Advanced Snakes Research Articles

Why Snakes Have Forked Tongues

The serpent's forked tongue has intrigued humankind for millennia, but its function has remained obscure. Theory, anatomy, neural circuitry, function, and behavior now support a hypothesis of the forked tongue as a chemosensory edge detector used to follow pheromone trails of prey and conspecifics. The ability to sample simultaneously two points along a chemical gradient provides the basis for instantaneous assessment of trail location. Forked tongues have evolved at least twice, possibly four times, among squamate reptiles, and at higher taxonomic levels, forked tongues are always associated with a wide searching mode of foraging. The evolutionary success of advanced snakes might be due, in part, to perfection of this mechanism and its role in reproduction.

On the Phylogenetic Relationship of Colubrinae, Elapidae, and Viperidae and the Evolution of Front-Fanged Venom Systems in Snakes

Phylogenetic relationships among major clades of advanced snakes and the origin of the front-fanged venom systems of elapids and viperids have been the focus of considerable study and debate during the past century, but a general consensus on the resolution of these questions has not been reached. Here we compare DNA sequences of portions of the mitochondrial small and large subunit ribosomal RNA genes for representatives of three major clades of advanced snakes: an elapid (Naja naja), a viperid (Vipera ammodytes), a colubrine (Coluber constrictor), and, for an outgroup, a boid (Boa constrictor). Phylogenetic analysis indicates a close relationship between the elapid and colubrine relative to the viperid. This finding is congruent with the immunological data of Cadle (1988). Essentially no support was found for the hypothesis of a single origin for frontfanged venom systems and sister status for viperids and elapids, as first proposed by Cope (1900). The hypothesis of a basal position for elapids, as proposed by McDowell (1986), was refuted. T WO major groups of snakes possess large, muscular, temporal venom glands and subocular venom ducts leading to front fangs. Elapidae (cobras, kraits, coral snakes, sea snakes, and their allies) constitutes one group, Viperidae (vipers and pitvipers) the other. With the possible exclusion of a small number of prob

Venom Delivery of Snakes as High-Pressure and Low-Pressure Systems

Two fundamentally different venom delivery systems are found among advanced snakes. One is a high-pressure system present in viperids and elapids wherein a pulse of venom is delivered quickly by a sudden pressure surge. The other is a low-pressure system found in some colubrids wherein release of oral secretions is more protracted. These differences help account for the great variation in medical signs and symptoms following bites of humans by colubrid snakes. Further, the high-pressure venom system of elapids and viperids represents an evolutionary innovation in snakes accompanied by a change from a mechanical to a chemical predatory strategy.

Anatomy of the pancreas and langerhans islets in snakes and lizards

The pancreas of snakes (18 species) was comparatively examined and classified into five major types, based on structure of the lobes and ducts, spatial relationships with the spleen and the gall bladder, and the disposition of islet cells. These types trend toward fusion of the pancreatic lobes and compaction of the pancreas--a progression that coincides with the phylogeny of the snakes. The more primitive pancreas of lizards (17 species) also was surveyed; that of Varanus is of special interest because its structure is intermediate between the extended, tri-lobate pancreas of lizards and the compact pancreas of snakes and may represent a transitional link in the evolution of this organ. Islet tissue is always confined to the dorsal lobe and is concentrated in its distal region adjacent to the spleen. In primitive snakes and in Varanus, a large islet mass is sequestered within a distinct juxtasplenic "islet body" distanced from the dorsal lobe and connected to it by a slender stalk. In some of the most advanced snake species, numerous islets of endocrine cells are found within the spleen. The occurrence and formation of these intrasplenic islets is described in detail. The anatomic "affinity" between spleen and the islet region of the pancreas is discussed. A hypothesis for the development of the pancreas from embryonal placodes on the mid-gut is presented; it proposes that the exocrine and the endocrine components derive from different progenitor cells, and that the endocrine progenitors are located in the center of the dorsal placode. The hypothesis combines embryological and evolutionary views about the origin of the pancreas, and offers a rationale for differences in its structure and in the disposition of the islets.

