Functional plasticity of the venom delivery system in snakes with a focus on the poststrike prey release behavior

We explored variations in the morphology and function of the envenomation system in the four families of snakes comprising the Colubroidea (Viperidae, Elapidae, Atractaspididae, and Colubridae) using our own prey capture records and those from the literature. We first described the current knowledge of the morphology and function of venom delivery systems and then explored the functional plasticity found in those systems, focusing on how the propensity of snakes to release prey after the strike is influenced by various ecological parameters. Front-fanged families (Viperidae, Elapidae, and Atractaspididae) differ in the morphology and topographical relationships of the maxilla as well as in the lengths of their dorsal constrictor muscles (retractor vomeris; protractor, retractor, and levator pterygoidei; protractor quadrati), which move the bones comprising the upper jaw, giving some viperids relatively greater maxillary mobility compared to that of other colubroids. Rear-fanged colubrids vary in maxillary rotation capabilities, but most have a relatively unmodified palatal morphology compared to non-venomous colubrids. Viperids launch rapid strikes at prey, whereas elapids and colubrids use a variety of behaviors to grab prey. Viperids and elapids envenomate prey by opening their mouth and rotating both maxillae to erect their fangs. Both fangs are embedded in the prey by a bite that often results in some retraction of the maxilla. In contrast, Atractaspis (Atractaspididae) envenomates prey by extruding a fang unilaterally from its closed mouth and stabbing it into the prey by a downward-backwards jerk of its head. Rear-fanged colubrids envenomate prey by repeated unilateral or bilateral raking motions of one or both maxillae, some aspects of which are kinematically similar to the envenomation behavior in Atractaspis. The envenomation behavior, including the strike and prey release behaviors, varies within families as a function of prey size and habitat preference. Rear-fanged colubrids, arboreal viperids, and elapids tend to hold on to their prey after striking it, whereas atractaspidids and many terrestrial viperids release their prey after striking it. Larger prey are more frequently released than smaller prey by terrestrial front-fanged species. Venom delivery systems demonstrate a range of kinematic patterns that are correlated to sometimes only minor modifications of a common morphology of the jaw apparatus. The kinematics of the jaw apparatus are correlated with phylogeny, but also show functional plasticity relating to habitat and prey.     

Specializations of the Body Form and Food Habits of Snakes

Viperid snakes have stouter bodies, larger heads, and longerjaws than snakes in other families; there are no major differencesbetween the two subfamilies of vipers in these features. A suiteof morphological characters that facilitates swallowing largeprey finds its greatest expression among vipers, but certainelapid and colubrid snakes have converged upon the same bodyform. The number of jaw movements required to swallow prey islinearly related to the size of a prey item when shape is heldconstant. Very small and very large prey are not disproportionatelydifficult for a snake to ingest. Vipers swallow their prey withfewer jaw movements than do colubrids or boids and can swallowprey that is nearly three times larger in relation to theirown size. Proteolytic venom assists in digestion of prey, andmelanin deposits shield the venom glands from light that woulddegrade the venom stores. Ancillary effects of the morphologicalfeatures of vipers, plus the ability to ingest a very largequantity of food in one meal, should produce quantitative andqualitative differences in the ecology and behavior of vipersand other snakes.     

Higher-level snake phylogeny inferred from mitochondrial DNA sequences of 12S rRNA and 16S rRNA genes

Portions of two mitochondrial genes (12S and 16S ribosomal RNA) were sequenced to determine the phylogenetic relationships among the major clades of snakes. Thirty-six species, representing nearly all extant families, were examined and compared with sequences of a tuatara and three families of lizards. Snakes were found to constitute a monophyletic group (confidence probability [CP] = 96%), with the scolecophidians (blind snakes) as the most basal lineages (CP = 99%). This finding supports the hypothesis that snakes underwent a subterranean period early in their evolution. Caenophidians (advanced snakes), excluding Acrochordus, were found to be monophyletic (CP = 99%). Among the caenophidians, viperids were monophyletic (CP = 98%) and formed the sister group to the elapids plus colubrids (CP = 94%). Within the viperids, two monophyletic groups were identified: true vipers (CP = 98%) and pit vipers plus Azemiops (CP = 99%). The elapids plus Atractaspis formed a monophyletic clade (CP = 99%). Within the paraphyletic Colubridae, the largely Holarctic Colubrinae was found to be a monophyletic assemblage (CP = 98%), and the Xenodontinae was found to be polyphyletic (CP = 91%). Monophyly of the henophidians (primitive snakes) was neither supported nor rejected because of the weak resolution of relationships among those taxa, except for the clustering of Calabaria with a uropeltid, Rhinophis (CP = 94%).      

