How many snakes are venomous and how many are constrictors?

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Data from all 3,631 living species of snakes in The Reptile Database

as of April 2017. I made the assumption that prey-killing behavior

didn't vary within genera, so if I found data for one species in a genus

I applied it to all others in the absence of specific data for those species.

Many people are aware that some snakes constrict their prey, and others use venom to kill their prey. Recently, somebody asked me what the breakdown was, and I had to admit that I didn't know exactly. My initial estimate was that 20% were venomous in a way that is medically-significant to humans, and that probably a similar number of species are opisthoglyphs that use venom that is not life-threatening to humans to subdue their prey (with a decent number of these pending discovery, confirmation, or further investigation). Estimating the percentage of constrictors was more difficult, but I suspected that it was no more than the percentage of snake species that use venom, and probably somewhat less. A lot of people don't realize that there is a huge third category of snakes that just seize their prey and swallow it alive, sometimes subduing it first by crushing it with strong jaws or pinning it to the ground with a coil (which hardly counts as constriction but could be an evolutionary precursor).

This inspired me to do some literature searching, and as I suspected nobody has ever attempted to estimate the exact percentages of snake species that use each kind of prey-killing behavior. As such, I have prepared a preliminary analysis, the full contents of which I intend to make publicly available after peer review. I hope that doing so will stimulate others to publish their observations of feeding behavior in poorly-known snakes (of which there are many), and add to the long history of discussion about the evolution of snake feeding modes, most of which took place before we had a solid grasp on the evolutionary relationships of extant snake families.

I found that the answer to this question is not as simple as it may seem. Many snakes unambiguously use venom or constriction, but many use neither, and some use both! Of course the data are not as detailed or abundant as we would like. What follows is a break-down of the categories I used, and some interesting exceptions that I uncovered.

Constrictors

Unambiguous constrictors make up just 11% of snake species, but include several well-known groups that are common in the popular consciousness, in zoos, and in the pet trade, including:

• Boas: 61 species, including the eponymous Neotropical Boa constrictor, anacondas (Eunectes), and smaller tree and rainbow boas (Corallus, Epicrates, Chilabothrus) as well as several (sub)families of booid snakes from various and sundry locations around the world—Candoia from New Guinea and Melanesia, sand boas (Eryx) from northeast Africa, the Middle East, and southwestern Asia, Charina and Lichanura from North America, Ungaliophis and Exiliboa from Central America, Acrantophis and Sanzinia from Madagascar, and Calabaria from tropical west-central Africa.
• Pythons: 40 species from Africa, Asia, and Australia
• Ratsnakes, kingsnakes, and close relatives: 43 species of New World colubrine colubrids in the clade Lampropeltini and their Old World counterparts, including:
• Lampropeltis kingsnakes, the consummate constrictors, which prey on other constricting snakes and are rarely, if ever, out-constricted because they are capable of exerting 20 kilopascals of pressure, twice as much as a ratsnake (average 10 kPa)
• southwestern North American species in the genera Pseudelaphe, Arizona, Rhinocheilus, Bogertophis, and Senticolis
• Pantherophis ratsnakes, as well as their sister taxon Pituophis (pine, bull, and gophersnakes), which often press their prey against rocks or other solid objects
• 2 species of live-bearing Eurasian Coronella and their close relative, the Frog-eating Rat Snake Oocatochus rufodorsatus from eastern Russia, Korea, Taiwan, and northeastern China
• 26 species of Old World Elaphe and their relatives in the genera Zamenis, Orthriophis, Oreocryptophis, Euprepiophis, and Archelaphe.

as well as some more obscure groups:

Anilius scytale constricting an amphisbaenian
From Marques & Sazima 1998

• Tropidophiids or "dwarf boas", which are not closely related to boids and certainly evolved constriction independently (34 species)
• Their close relative Anilius scytale (sort of; this snake has been observed to constrict large prey such as amphisbaenians)
• Loxocemus bicolor, the Mexican burrowing snake, a close relative of pythons
• Two speceis of Asian sunbeam snakes (genus Xenopeltis), which are also closely related to pythons
• At least some (maybe all) Asian pipesnakes (family Cylindrophiidae)
• Filesnakes (genus Acrochordus), which don't necessarily kill fish by constricting them but use their coils to hold them while they swallow
• some lamprophiine colubrids (especially the well-known African house snakes Lamprophis and Boaedon)
• the colubrine colubrid tribe Lycodontini (mostly wolf snakes, genus Lycodon)
• some snail-eating snakes (Dipsas) coil around snails as they pry them out of their shells
• even Wandering Gartersnakes (Thamnophis elegans)—sometimes! (more below)

These groups of snakes vary considerably in how often they employ constriction to kill their prey. Some probably use it almost all the time (although even ratsnakes eat prey that they don't constrict, such as bird eggs), whereas others use constriction only rarely, when encountering an unusually large or dangerous prey item relative to their size and strength (for example, one study showed that species of Python, Boa, Pantherophis, and Lampropeltis always constricted mice if they were at least 90% the diameter of the snake's head). Some, such as Regina alleni and Acrochordus filesnakes, may use constriction more so to immobilize the prey than to kill it/it probably doesn’t work that well under water (although Wandering Gartersnakes usually killed mice before eating them).

