old skin points in the direction of the departing creature. Popular accounts imply that snakes shed against surface objects, but a free-living Indigo Snake (Drymarchon corais) was seen moving rectilinearly while spasmodic jerks loosened the skin and folded it backward; a large Terciopelo (Bothrops asper) simply crawled slowly over wet forest litter, emerging from its old skin in a matter of minutes. Chapter 13 discusses specialized molting behavior in marine snakes.
THE SENSES AND PHYSIOLOGICAL ECOLOGY
Behavior and physiology link an animal with its external environment. Like most other aspects of their biology, elongate shape and limblessness profoundly affect these responses in snakes. Vegetation and other environmental obstacles are more complex at ground level, so visual and auditory cues would be less effective there than they are for elevated organisms. Moreover, snakes evolved from a secretive, perhaps burrowing ancestor and thus relinquished an emphasis on visual and airborne sound cues early in their history.
Unlike most other amniotes, snakes lack external ears; able to perceive some low-frequency airborne sounds, they hear mainly vibrations conducted via the substrate. Ground-borne sounds are transmitted through a snake's body to the quadrate bone (a connection between the lower jaw and the skull) and thence through the columella (middle-ear bone) to the inner ear. Eyes vary from reduced or even absent in blindsnakes to birdlike globes in the Boomslang (Dispholidus typus) and some other colubrids. Usually the eye is protected by a convex spectacle, or brille, but head scales cover the eyes of blindsnakes and a few other taxa. Diurnal snakes have round pupils, and nocturnal species often have vertically elliptical pupils, which shut to a tight slit and thus protect especially sensitive retinas from daylight. Evolutionary history must also influence pupil shape, however, because many facultatively diurnal snakes (e.g., some boas, colubrids, and vipers) have "cat eyes."
Although humans might view ground-level environments as depauperate, the sensory world of snakes is surprisingly rich in tactile, thermal, and chemical cues. An elongate body predisposes heavy reliance on touch, because positional control mechanisms are integral to serpentine locomotion and because increased surface area enhances bodily contact during social encounters. Snake skin is indeed richly supplied with tactile receptors, and these animals seem especially responsive to touch. Pythons and boas also have highly sensitive thermal receptors in the supralabial and infralabial scales, and some vipers probably form infrared images with their facial pits (see p. 254). The Olive Seasnake (Aipysurus laevis) even has photoreceptors on its tail.
Chemical cues are of overriding importance in the lives of all serpents, processed by a sensory system with which we are largely unfamiliar (see the Special Topic in this chapter). Their nostrils, as in other terrestrial vertebrates, are openings for respiration; smell, however, plays a minor role in snake behavior. In contrast, they have elaborated ancestral mechanisms of autarchoglossan lizards to extremes found nowhere else among vertebrates. A deeply forked tongue gathers odor molecules, relative concentrations on the right and left tines indicating the proximity and direction of potential mates, prey, and enemies. Odor molecules are transferred from the tongue tips to the exquisitely sensitive vomeronasal (or Jacobson's) organ. Taste buds, concentrated in tissue along the tooth rows, function after objects have been grasped in the mouth. Later chapters detail the roles of chemical cues in the lives of serpents.
Like most other vertebrates and with the exception of brooding pythons, snakes do not produce enough excess metabolic heat to sustain high body temperatures irrespective of their surroundings; they are ectothermic ("cold-blooded" is best reserved for some humans!). Endothermic birds and mammals burn about ten times as much energy as ectotherms, and that, coupled with insulating feathers or fur, maintains their high body temperatures. Ectothermy does not, however, necessarily imply low or wildly fluctuating body temperatures; some reptiles behaviorally thermoregulate at fairly constant, high levels. Ectotherms often circumvent potential disadvantages of their low-energy lifestyles: snakes cannot sustain high aerobic activity for longer than a few minutes, as only endotherms can, but they escape predators by confrontation or sprinting to inaccessible retreats rather than by winning endurance races. Many endotherms can operate at relatively low temperatures, whereas serpents generally are inactive during harshly cold weather; some snakes, however, are active under surprisingly cold conditions, such as Desert Blacksnakes (Walterinnesia aegyptia) and European Adders (Vipera berus).
Temperature influences the speed at which bodily functions proceed in ectotherms, but extreme temperatures are dangerous for slender creatures, because high surface area/mass ratios dictate rapid heating and cooling rates. Snakes consequently prefer lower body temperatures (averaging around 30 [degrees] C) than many lizards, and most desert serpents are nocturnal. Body elongation, however, has tremendous advantages: Snakes can rapidly warm and become active by extending themselves in the sun or on a hot substrate; they can also conserve heat by coiling. Perhaps more important, differentially exposing small portions of the body lets snakes warm particular organs while remaining hidden and therefore safe from predators.
Snakes lose water through respiration, metabolic wastes, and - the more so because of high surface area/mass ratios - their skin. Like most other tetrapods, snakes preserve water by excreting uric acid (a white semisolid slurry with the feces) instead of urine. Although some undoubtedly visit pools and streams, many species probably drink beads of dew or raindrops from their skin, and Peringuey's Adder (Bitis peringueyi) elevates and flattens its neck to condense coastal desert fog for drinking. Some marine snakes excrete excess salt via a gland under the tongue, whereas Salt Marsh Watersnakes (Nerodia clarkii) simply leave their estuarine habitats to drink and thus avoid the problem of consuming too much sodium. Desert serpents are more resistant to desiccation than species in humid regions, and some psammophiine colubrids may even condition their skin with nasal gland secretions to retard water loss (Chapter9). Snakes seek moist, sheltered microhabitats during dry periods and prior to shedding, when they are especially vulnerable to water loss.