Evolutionary Patterns in Advanced Snakes

One prevalent view of phylogenetic events in advanced snakesholds that the fangs evolved along at least two pathways one(e.g. elapids) from ancestors with enlarged anterior and theother (e.g. viperids) from ancestors with enlarged posteriormaxillary teeth. Selective forces driving these changes arepresumed to arise from the increasing advantages of teeth andglands in venom injection. In this paper another plausible viewof these events is proposed. First fangs of both elapids and viperids likely evolved fromreal maxillary teeth. In non-venomous snakes, differences intooth morphology and function suggest that there may be somedivision of labor among anterior and posterior maxillary teeth.Anterior maxillary teeth, residing forward in the mouth likelyserve the biological role of snaring and impaling prey duringthe strike. They are also conical frequently recurved and lacka secretion groove. On the other hand posterior teeth becauseof their geometric position on the maxilla and mechanical advantages,tend to serve as aids in preingestion manipulation and swallowingof prey. They are often blade shaped and occasionally bear asecretion groove along their sides. Although both front andrear maxillary teeth of nonvenomous snakes may be elongatedthis is likely to serve these different functional roles andhence they evolved under different selective pressures. Whenfangs evolved they did so several times independently but fromrear maxillary teeth. In support one notes a) the similar positionpostorbital of venom and Duvernoy s glands b) similar embryonicdevelopment of fangs and rear maxillary teeth c) secretion groovewhen present, is found only on rear teeth and d) similar biologicalroles of some rear teeth and fangs. For ease in clearance ofthe prey during the strike the fangs are positioned forwardin the mouth accomplished in viperid snakes by forward rotationof the maxilla and elapids by rostral anatomical migration tothe front of the maxilla. Second, the adaptive advantage first favoring initial rear toothenlargement likely centered not on their role in venom injectionbut rather on their role in preingestion manipulation and swallowing.However once enlarged, teeth would be preadapted for later modificationinto fangs under selection pressures arising from advantagesof venom introduction. This has implications for the function and evolution of associatedstructures. Besides possibly subduring or even killing of preythe secretion of Duvernoy's gland may be involved in digestionor in neutralizing noxious or fouling products of the prey.The presence or absence of constriction need not be functionallytied to absence or presence of venom injection. The phylogeneticpathways outlined herein were likely traveled several timesindependently in advanced snakes.     

Melanin deposits associated with the venom glands of snakes

Melanin deposits in the heads of both true vipers (Viperinae) and pit vipers (Crotalinae) are concentrated over the dorsal and dorsolateral aspects of the venom glands. This pigment may occur in any or all of six sites which include the epidermis, dermis, tissues covering the venom glands, and the interior of the glands themselves. The extreme localization of these melanin deposits suggests that they shield the venom glands from light. Calculations indicate that without such shielding the light energy penetrating the venom glands in the visible and ultraviolet portions of the solar spectrum would damage the venom-synthesizing apparatus and detoxify stored venom. Elapid and hydrophiid snakes have less dense pigment over the venom gland than vipers. Literature reports indicate that elapid venom is less sensitive to photodetoxification than is venom from vipers. Most colubrid snakes, including several with protein-secreting Duvernoy's glands, have little or no melanin associated with the glands. Venomous colubrids in the genera Ahaetulla, Dryophis, Leptophis, and Oxybelis have pigment over the glands as dense as that seen in vipers. Iridophores probably also shield venom glands from radiation. In puff adders and Gaboon vipers (Bitis) there appears to be an ontogenetic change in the shielding of the venom glands from melanocytes in young individuals to iridophores in adults.     