It seems that mammal-eating is a driver of the evolution of constriction in many cases: species that eat mammals are the only members of their genera/families that use constriction (Thamnophis elegans, Boiga irregularis, Lamprophis/Boaedon, some members of the Oxyrhopus/Clelia/Pseudoboa clade) and both these and species that are nested within mammal-eating clades but have shifted to other prey (Lampropeltis extenuatum, Elaphe quadrivirgata, Cemophora coccinea¹) tend to have more variable, less efficient constricting behavior that is generally only used to immobilize rather than to kill prey, if it is used at all. As Alan de Queiroz and Rebecca Groen put it: “Thamnophis elegans are not finely tuned constricting machines” and “Numerous trials in which a garter snake, holding a mouse in its jaws, was chaotically thrown about by the prey's movements support our interpretation that long constriction latencies do not reflect adaptive plasticity in T. elegans.”. Constriction probably functions to reduce the cost of feeding in terms of time, energy, and/or the probability that the prey will harm the snake.

Conspicuously not in this category, we have the poorly-named and misleading North American Racer, Coluber constrictor, which is not a constrictor (thanks for nothing, Linnaeus).

Venom

Black Mamba (Dendroaspis polylepis) eating a bird

It's pretty clear which snakes use strong venom to subdue their prey; most of these are dangerously venomous to humans and so we're well aware of them. There are five major groups:

• Viperids (341 species), including well-known pit vipers such as rattlesnakes, copperheads, and cottonmouths
• Elapids (359 species), including coralsnakes, cobras, mambas, kraits, sea snakes, and diverse terrestrial Australian snakes ranging from death adders (genus Acanthophis) to bandy-bandys (genus Vermicella)
• Genus Atractaspis (21 species), the stiletto snakes now known to be lamprophiids, which stab backwards with their fangs, mouth closed, to envenomate prey in subterranean burrows
• Non-front-fanged colubrine colubrids, most notably boomslangs (Dispholidus typus), twigsnakes (genus Thelotornis), and probably their close relatives in the genus Thrasops, all of which have many functional characteristics of front-fanged snakes while their elongated teeth remain at the rear of the (albeit rather short) maxilla
• some Asian natricine colubrids in the genera Rhabdophis, Macropisthodon, and Balanophis, which in addition to being (in a few cases lethally) venomous, also have the distinction of being among the only known poisonous snakes

Also, many snakes use venom to subdue their prey but are not dangerous to humans, either because they have fangs in the back of their mouth, have venom that is not adapted for causing physiological damage to mammals, or both. These include:

• numerous dipsadine colubrids from the Caribbean and Central and South America, such as Xenodon, Thamnodynastes, Hydrodynastes, Coniophanes, Erythrolamprus, Rhadinaea, Leptoderia, and Apostolepis (and a few from North America, such as Heterodon and Hypsiglena)
• some colubrine colubrids (genera such as Boiga, Leptophis, Tantilla, Toxicodryas, Platyceps, Oxybelis, Hierophis, Crotaphopeltis, Drymobius, Chilomeniscus, Ficimia, and Gyalopion) as well as the Asian genera Ahaetulla and Chrysopelea, sometimes split into a different subfamily (Ahaetullinae)
• at least some natricine colubrids, such as Paratapinophis praemaxillaris and some North American gartersnakes (Thamnophis)
• many species in the family Homalopsidae, 53 species of southeast Asian semi-aquatic snakes, some of which are also well-known for pulling apart large crabs and eating pieces of them
• some (maybe most) lamprophiids, including aparallactines (Amblyodipsas, Aparallactus, Micrelaps, Polemon, Xenocalamus), lamprophiines (Gonionotophis), psamophiines (Mimophis, Psammophis), and the weird genus Psammodynastes ("mock viper")

and probably many more. It's actually possible that this is the largest group, because some of the "unknown" and "neither" species probably actually belong here. An interesting exception are Turtle-headed Seasnakes (Emydocephalus annulatus) and Beaded Seasnakes (Aipysurus eydouxii), which eat fish eggs and have mostly lost their venom, fangs, and venom glands. Another example of a reduction in fangs are some fossorial species of Tantilla, which have only slightly enlarged and faintly grooved rear maxillary teeth, in contrast to the more well-developed rear fangs of most other members of this large genus. These snakes appear to specialize on beetle larvae rather than on centipedes, although no one has looked to see if their venom is any different as a result.