Evolution of the red nucleus and rubrospinal tract

A red nucleus, defined by its relative position in the tegmentum mesencephali, its contralateral rubrospinal or rubrobulbar projections and by crossed cerebellar afferents, is found in terrestrial vertebrates and certain rays. A crossed rubrospinal tract occurs in anurans, limbed urodeles and reptiles, birds and mammals, but is apparently absent in boid snakes, caecilians and sharks. A distinct rubrospinal tract is found in certain rays which use their enlarged pectoral fins for locomotion. A crossed tegmentospinal tract, possibly a rubrospinal tract, is found in lungfishes. Although evidence was presented for a rubrospinal tract in more advanced snakes, the available experimental data in lower vertebrates suggest that the presence of a rubrospinal tract is related to the presence of limbs or limb-like structures. In the connectivity of the red nucleus in terrestrial vertebrates, ‘levels’ of complexity can be distinguished, paralleled by the development of the cerebellum. These ‘grades of organization’ are probably related to the type of motor performance the particular terrestrial vertebrates are capable of.

Morphometrics of the ectopterygoid in advanced snakes (Colubroidea): a concordance of shape and phylogeny

A principal components analysis was performed on 20 measurements of the ectopterygoids of 85 colubroid snakes. This sample encompassed all the shape variation previously recognized in the ectopterygoid of colubroids. Simple proportions which correlate with the first two principal component axes are: relative ectopterygoid length with the first and five measures of absolute or relative head shape with the second. Using these simple proportions colubroid ectopterygoids can be sorted into four shape classes each concordant with a taxonomic grouping: relatively long with broad notched head—Crotalinac; relatively long with narrow, flat head—Viperinae; relatively short with broad, notched head—Colubridae; and relatively short with narrow, flat head—Elapidae. This concordance has an error of about 1000. We propose that these shape classes reflect phylogenetically old and conservative functional differences in the palatomaxillary complexes of the four taxonomic groupings. Other aspects of ectopterygoid shape are described and provisional character state phylogenies for some aspects of the ectopterygoid are presented. Finally, the bearing of our data on the systematics of aparallactines, micrurines, sea snakes, Azemiops and certain other genera are discussed.

Seasonal Production Dynamics of Six Species of Periphyton-Grazing Stream Insects

innovations (e.g., elongate, more movable quadrate and supratemporal bones) could then have allowed boids a broad range of prey types, including many of those currently eaten by advanced snakes. The available data are not consistent with previous suggestions that mammalian prey played an important role in the early evolution of snakes. More recent dietary themes include the consumption of even heavier prey by highly venomous elapids and viperids, sometimes exceeding 150% of the predator's mass. Some other advanced snakes feed frequently on very small items, thereby secondarily resembling lizards in their foraging dynamics.

Dietary Correlates of the Origin and Radiation of Snakes

Stomach analyses of living families and of a fossil containing prey were used to address possible dietary correlates of the history of snakes. Aniliids, morphologically primitive among living snakes, feed on relatively heavy, elongate vertebrates. Large aniliids eat larger prey than do small individuals but, as in advanced snakes, they also take small items. Living boids, structurally intermediate between aniliids and advanced snakes, feed on relatively heavy prey of a much greater variety of shapes than do aniliids. An Eocene fossil that might be a boid contains a relatively large crocodilian in its gut. These findings, previous studies, and morphological considerations suggest that very early snakes used constriction and powerful jaws to feed on elongate, heavy prey. This would have permitted a shift from feeding often on small items to feeding rarely on heavy items, without initially requiring major changes in jaw structure relative to a lizard-like ancestor. Subsequent morphological changes could then have allowed boids to utilize a broad range of prey types, including many of those currently eaten by advanced snakes. More recent dietary themes include the consumption of even heavier prey by highly venomous elapids and viperids, and frequent feeding on relatively small items by some other advanced snakes.

The Hyobranchial Skeleton in Some Little Known Lizards and Snakes

The structure of the hyobranchial skeleton in some burrowing lizards and snakes is analyzed and compared. Anniella is shown to retain hypohyal processes. In Dibamus the hypohyal processes are specialized to support an anterior extension of the aditus laryngis. The only lizards having lost hypohyal processes are those of the genera Acontophiops and Typhlosaurus. These lizards approach primitive and advanced snakes respectively in hyoid structure, and support the view that the hyoid cornua of the alethinophidian hyobranchium correspond to elongated posterolateral limbs of the basihyal which replace the first ceratobranchials. The hyoid of Lan- thanotus bears no special similarity to that of snakes.