INSTINCT AND MIND: BEHAVIORAL COMPLEXITY IN SNAKES
Ethology has traditionally addressed four questions about behavior, codified by Nobel laureate Niko Tinbergen: its motivational and sensory control; the roles of genetics, maturation, and experience in shaping final form; its advantage in nature; and its evolutionary history. Gordon M. Burghardt confronted these issues by combining undergraduate training in chemistry, rigorous experiments, and an interest in the behavior of young animals. Using the literature on natural history and some everyday cotton swabs, Burghardt's doctoral research launched a generation of snake ethologists; thirty years later, he is bent on revising Tinbergen's manifesto.
As a graduate student, Burghardt presented naive, young snakes with surface washes from various potential prey, using horse meat and distilled water as experimental controls. Plains Gartersnakes (Thamnophis radix) briefly tongue-flicked at extracts of crickets, mice, and the controls, whereas they rapidly attacked and tried to swallow swabs laced with the odors of leeches, worms, fish, or amphibians—all typical prey for that species. Several other natricine colubrids also preferred extracts that coincided with their natural diets; indeed, baby Queen Snakes (Regina septemvittata) reacted only to freshly molted crayfish. Not all species conformed so well to the cotton swab paradigm, but exceptions were still instructive: Wild Butler's Gartersnakes (T. butleri) eat only leeches and worms, but neonates also responded to fish and frog odors, so perhaps their chemosensory preferences have not yet diverged from those of the closely related Plains Gartersnake. Corn Snakes (Elaphe guttata) and Cottonmouths (Agkistrodon piscivorus) scarcely discriminated among the extracts, but both have broad diets that shift with age and thus might be hampered if they had preprogrammed perceptual constraints. Overall, the feeding behavior of young snakes, evoked by specific stimuli and without the necessity of prior experience, nicely matches classical notions of an instinctive or inborn mechanism.
Other researchers have subsequently extended experimental approaches to many aspects of snake behavior, some discussed elsewhere in this book. Burghardt himself pursued a broad range of problems after graduate school, from chemical characterization of snake prey to behavioral development in hand-reared Black Bears (Ursus americanus) and free-living Green Iguanas (Iguana iguana). In his teaching and writing he often stressed Jacob von Uexkuhl's concept of Umwelt, or "outer world"—an animal's perceptions of its surroundings—and two projects sharpened his parallel concerns for the counterconcept of a perceptual inner world. Together we studied Eastern Hog-nosed Snakes (Heterodon platirhinos), establishing that threatened hatchlings consistently bluffed, death-feigned, or both; they had individually distinctive and stable behavioral profiles, although the responses could be modified by experience. Our most dramatic finding was that the little snakes would rapidly and repeatedly death-feign or right themselves and crawl, depending on whether a simulated predator (Gordon or a stuffed owl) watched them or averted its gaze. About the same time, Burghardt acquired a two-headed Black Ratsnake (Elaphe o. obsoleta), promptly named "IM" for the conflicting concepts of instinct and mind, and accumulated many fascinating observations on its behavior. The two heads often struggled over food, and dominance shifted repeatedly over periods of months; one head consistently preferred smaller prey than the other, although over the years each consumed roughly the same total mass.
After decades of studying reptiles and influenced by Donald R. Griffin, Burghardt recently has raised a fifth and controversial question for ethologists: What are the private experiences of animals, and what role does an inner perceptual world play in their lives? Griffin, best known for discovering echolocation in bats, argued that mental events such as consciousness and awareness are indicated by surprising yet effective solutions to changing, unforeseen, and uncommon problems. In this regard the observations on snakes are inconclusive yet provide contrasting, tantalizing insights. IM's two heads seemed ludicrously irrational, with no reduction of conflict in the face of their common need to provision the same body! Hog-nosed snakes, however, meet Griffin's criteria rather well: they behave as if aware of their deceptive and dangerous relation to the predator—as if they rapidly, consciously assess the dynamic and alternative roles of bluffing, death-feigning, and escape.
But does a mere serpent have reflections and intentions? Can one dare speak of the mind of a snake? Burghardt advocates critical anthropomorphism, combining empirical natural history with our perceptions, intuition, and feelings to predict the outcomes of experiments and comparisons—in short, that we use human experience to forge novel, ultimately testable hypotheses about the inner worlds of animals. His approach steers clear of uncritical caricatures of other creatures as little more than poorly formed humans; in the spirit of "nothing ventured, nothing gained," it also rejects strict but stifling objectivism. Perhaps snakes hold special promise for answering ethology's fifth question, because they challenge us to go beyond the language and nonverbal gestures with which we readily identify mental events in fellow humans.
|List of Special Topics|
|1||Classification and General Biology||11|
|2||Locomotion and Habitats||35|
|3||Diet and Feeding||51|
|4||Venomous Snakes and Snakebite||75|
|5||Predators and Defense||97|
|6||Behavior, Reproduction, and Population Biology||117|
|8||Pipesnakes, Boas, and Other Basal Groups||155|
|9||Old World Colubrids||173|
|10||New World Colubrids||191|
|11||Stiletto Snakes and Other African Enigmas||207|
|12||Cobras, Coralsnakes, and Their Relatives||215|
|13||Seakraits and Seasnakes||231|
|14||Vipers, Adders, and Pitvipers||245|
|15||Evolution and Biogeography||267|
|16||Snakes and Others: Past, Present, and Future||285|
|Epilogue: Why Snakes?||303|
|Appendix||Systematics and Evolutionary Inference||307|