Neither

Dipsas indica coiling around a snail, from Sazima 1989

Most snakes (38% of species) seize their prey and swallow them alive. Generally these snakes are eating prey that are much smaller than they are, which lack serious physical defenses (although many of them may have chemical defenses that the snakes circumvent in other ways, such as through toxin resistance). These include:

• Scolecophidians: Almost 450 species of blindsnakes that eat ant and termite larvae and pupae
• Uropeltids or Shield-tailed Snakes: 55 species that eat almost exclusively earthworms
• Snail-eating snakes in the family Pareidae: 20 southeast Asian species with asymmetrical jaws
• About 300 species of mostly South American dipsadine colubrids that eat soft, gooey things like slugs, snails, earthworms, or frog eggs, including:
• the most speciose genus of snakes, Atractus (currently with 140 species)
• the genus Geophis, currently in a four-way tie for the 5th-most speciose snake genus with 50 species
• some slender arboreal snakes in the genus Sibon, which crawl backward through crevices to wedge snails into them, providing an anchor against which they use their body muscles to pull out the soft parts
• Asian Thermophis
• North American Carphophis and Contia
• Most Old and New World natricine colubrids
• most gartersnakes (Thamnophis)
• watersnakes (Nerodia) and their relatives (Regina, Seminatrix, Clonophis, Tropidoclonion)
• slug-eating Storeria
• Asian ecological analogues (e.g., Amphiesma, Hebius, Opisthotropis, Xenochrophis)
• Numerous colubrine colubrids, such as:
• New World racers and coachwhips (Coluber)
• Indigo snakes (Drymarchon), which are well-known for crushing their prey in their strong jaws
• Indian ratsnakes (Ptyas)
• the Mole Snake (Pseudaspis cana)
• Egg-eating snakes (Dasypeltis), which have no need to kill the bird eggs that they eat or prevent them from escaping
• Calamariinae, an obscure subfamily of 89 species of colubrids from Asia that are thought to eat mostly earthworms

Some of the aforementioned goo-eaters do use their coils to support the shells of snails while they pry out the soft innards. Dipsas coils around the snail’s shell and Sibynomorphus use as s-shaped loop of their body to support the shell, whereas some Sibon crawl backward through crevices to wedge snails into them, providing an anchor against which they use their body muscles to pull out the soft parts.

Both

Finally, there are some really interesting examples of snakes that use both venom and constriction to subdue their prey, although not always at the same time. Perhaps most impressive but least well-documented in the scientific literature are two viper species that sometimes use constriction in conjunction with venom: Ovophis monticola and O. okinavensis².

Pseudonaja textilis constricting a mouse
From Mirtschin et al. 2006

A review by Rick Shine & Terry Schwaner brought together data on numerous Australian elapids that, although they clearly have and use venom, also use their coils to subdue and hold prey while envenoming it. In many of these species, including tiger snakes (Notechis), brown snakes (Pseudonaja), curl/myall snakes (Suta), whip snakes (Demansia), Australian coral snakes (Simoselaps), crowned snakes (Cacophis), and olive seasnakes (Aipysurus laevis), the coils are not used alone as the primary method of prey subjugation, and one recent paper suggested that we think of them as "part of a 'combined arsenal' of prey subjugation strategies".

To explain the "apparent paradox of why a species should use both venom and constriction to subdue its prey", Shine & Schwaner offered three possible non-mutually-exclusive explanations:

1. The venom may be of low toxicity and thus slow to act, so holding onto the prey with either jaws or coils might allow more venom to be injected
2. Species with short fangs, such as Pseudonaja, and/or that feed on on heavily armored prey , such as skinks, may use constriction to give themselves additional time to find a "chink in the armor" and envenomate their prey
3. Using constriction in addition to venom may prevent snakes from losing track of bitten and envenomated prey that escape, or from being harmed by retaliating prey that are held onto

The Australian elapids recorded to use constriction feed mainly on lizards and frogs, although mammals are common prey items of Pseudonaja and Notechis. Puff Adders (Bitis arietans) choose to release large rodents and rabbits, but hold onto smaller prey, although they have not been reported to use constriction (and given their specialized body shape, they probably do not, nor do they need to since they are equipped with long fangs, strong venom, and strike-induced chemosensory searching). However, immobilizing prey with coils probably plays a larger role in prey subjugation for many rear-fanged species with slower-acting venom, such as:

• colubrine colubrids Boiga irregularis, Macroprotodon, Platyceps gracilis, Stegonotus, Telescopus, Trimorphodon
• dipsadine colubrids from the Caribbean (Alsophis, Cubophis), Central & South America (Clelia, Helicops, Imantodes, Oxyrhopus, Philodryas, Tropidodryas, Siphlophis, Phimophis, and Pseudoboa), and North America (Diadophis, Farancia)
• the sibynophiine colubrid Sibynophis collaris
• some homalopsids, like Fordonia, Hypsiscopus, and Myron
• a few lamprophiine lamprophiids, such as Lycophidion
• pseudaspine lamprophiids Pseudaspis and Pythonodipsas
• some pseudoxyrhophiine lamprophiids Leioheterodon and Madagascarophis
• some psammophiine lamprophiids (e.g., the Montpellier Snake and its relatives in the genus Malpolon, Hemirhagerrhis, Psammophis, and Rhamphiophis)
• even Wandering Gartersnakes (Thamnophis elegans)—sometimes!