How tubular venom-conducting fangs are formed

Elapids, viperids, and some other groups of colubroid snakes have tubular fangs for the conduction of venom into their prey. The literature describing the development of venom-conducting fangs provides two contradictory accounts of fang development. Some studies claim that the venom canal forms by the infolding of a deep groove along the surface of the tooth to produce an enclosed canal. In other works the tubular fang is said to form by the deposition of material from tip to base, so that the canal develops without any folding. This study was undertaken to examine fang development and to account for the disagreement in the literature by determining whether fang formation varies among groups of venomous snakes and whether it differs between embryos and adults. Adult and embryonic representatives of elapids and viperids were examined. All fangs examined, elapid and viperid, embryos and adults, were found to develop into their tubular shape by the addition of material to the basal end of the tooth rather than by the folding inward of an ungrooved tooth to form a tubular fang. In some cases, the first fang that develops in embryonic snakes differs morphologically from all those formed subsequently.     

Defensive and infrared reception responses of true vipers, pitvipers, Azemiops and colubrids

It has been suggested that true vipers (Viperidae: Viperinae) possess the ability to detect temperature differences between objects despite the lack of an apparent infrared radiation sensor. We tested the ability to distinguish between heated and unheated targets in three species of pitvipers (Viperidae: Crotalinae), four species of true vipers, two species of colubrids (Colubridae: Natricinae, Colubrinae) and Azemiops feae (Viperidae: Azemiopinae). All species of pitvipers tested could distinguish between the warm and cool targets, while no tested species of true viper, colubrid or Azemiops demonstrated this ability. In addition, pitvipers exhibited behaviors that true vipers or Azemiops did not exhibit. Our results suggest that the tested species of true vipers, Azemiops and colubrids may not posses the ability to sense infrared radiation or do not use it in a defensive context, and suggest that some defensive behaviors are associated with the pit organ in pitvipers.     

Evaluation of cytotoxic activities of snake venoms toward breast (MCF-7) and skin cancer (A-375) cell lines

Snake venoms are mixtures of bioactive proteins and peptides that exhibit diverse biochemical activities. This wide array of pharmacologies associated with snake venoms has made them attractive sources for research into potentially novel therapeutics, and several venom-derived drugs are now in use. In the current study we performed a broad screen of a variety of venoms (61 taxa) from the major venomous snake families (Viperidae, Elapidae and “Colubridae”) in order to examine cytotoxic effects toward MCF-7 breast cancer cells and A-375 melanoma cells. MTT cell viability assays of cancer cells incubated with crude venoms revealed that most venoms showed significant cytotoxicity. We further investigated venom from the Red-bellied Blacksnake (Pseudechis porphyriacus); venom was fractionated by ion exchange fast protein liquid chromatography and several cytotoxic components were isolated. SDS-PAGE and MALDI-TOF mass spectrometry were used to identify the compounds in this venom responsible for the cytotoxic effects. In general, viper venoms were potently cytotoxic, with MCF-7 cells showing greater sensitivity, while elapid and colubrid venoms were much less toxic; notable exceptions included the elapid genera Micrurus, Naja and Pseudechis, which were quite cytotoxic to both cell lines. However, venoms with the most potent cytotoxicity were often not those with low mouse LD₅₀s, including some dangerously venomous viperids and Australian elapids. This study confirmed that many venoms contain cytotoxic compounds, including catalytic PLA₂s, and several venoms also showed significant differential toxicity toward the two cancer cell lines. Our results indicate that several previously uncharacterized venoms could contain promising lead compounds for drug development.     

Antipredatory function of head shape for vipers and their mimics

Most research into the adaptive significance of warning signals has focused on the colouration and patterns of prey animals. However, behaviour, odour and body shape can also have signal functions and thereby reduce predators' willingness to attack defended prey. European vipers all have a distinctive triangular head shape; and they are all venomous. Several non-venomous snakes, including the subfamily Natricinae, commonly flatten their heads (also known as head triangulation) when disturbed. The adaptive significance of this potential behavioural mimicry has never been investigated.We experimentally tested if the triangular head shape typical of vipers offers protection against predation. We compared the predation pressure of free-ranging predators on artificial snakes with triangular-shaped heads against the pressure on replicas with narrow heads. Snakes of both head types had either zigzag patterned bodies, typical of European vipers, or plain (patternless) bodies. Plain snakes with narrower Colubrid-like heads suffered significantly higher predation by raptors than snakes with triangular-shaped heads. Head shape did not, however, have an additive effect on survival in zigzag-patterned snakes, suggesting that species which differ from vipers in colouration and pattern would benefit most from behavioural mimicry. Our results demonstrate that the triangular head shape typical of vipers can act as a warning signal to predators. We suggest that head-shape mimicry may be a more common phenomenon among more diverse taxa than is currently recognised.     