THE ROLE OF VENOM DELIVERY STRATEGIES IN SNAKE EVOLUTION.

The recent proposal that front-fanged venom delivery systems have been derived independently from the rear-fanged condition at least five times in the history of snakes (Savitsky, 1978) suggests the need for a reassessment of the role of venom delivery in ophidian history. Despite the fact that serous oral glands have long been known in aglyphous (fangless) and opisthoglyphous (rear-fanged) members of the family Colubridae (see Taub, 1967, p. 1618 for a historical resume), venom delivery has been ascribed a major role only in the evolution of front-fanged snakes. The latter group embraces two polyphyletic assemblages, the solenoglyphs (such as vipers, pit vipers, and mole vipers) with relatively kinetic fang-bearing maxillae, and the proteroglyphs (such as cobras, coral snakes, and seasnakes), which generally possess less mobile maxillae. Both groups possess specialized glands for the secretion and storage of venom and gland-deforming musculature to aid in delivering the venom. My premise is that envenomation has been a key adaptation in determining the success of all of the higher snakes. Furthermore, although envenomation is not the first innovative feeding strategy in ophidian history, its special role in the adaptive radiation of advanced snakes derives from a complex morphological response to changing environmental conditions that embraced both the locomotor and feeding systems of snakes. The current fluid nature of ophidian

The sound-transmitting apparatus in primitive snakes and its phylogenetic significance

The structure of the sound-transmitting apparatus in primitive snakes (Scolecophidia, Henophidia) is reviewed and compared with that of advanced snakes (Caenophidia) and of some fossorial lizards. Assuming a constant course of the chorda tympani, the ophidian stylohyal can be homologized with the intercalary cartilage of lizards while the cartilaginous distal portion of the ophidian stapes represents the internal process. The cladistic significance of the stapes-quadrate-articulation in the Henophidia and Caenophidia is discussed. The Booidea and the Caenophidia show a shift of the stapes-quadrate-articulation which is correlated with changes in the suspensorium as an adaptation to relatively larger prey. However, convergence cannot be ruled out. Dibamus is shown to be the only lizard known so far which approaches the ophidian middle ear structure. Convergence has to be assumed since there is no sign of a stylohyal in Dibamus and since the course of the ramus communicans externus n. facialis cum glossopharyngeo supports the hypothesis that snakes are to be derived from a pre-lacertilian stage of lepidosaurian evolution.

Evolutionary Patterns in Advanced Snakes

One prevalent view of phylogenetic events in advanced snakes holds that the fangs evolved along at least two pathways one (e.g. elapids) from ancestors with enlarged anterior and the other (e.g. viperids) from ancestors with enlarged posterior maxillary teeth. Selective forces driving these changes are presumed to arise from the increasing advantages of teeth and glands in venom injection. In this paper another plausible view of these events is proposed. First fangs of both elapids and viperids likely evolved from real maxillary teeth. In non-venomous snakes, differences in tooth morphology and function suggest that there may be some division of labor among anterior and posterior maxillary teeth. Anterior maxillary teeth, residing forward in the mouth likely serve the biological role of snaring and impaling prey during the strike. They are also conical frequently recurved and lack a secretion groove. On the other hand posterior teeth because of their geometric position on the maxilla and mechanical advantages, tend to serve as aids in preingestion manipulation and swallowing of prey. They are often blade shaped and occasionally bear a secretion groove along their sides. Although both front and rear maxillary teeth of nonvenomous snakes may be elongated this is likely to serve these different functional roles and hence they evolved under different selective pressures. When fangs evolved they did so several times independently but from rear maxillary teeth. In support one notes a) the similar position postorbital of venom and Duvernoy s glands b) similar embryonic development of fangs and rear maxillary teeth c) secretion groove when present, is found only on rear teeth and d) similar biological roles of some rear teeth and fangs. For ease in clearance of the prey during the strike the fangs are positioned forward in the mouth accomplished in viperid snakes by forward rotation of the maxilla and elapids by rostral anatomical migration to the front of the maxilla. Second, the adaptive advantage first favoring initial rear tooth enlargement likely centered not on their role in venom injection but rather on their role in preingestion manipulation and swallowing. However once enlarged, teeth would be preadapted for later modification into fangs under selection pressures arising from advantages of venom introduction. This has implications for the function and evolution of associated structures. Besides possibly subduring or even killing of prey the secretion of Duvernoy's gland may be involved in digestion or in neutralizing noxious or fouling products of the prey. The presence or absence of constriction need not be functionally tied to absence or presence of venom injection. The phylogenetic pathways outlined herein were likely traveled several times independently in advanced snakes.