Elaphe quadrivirgata not constricting a frog (Rana ornativentris)
Mori (1991) showed that these snakes constrict large mice,
pin small mice with a single coil, and swallow frogs alive

In many cases, only large endothermic prey (usually mammals) are constricted, whereas snakes will swallow small, easily subdued prey alive. Even some specialized constrictors will consume small prey whole, suggesting that almost all snakes can change strategies depending on what type of prey they are subduing. The bottom line is that, if you're a snake that's eating mammals, you need to have either constriction or venom, and maybe both, because:

1. Mammals are big, or at least a lot of snakes like to eat mammals that are relatively large compared to their body size
2. They are endotherms with the metabolic capacity for sustained struggling
3. They can fight back with sharp teeth and strong jaws capable of seriously injuring or killing a snake, in a way that a frog or a lizard cannot

This generalization is supported by observations showing that mammals tend to be killed by constriction prior to being swallowed more often than prey such as frogs, and that larger prey tend to be killed by constriction first, then swallowed. Evidently the amount of struggling is one cue used by Thamnophis elegans to decide whether or not to constrict prey. Experiments carried out by Akira Mori and others have shown that "the degree of such behavioral flexibility is, to some extent, species-specific, and it has been suggested that dietary specialists change their behavior more efficiently than dietary generalists, especially when they are young".

Unknown

After my initial pass at collecting these data (during which I made several sweeping assumptions, some of which later turned out to be oversimplifications), I was left with 36% of species unknown. Following a more thorough literature search, I managed to get this down to 10%, which is still 363 species of snakes. In many cases I made assumptions based on generalizations about the biology of groups of snakes—for instance, I assumed that all scolecophidians use neither constriction nor venom, that all vipers use venom, and so forth. But many dipsadine and colubrine colubrids, and many lamprophiids have not been directly studied, and I could find no reports in the literature about their feeding habits. In some cases we don't even know what they eat, and ecological diversity in these groups is very high, such that there are few consistent patterns that I could use to infer prey subjugation mode for these 370 species. Teach yourself about obscure snakes and help fill in the blanks!

A few examples:

• anomochilids (dwarf pipesnakes)—we don't even know what they eat
• many Malagasy pseudoyrhophiine lamprophiids (e.g., Ithycyphus, Alluaudina)
• lamprophiids from mainland Africa, such as Bothrolycus, Chamaelycus, and Dendrolycus
• obscure dipsadines—e.g., Cryophis, Tantalophis
• obscure colubrines—e.g., Bamanophis, Hemerophis
• most of the xenodermids (Fimbrios, Parafimbrios, Stoliczkia, Xylophis)
• species known only from a few specimens, like Xenophidion

Evolution of prey subjugation strategies in snakes

Phylogenetic tree from Greene 1994
For an overview of some of the updates, click here

The most recent similar review was done by Harry Greene in 1994, in which he revised earlier hypotheses he put forth with Gordon Burghardt in the journal Science 16 years before. We now know a lot more about the snake family tree than we did in 1994, particularly the fine details of relationships within the Caenophidia. Overall, the basic pattern has held up rather well—constriction evolved first in basal alethinophidians during the late Cretaceous, accompanying or preceding most other evolutionary innovations that permit snakes to consume large prey, such as kinetic skulls. Greene pointed out that this was before the origin of rodents, often mentioned as potentially relevant to the evolution of snake prey-killing behaviors. Constriction was then lost at least twice—once in uropeltids (which feed underground on earthworms, although I'm not actually aware of any detailed observations of uropeltid feeding behavior) and at least once in basal colubroids, where it might have been  at first replaced by venom. Venom was then subsequently lost in numerous caenophidian lineages, replaced by re-evolution of constriction in some or by other specializations (tooth diastemata for holding skinks, egg-eating) in others, and in some caenophidian lineages snakes use both as appropriate, sometimes together (or they may elect to use neither even if both are available).

Both constriction and venom reduce the cost of feeding in terms of time, energy, and/or the probability of the prey harming the snake, but in constricting snakes, everyday locomotion and large prey neutralization are coupled, whereas in venomous snakes they are independent (snakes don't use their fangs to get around). This could be one reason why venom as an evolutionary innovation led to a more speciose radiation of snakes; it's also more susceptible to evolutionary arms races, because prey can evolve resistance to certain venom compounds, but not to constriction. Specialization for constriction is more than just behavior—constricting species also have more vertebrae per unit length than non-constricting species. And there are costs to both, which must be outweighed by the benefits of that defining snake trait: being able to consume prey almost as large, and sometimes much larger, than yourself!