Assembling an arsenal: origin and evolution of the snake venom proteome inferred from phylogenetic analysis of toxin sequences

We analyzed the origin and evolution of snake venom toxin families represented in both viperid and elapid snakes by means of phylogenetic analysis of the amino acid sequences of the toxins and related nonvenom proteins. Out of eight toxin families analyzed, five provided clear evidence of recruitment into the snake venom proteome before the diversification of the advanced snakes (Kunitz-type protease inhibitors, CRISP toxins, galactose-binding lectins, M12B peptidases, nerve growth factor toxins), and one was equivocal (cystatin toxins). In two others (phospholipase A(2) and natriuretic toxins), the nonmonophyly of venom toxins demonstrates that presence of these proteins in elapids and viperids results from independent recruitment events. The ANP/BNP natriuretic toxins are likely to be basal, whereas the CNP/BPP toxins are Viperidae only. Similarly, the lectins were recruited twice. In contrast to the basal recruitment of the galactose-binding lectins, the C-type lectins were shown to be Viperidae only, with the alpha-chains and beta-chains resulting from an early duplication event. These results provide strong additional evidence that venom evolved once, at the base of the advanced snake radiation, rather than multiple times in different lineages, with these toxins also present in the venoms of the "colubrid" snake families. Moreover, they provide a first insight into the composition of the earliest ophidian venoms and point the way toward a research program that could elucidate the functional context of the evolution of the snake venom proteome.     

Dietary Correlates of the Origin and Radiation of Snakes

Stomach analyses of living families and of a fossil containingprey were used to address possible dietary correlates of thehistory of snakes. Aniliids, morphologically primitive amongliving 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 shapesthan do aniliids. An Eocene fossil that might be a boid containsa relatively large crocodilian in its gut. These findings, previousstudies, and morphological considerations suggest that veryearly snakes used constriction and powerful jaws to feed onelongate, heavy prey. This would have permitted a shift fromfeeding often on small items to feeding rarely on heavy items,without initially requiring major changes in jaw structure relativeto a lizard-like ancestor. Subsequent morphological changescould then have allowed boids to utilize a broad range of preytypes, including many of those currently eaten by advanced snakes.More recent dietary themes include the consumption of even heavierprey by highly venomous elapids and viperids, and frequent feedingon relatively small items by some other advanced snakes.     

The mechanism of venom secretion from Duvernoy's gland of the snake Thamnophis sirtalis

The venom glands of snakes of the families Elapidae and Viperidae are thought to have evolved from Duvernoy's gland of colubrid ancestors. In highly venomous snakes elements of the external adductor musculature of the jaw insert fibers directly onto the capsule of the venom gland. These muscles, upon contraction, cause release of contents by increasing intraglandular pressure. In Thamnophis sirtalis, a colubrid, there is no direct connection between Duvernoy's gland and the adductor musculature. The anatomical arrangement of the gland, skull, adductor muscles, and the integument is such that contraction of the muscles may facilitate emptying of the gland. This hypothesis was tested by electrical stimulation of the muscles, which resulted in significantly greater release of secretion than elicited by controls. The results suggest a possible early step in the evolution of a more intimate association between venom glands and adductor musculature in highly venomous snakes.     

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.     

Functional and Numerical Responses of Predators: Where Do Vipers Fit in the Traditional Paradigms?