MAJOR ECOLOGICAL AND GEOGRAPHIC PATTERNS IN THE EVOLUTION OF COLUBROID SNAKES.

For most groups of organisms there is little hope of determining much of their phylogenetic history directly from the fossil record. However, phyletic analysis of taxonomic characteristics can afford probabilistic schemes of morphological changes within groups. Coupling measures of divergence from such morphological studies with ecological and geographic knowledge of extant taxa or with fragmentary paleontological materials can produce coherent evolutionary pictures. Even for taxa used as an out-group or baseline reference, the patterns of character data arranged on a phyletic scale (primitivederived) may yield considerable insights into evolutionary processes and history when correlated with ecological and geographic materials. The advanced or colubroid snakes, poorly known from the fossil record, are used here to exemplify this approach. In an attempt to understand the evolutionary development of the venomous solenoglyphous snakes, we made a survey of characteristics of the Colubroidea, the diverse and complex group to which they belong. The Colubroidea includes the families Colubridae (harmless snakes), Elapidae (cobras, coral snakes, etc.), Hydrophiidae (sea-snakes), and Viperidae (vipers and pit-vipers). Twenty-four integumentary and 26 skull characters from a sample of 508 species of extant advanced snakes were analyzed phyletically (Marx and Rabb, 1972). For many of the scutellation features, data were available in the literature on an additional 500 species. Our methodology and rationale for the analysis of characters and the taxonomic sample employed are recorded elsewhere (Marx and Rabb, 1970; 1972). Basically we attempted to determine the primitive and derived states for each character, using relative frequencies of occurrences in the ancestral or out-group as the primary basis for decisions (see also p. 74). The Colubridae (sensu lato) was used as the out-group. The characters varied widely in their taxonomic distributions, and for some, the phyletic information content is very low. Nevertheless, a sufficient number of the characters are substantial ones that allow useful overall characterization of segments of the sample in respect to morphology, ecology and zoogeography. On the basis of this analysis, this paper focuses on primitive and derived members of the Colubroidea and, more particularly, of the Colubridae.

Character analysis: an empirical approach applied to advanced snakes

Fifty characters of extant advanced snakes were selected for phyletic analysis, with the primary aim of determining evolutionary paths of the venomous taxa. The characters chosen showed roughly equivalent variation. States of characters were distinguished with reference to range of variation at species and generic levels. The heterogeneous, widespread and abundant family Colubridae was designated as representing the ancestral group. Direction of change in states was then determined by reference to colubrid conditions. Criteria used for judgement of direction were (1) uniqueness, (2) relative abundance, (3) correlation of derived states, (4) morphological specialization, (5) ecological specialization, (6) geographic restriction, (7) closely related taxa, and (8) correlation of applicable criteria. Two other criteria, (9) genetic structure and (10) fossil record, were not applicable.Characters used as examples of the approach are number of palatine teeth and the pattern of the head shields. In the latter, the derivative states are correlated with particular modes of life (aquatic, fossorial and terrestrial). The familial level taxa show rather different frequency distributions in respect to the four states of this character, with one derived state unique to the viperids.The second character, number of palatine teeth, was divided into classes by using a span covering most intraspecific variation. The resulting classes were lumped into four states emphasizing the classes of low numbers of teeth. The extreme derived states are correlated in the colubrids with distinctive modes of life (burrowing and digging) and with functional morphological specializations. The distribution of the states shows a trend toward low numbers of teeth in all the venomous families.