---

1 An interesting exception are Scarletsnakes, Cemophora coccinea, the closest relatives of kingsnakes, which feed mostly on reptile eggs but also use their coils to hold lizard prey in the rare instances when they eat them. It is certain that Scarletsnakes evolved from constricting ancestors but because they almost never eat prey that need to be killed beforehand, evidently they rarely constrict.^↩

---

2 okinavensis has been shown not to be closely related to other Ovophis, but no new genus has yet been created for it because more data are needed.^↩

ACKNOWLEDGMENTS

Thanks to Karen Morris for asking me this question, and to Alpsdake and Danny Davies for the use of their photos.

SELECTED REFERENCES

For a full list of all the references I consulted in preparing this post, click here

Andrade, R. d. O. and R. A. M. Silvano. 1996. Comportamento alimentar e dieta da "Falsa-coral" Oxyrhopus guibei Hoge & Romano (Serpentes, Colubridae). Revista Brasileira de Zoologia 13:143-150 <full-text>

Auffenberg, W. 1961. Additional remarks on the evolution of trunk musculature in snakes. The American Midland Naturalist 65:1-16 <full-text>

Bealor, M. T. and A. J. Saviola. 2007. Behavioural complexity and prey-handling ability in snakes: gauging the benefits of constriction. Behaviour 144:907-929 <ResearchGate>

Bealor, M. T., J. L. Miller, A. de Queiroz, and David A. Chiszar. 2013. The evolution of the stimulus control of constricting behaviour: inferences from North American gartersnakes (Thamnophis). Behaviour 150:225-253 <full-text>

de Queiroz, A. and R. R. Groen. 2001. The inconsistent and inefficient constricting behavior of Colorado western terrestrial garter snakes, Thamnophis elegans. Journal of Herpetology 35:450-460 <full-text>

Franz, R. 1977. Observations on the food, feeding behavior, and parasites of the striped swamp snake, Regina alleni. Herpetologica 33:91-94 <full-text>

Gans, C. 1976. Aspects of the biology of uropeltid snakes. Pages 191-204 in A. d. A. Bellairs and C. B. Cox, editors. Morphology and Biology of Reptiles. Linnean Society Symposium Series No.3. Academic Press, London.

Götz, M. 2002. The feeding behavior of the snail-eating snake Pareas carinatus Wagler 1830 (Squamata: Colubridae). Amphibia-Reptilia 23:487-493 <ResearchGate>

Greene, H. W. 1994. Homology and behavioral repertoires. Pages 369-391 in B. Hall, editor. Homology: The Heirarchical Basis of Comparative Biology. Academic Press, San Diego <Google book>

Greene, H. W. and G. M. Burghardt. 1978. Behavior and phylogeny: constriction in ancient and modern snakes. Science 200:74-77 <abstract>

Hampton, P. M. 2011. Ventral and sub-caudal scale counts are associated with macrohabitat use and tail specialization in viperid snakes. Evolutionary Ecology 25:531-546 <link>

Holm, P. A. 2008. Phylogenetic biology of the burrowing snake tribe Sonorini (Colubridae). PhD dissertation. University of Arizona <full-text>

Jackson, K. and T. H. Fritts. 2004. Dentitional specialisations for durophagy in the Common Wolf snake, Lycodon aulicus capucinus. Amphibia-Reptilia 25:247-254 <full-text>

Loop, M. S. and L. G. Bailey. 1972. The effect of relative prey size on the ingestion behavior of rodent-eating snakes. Psychonomic Science 28:167-169 <full-text>

Marques, O. A. V. and I. Sazima. 2008. Winding to and fro: constriction in the snake Anilius scytale. Herpetological Bulletin 103:29-31 <link>

Martins Teixeria, D., M. Luci Lorini, V. G. Persson, and M. Porto. 1991. Clelia clelia (Mussurana). Feeding behavior. Herpetological Review 22:131-132 <link>

Mehta, R. S. and G. M. Burghardt. 2008. Contextual flexibility: reassessing the effects of prey size and status on prey restraint behaviour of macrostomate snakes. Ethology 114:133-145 <full-text>

Mirtschin, P. J., N. Dunstan, B. Hough, E. Hamilton, S. Klein, J. Lucas, D. Millar, F. Madaras, and T. Nias. 2006. Venom yields from Australian and some other species of snakes. Ecotoxicology 15:531-538 <full-text>

Mori, A. 1991. Effects of prey size and type on prey-handling behavior in Elaphe quadrivirgata. Journal of Herpetology 24:160-166 <link>