Snakes typically are not considered top carnivores, yet in many ecosystems they are a major predatory influence. A literature search confirmed that terrestrial ectotherms such as snakes are largely absent in most discussions of predator‐prey dynamics. Here, we review classical functional and numerical responses of predator‐prey relationships and then assess whether these traditional views are consistent with what we know of one group of snakes (true vipers and pitvipers: Viperidae). Specifically, we compare behavioural and physiological characteristics of vipers with those of more commonly studied mammalian (endothermic) predators and discuss how functional and numerical responses of vipers are fundamentally different. Overall, when compared to similar‐sized endotherms, our analysis showed that vipers have: (i) lower functional responses owing primarily to longer prey handling times resulting from digestive limitations of consuming large prey and, for some adults, tolerance of fasting; (ii) stronger numerical responses resulting from higher efficiency of converting food into fitness currency (progeny), although this response often takes longer to be expressed; and (iii) reduced capacity for rapid numerical responses to short‐term changes in prey abundance. Given these factors, the potential for viperids to regulate prey populations would most likely occur when prey populations are low. We provide suggestions for future research on key issues in predator‐prey relationships of vipers, including their position within the classical paradigms of functional and numerical responses.     

Feeding behavior and venom toxicity of coral snake Micrurus nigrocinctus (Serpentes: Elapidae) on its natural prey in captivity

The feeding behavior and venom toxicity of the coral snake Micrurus nigrocinctus (Serpentes: Elapidae) on its natural prey in captivity were investigated. Coral snakes searched for their prey (the colubrid snake Geophis godmani) in the cages. Once their preys were located, coral snakes stroke them with a rapid forward movement, biting predominantly in the anterior region of the body. In order to assess the role of venom in prey restraint and ingestion, a group of coral snakes was 'milked' in order to drastically reduce the venom content in their glands. Significant differences were observed between snakes with venom, i.e., 'nonmilked' snakes, and 'milked' snakes regarding their behavior after the bite. The former remained hold to the prey until paralysis was achieved, whereas the latter, in the absence of paralysis, moved their head towards the head of the prey and bit the skull to achieve prey immobilization by mechanical means. There were no significant differences in the time of ingestion between these two groups of coral snakes. Susceptibility to the lethal effect of coral snake venom greatly differed in four colubrid species; G. godmani showed the highest susceptibility, followed by Geophis brachycephalus, whereas Ninia psephota and Ninia maculata were highly resistant to this venom. In addition, the blood serum of N. maculata, but not that of G. brachycephalus, prolonged the time of death of mice injected with 2 LD(50)s of M. nigrocinctus venom, when venom and blood serum were incubated before testing. Subcutaneous injection of coral snake venom in G. godmani induced neurotoxicity and myotoxicity, without causing hemorrhage and without affecting heart and lungs. It is concluded that (a) M. nigrocinctus venom plays a role in prey immobilization, (b) venom induces neurotoxic and myotoxic effects in colubrid snakes which comprise part of their natural prey, and (c) some colubrid snakes of the genus Ninia present a conspicuous resistance to the toxic action of M. nigrocinctus venom.     

Anurans as prey: an exploratory analysis and size relationships between predators and their prey

The vertebrate predators of post-metamorphic anurans were quantified and the predator–prey relationship was investigated by analysing the relative size of invertebrate predators and anurans. More than 100 vertebrate predators were identified (in more than 200 reports) and classified as opportunistic, convenience, temporary specialized and specialized predators. Invertebrate predators were classified as solitary non-venomous, venomous and social foragers according to 333 reviewed reports. Each of these categories of invertebrate predators was compared with the relative size of the anurans, showing an increase in the relative size of the prey when predators used special predatory tactics. The number of species and the number of families of anurans that were preyed upon did not vary with the size of the predator, suggesting that prey selection was not arbitrary and that energetic constraints must be involved in this choice. The relatively low predation pressure upon brachycephalids was related to the presence of some defensive strategies of its species. This compounding review can be used as the foundation for future advances in vertebrate predator–prey interactions.     