Mori, A. and K. Tanaka. 2001. Preliminary observations on chemical preference, antipredator responses, and prey-handling behavior of juvenile Leioheterodon madagascariensis (Colubridae). Current Herpetology 20:39-49 <full-text>

Mushinsky, H. R. 1984. Observations of the feeding habits of the short-tailed snake, Stilosoma extenuatum in captivity. Herpetological Review 15:67-68 <link>

Penning, D. A. and B. R. Moon. 2017. The king of snakes: performance and morphology of intraguild predators (Lampropeltis) and their prey (Pantherophis). The Journal of Experimental Biology 220:1154 <link>

Rossi, J. V. and R. Rossi. 1993. Notes on the captive maintenance and feeding behavior of a juvenile short-tailed snake (Stilosoma extenuatum). Herpetological Review 24:100-101 <link>

Savitzky, A. H. 1980. The role of venom delivery strategies in snake evolution. Evolution 34:1194-1204 <link>

Sazima, I. 1989. Feeding behavior of the snail-eating snake, Dipsas indica. Journal of Herpetology 23:464-468 <link>

Shine, R. 1977. Habitats, diets, and sympatry in snakes: a study from Australia. Canadian Journal of Zoology 55:1118-1128 <abstract>

Shine, R. and T. Schwaner. 1985. Prey constriction by venomous snakes: a review, and new data on Australian species. Copeia 1985:1067-1071 <link>

Stettler, P. H. 1959. Zur Lebensweise von Dipsas turgidus (Cope), einer schneckenfressenden Schlange. Aquarien und Terrarien 8:238-241.

Vidal, N. and S. B. Hedges. 2002. Higher-level relationships of snakes inferred from four nuclear and mitochondrial genes. Comptes Rendus-Biologies 325:977-985 <link>

Willard, D. E. 1977. Constricting methods of snakes. Copeia 1977:379-382 <link>

Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.

Snakes with feet, anti-goo saliva, and more recent updates

This post will soon be available in Spanish

More of the latest snake news and research (for other recent updates, see posts from March, June, and August)—and, perhaps the most exciting news of all is that I have defended my dissertation and will be returning to writing more in-depth content in the next few months!

Rattlesnake Roundups (I and II)

A Texas conservation licence plate ironically depicting
a Western Diamond-backed Rattlesnake (Crotalus atrox).
Funds from these plates support a variety of valuable
conservation projects in Texas under the Texas
Wildlife Action Plan, although none are specific to snakes.

Advocates for increasing state oversight of rattlesnake roundups in Texas received disappointing news this week when the Texas Parks and Wildlife Commission decided that they would not support a proposed ban on using gasoline fumes to collect rattlesnakes. Rather than reviewing and voting on the issue at their bi-annual meeting next month, the TPW Commission decided to remove it from their agenda entirely, citing "insufficient support from legislative oversight or the potentially regulated community". This decision marks the second time reviewing the ban has been put off, and unfortunately it is likely to be the last until the effort to reform roundups is re-initiated. The announcement included the statement that "TPWD [Texas Parts and Wildlife Department] staff still believe that there are better options for collecting snakes that do not adversely impact non-target species, and we will continue to work with the snake collecting community to develop and implement best practices that reduce potential impacts to these species", although in the absence of specific details it is hard to believe that this issue will remain at the fore of wildlife management in Texas without continued pressure from advocates of scientific rattlesnake management. However, Representative Susan King of Sweetwater's 2015 house bill 763 requires that petitions to state agencies (including TPWD) that are signed by <51% Texas residents are not valid, which means that the ability of non-Texans to influence policy on this issue is now greatly diminished.

If you're not familiar with the issues surrounding the gassing ban, I encourage you to read the 2016 Snake Harvest Working Group report, the same document that was available to the TPW Commission prior to their decision this week. Among other topics, it contains data on the adverse impacts of gassing on non-target endangered species, which is the primary impetus for the ban. It hints at human health impacts of consuming meat from gassed rattlesnakes. The SHWG report also summarizes previously unavailable data on roundup economics, showing that profits are not related to the number of rattlesnakes at an event and did not decline after gassing was banned in Alabama and Oklahoma. Stakeholder survey responses and the vast majority (>90%) of public comments from Texans were in favor of the gassing ban, as are many TWPD employees.

The TPW Commission is solely responsible for this decision. You can let the TPW Commission and Texas State Representative Susan King of Sweetwater (or your own state representative, if you live in Texas) know whether you think they are acting in the best interest of the majority of the public and in accordance with game management principles at the links provided (if you no longer have a fax machine, you can send a fax over the Internet here).

Goo-eating Snakes and the Eggs that Evade Them and Basics of Snake Fangs

Mandibular glands of Dipsas alternans
From Zaher et al. 2014

This discovery is from 2014, but it's newer than either of the past posts to which it's germane and I just found out about it. Perhaps you've seen the incredible rapid hatching behavior that treefrog eggs have evolved to escape from snake predators, including cat-eyed snakes (genus Leptodeira), blunt-headed tree snakes (genus Imantodes), and snail-sucking snakes (genera Sibon and Dipsas). These snakes also eat a variety of other gooey prey, such as earthworms, leeches, snails, slugs, adult frogs, caecilians, and, more rarely, non-gooey prey like lizards and reptile eggs. They have a number of adaptations that help them consume their sticky, viscous prey, including long, slender teeth, skull bones and muscles modified for extreme lower jaw extrusion, and a short-snouted, large-eyed look that resembles a snake embryo. Recently, a team of scientists from Brazil discovered a new one: a protein-secretion delivery system in the lower jaw.

Are the secretions venom? No. Dipsas and its relatives always extract snails using a sudden strike, followed by fast, alternating probing motions of the mandible inside the shell; this behavior could hardly depend on a chemical reaction of any kind. Instead, the gland secretions probably play a role in mucus control and prey transport rather than immobilization or killing of the prey. Although the glands in some species are associated with muscles, they are not connected to any teeth, but rather open onto the floor of the mouth, which in some species is covered with extensively loose, folded skin. Hypertrophied infralabial glands have been known from some dipsadine species since the 1960s, but the new paper describes the muscles and other soft tissues surrounding them and documents their variation among several dozen species of this very speciose group of snakes. On the other side of the world, pareatid snail-eating snakes have independently evolved a similar lifestyle, complete with upper jaw glands of perhaps similar function.

Why snakes are long and Why do snakes have two penises?

Pelvic girdles (dark blue) and hind limbs (red) of lizards,
living snakes, and extinct snakes with fully-developed limbs.
ZRS is the name of the SHH enhancer gene
that has been partially deleted in snakes.
From Leal & Cohn 2016

Many people are familiar with the tiny vestigial legs or "spurs" of boas, pythons, and other henophidian snakes. These structures are sexually dimorphic and are used by male boas and pythons in male-male combat and also to titillate females before and during mating. New data from the University of Florida describes how the spurs are formed: a weak flicker of activity by a gene called Sonic hedgehog (SHH) during the first few hours of embryonic development, in contrast to strong, sustained activity of this gene in lizard embryos throughout their development, forming legs. In snakes, unique genetic deletions from an enhancer of SHH explain its weak activity; transgenic mouse embryos with the same deletions showed similarly weak SHH activity, whereas mouse embryos grown with a lizard enhancer developed normally. Caenophidian snakes, such as vipers, gartersnakes, and cobras, had more extreme deletions and mutations, with the cobra barely retaining any of the SHH enhancer gene.

Amazingly, the researchers also found that HOXD13, the part of the limb-building gene that's responsible for building hands and feet, was unaltered in python embryos, and that python embryos develop not just a pelvic girdle and femur, which form the spur in adulthood, but cartilaginous templates of a tibia, fibula, and foot, which are reabsorbed prior to hatching. Although living snakes appear to follow a gradual pattern of limb shrinkage and loss, some extinct snakes that are thought to have been more similar to boas and pythons than they were to blindsnakes also had fully-developed, albeit small, limbs, complete with feet, as adults. This new discovery helps explain the apparent evolutionary "re-appearance" of these structures; they were never completely lost in the first place. As for the reason why not, snake HOXD genes and their regulators appear to be equally important to the development of their paired hemipenes, structures of obvious importance.

REFERENCES

Oliveira, L., A. L. Costa Prudente, and H. Zaher. 2014. Unusual labial glands in snakes of the genus Geophis Wagler, 1830 (Serpentes: Dipsadinae). Journal of Morphology 275:87-99 <link>

Leal, F. & Cohn, M.J. 2016. Loss and re-emergence of legs in snakes by modular evolution of Sonic hedgehog and HOXD enhancers. Current Biology DOI:10.1016/j.cub.2016.09.020 <link>

Leal, F. & Cohn, M.J. 2014. Development of hemipenes in the ball python snake Python regius. Sexual Development, 9, 6-20 <link>

Savitzky, A.H. 1983. Coadapted character complexes among snakes: fossoriality, piscivory, and durophagy. American Zoologist, 23, 397-409 <link>

Texas Parks and Wildlife Department. 2016. Snake Harvest Working Group Final Report <link> <references> <summary>

Zaher, H., de Oliveira, L., Grazziotin, F.G., Campagner, M., Jared, C., Antoniazzi, M.M. & Prudente, A.L. 2014. Consuming viscous prey: a novel protein-secreting delivery system in neotropical snail-eating snakes. BMC Evolutionary Biology, 14, 1-28 <link>

Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.

Asymmetrical snakes

Click here to view this post in Spanish!

Haga clic aquí para ver este blog en español!