Ascaridoid nematodes of amphibians and reptiles: Ophidascaris Baylis, 1920

The genus Ophidascaris is revised and divided into five groups of species. A key for the species groups is provided. Group 1 (‘filaria’ group) occurs in pythons and a key is provided for differentiating eight species based on fresh and preserved specimens and on developmental patterns. O. papillifera (Linstow, 1898) is redescribed from the type-specimens and is considered to be close or identical to O. niuginiensis, for which Candoia carinatus is recorded as a new host. A key for the differentiation of species in Groups 2 to 5 is based on preserved specimens only. Group 2 (‘obconica’ group) contains (i) O. obconica and O. trichuriformis [= caballeroi] in South American colubrids (further investigation will probably show that O. trichuriformis is a synonym of O. obconica); new host records are Xenodon severus, X. neuwiedii, X. colubrinus, Leptodeira annulata, Thamnodynastes pallidus, Leimadophis poecilogyrus and Boa constrictor; (ii) O. ashi n. sp. (new species name for ‘O. labiatopapillosa’) in North American colubrids, new host records are Nerodia valida, Heterodon nasicus and Storeria occipitomaculata; (iii) O. mombasica in African colubrids; new host records are Psammophis phillipsii and P. sibilans; (iv) O. solenopoion in Madagascan colubrids; (v) O. pyrrhus in Australian elapids; new host records are Cacophis squamulosus, Cryptophis nigrescens, Demansia atra, D. olivacea, Hemiaspis signata, Hoplocephalus bitorquatus, H. stephensi, H. bungaroides and Tropedechis carinatus, it is also recorded in Australia in the colubrid Styporhyncus mairii (new host record) and in Demansia papuensis papuensis and D. olivacea papuensis in Papua New Guinea; (vi) O. piscatori in Asian colubrids; (vii) O. excavata [? = schikhobalovi] in Agkistrodon spp. and possibly other aquatic snakes in Asia; new host record is Agkistrodon halys blomhoffi. Group 3 (‘radiosa’ group) in African viperids contains O. radiosa [ = intorta] in Bitis spp. Specimens from Atheris nitschei, Causus rhombeatus and the colubrid Boaedon lineatus were similar, but showed differences indicating possibility of other species in this group. Group 4 (‘najae’ group) in African elapids and Asian elapids and colubrids contains O. najae [ = daubaylisi]; new host records are Ophiophagus hannah, Boiga cyanea, Elaphe carinata. Group 5 (‘arndti’ group) in South American crotalids and colubrids contains O. arndti [ = travassosi and sprenti] in Crotalus spp. and Bothrops spp.; new host record is B. atrox in Panama. No morphological differentiation except size could be detected between O. arndti in crotalines and O. sicki in colubrids, but in view of difference in the feeding habits of their host, both species names were tentatively sustained; new host records for O. sicki are Xenodon neuwiedii, Leimadophis poecilogyrus, Pseudoboa cloelia, Philodryas patagoniensis and Micrurus frontalis; O. ochoteranai was regarded as a species inquirenda. The following species previously placed in Amplicaecum are placed in Ophidascaris; excavata Hsu & Hoeppli, 1931; schikhobalovi Mozgovoy, 1950; robertsi Sprent & Mines, 1960; longispiculum Oshmarin & Demshin, 1972; orientalis Wang, 1965. The position of Ophidascaris in relation to other ascaridoids is discussed: it is placed within the subfamily Ascaridinae sensu Sprent (1983) containing all other ascaridoids of terrestrial animals. It is concluded that Ophidascaris is in a relatively recent stage of evolution. The most likely centre of dispersal for the genus appears to have been Central Africa with spread in one direction to Asia and thence to the New World and in another direction to Madagascar and Australia.     

Evolution of venom delivery structures in madtom catfishes (Siluriformes: Ictaluridae)

The use of venom to subdue prey or deter predators has evolved multiple times in numerous animal lineages. Catfishes represent one of the most easily recognized, but least studied groups of venomous fishes. Venom glands surround spines on the dorsal and pectoral fins that serve as venom delivery structures. Species of madtom catfishes in the genus Noturus were found to each have one of four venom delivery morphologies: (1) smooth spine with no venom gland; (2) smooth spine with venom gland associated with shaft of spine; (3) serrated spine with venom gland associated with shaft of spine; and (4) serrated spine with venom gland associated with shaft of spine and posterior serrations. Analyses accounting for the phylogenetic history of Noturus species suggest that a serrated pectoral spine with a venom gland is the ancestral condition for the genus. The presence of serrations and a venom gland have been largely conserved among Noturus species, but sting morphology has changed at least five times within the genus. Four of these changes have resulted in a loss of morphological complexity, including the loss of posterior serrations, loss of venom glands associated with the posterior serrations, and one complete loss of the venom gland. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 115–129.