Pareas margaritophorus

Animals have a long tradition of being bilaterally symmetrical - that is, of the left side and the right being nearly identical. Sure, there are a few exceptions - the human heart is nearly always farther to the left side, for instance. Snakes and other elongate, limbless animals sometimes stagger their paired organs (gonads, kidneys) so that one is in front of the other, to better fit in their cylindrical bodies. Most snakes have even done away with one of their two lungs. But the basic external body plan, the bones and muscles on the left and the right, are always mirror-images of one another, right?

Enter the pareatid snakes. This is a small group of colubroid snakes that relatively recently gained their family status - prior to 2005 they were, like many snakes, considered a subfamily of the Colubridae. Several phylogenetic analyses have found Pareatids to be only distantly related to other colubroids, having diverged from them at least 40 million years ago.

In any case they are incredibly unique. Distributed in tropical southeastern Asia, west of Wallace's line, they are relatively small terrestrial and arboreal snakes that feed mainly on slugs and snails (gastropods). In this respect, they are convergent with some Neotropical snakes, such as species of Dipsas, Sibon, Sibynomorphus, and Tomodon, as well as the African genus Duberria and the familiar North American snakes Storeria and probably Contia. However, pareatids possess a morphological adaptation to gastropodophagy (specifically, cochleophagy) unrivaled in the snake suborder. You see, most snails' shells coil in a clockwise direction from the center of their shell - that is, to the right. This is referred to as dextral, as opposed to sinistral (to the left or counterclockwise). If that seems weird, consider that about 90% of people also have an asymmetry: they are right-handed. This predominance is even reflected in our language: dextral comes from the Latin word dexterous, meaning manual skill, whereas the evil or unlucky connotation of sinistral is reflected in the word sinister. 

 

That's one sinister snail

So what does this mean for a snail specialist predator? It means that there is a selective force acting on one side of the snake's feeding apparatus, but not the other. Perhaps it goes without saying, but snakes have no hands, so they feed with their mouths only. Specifically, pareatids use their lower jaws to extract snails' soft bodies from their shells, because they lack the crushing bite force of mammals and other snail predators (but wait for my upcoming article on the snake Fordonia leucobalia).

A group of scientists from Kyoto and Shinshu Universities and the Japan Science and Technology Agency noticed this (one species of Pareas is endemic to the Ryukyu Islands of Japan) and decided to investigate museum specimens of pareatids for evidence of asymmetry in their jaws. So as not to damage the specimens (which are from an area of the world where specimens are hard to come by), they used X-ray photography to count the teeth in each mandible (lower jaw). Here's what they found:

Mandibles (lower jaws) of Pareas iwasakii 

Dorsal view of skull of Pareas iwasakii

These are two X-ray photographs of the skulls of Pareas iwasakii, from two papers published in Biology Letters and Nature Communications. The white bars are 10 mm long, for scale. If you didn't notice, count the teeth on the left and right jaws. That's right - way more on the right mandible. Which way did most of those snail shells coil again? Well, what if those two skulls were just weird?

Data from Pareas iwasakii

Data from 297 specimens

Ok, data from almost 300 snakes, including all 14 then-known species of pareatids (a 15th, Pareas nigriceps, was described in 2009). Now I'm convinced. The asymmetry index they calculated is based on the difference in the number of teeth between the left and right mandibles. If you did this in any other group of animals, you would have found that every individual had an asymmetry index between -1 and 1 - that is, an equal number of teeth in the left and right mandibles (imagine a deviation of ±1 if you had, say, a wisdom tooth erupt on one side but not the other). But pareatids had an average of 17.5 teeth in their left mandible and 25 teeth in their right mandible! The two species with asymmetry indices closer to 0 (Aplopeltura boa and Asthenodipsas malaccanus) are known to be slug or lizard-eating, rather than snail-eating, so you would expect different evolutionary pressures on their tooth number because slugs and lizards don't have to be scraped out of asymmetrical shells (which the snail-eaters can accomplish in as few as 24 seconds per snail!).

Aplopeltura boa

Asthenodipsas malaccanus

The authors weren't satisfied to stop there (scientists rarely are). They also did a manipulative experiment. They found a species of snail that had both dextral (clockwise) and sinistral (counterclockwise) morphs, and conducted feeding trials to see which were easier for the asymmetrical snakes for eat. Because these snakes feed nocturnally, they recorded the feeding trials with an infrared camera. This is also a good idea in behavioral experiments because it prevents the observer from unintentionally influencing the actions of the animals being studied merely by their presence.

Analysis of the tapes showed that dextral snails were easily eaten, whereas the snakes had considerable difficulty striking and holding onto sinistral snails. The snakes did not adjust their behavior when confronted with a sinistral snail, so as a result most of the sinistral snails escaped, whereas most of the dextral snails were successfully eaten. You can watch the video of a snake successfully attacking a dextral snail here, and the one of a snake struggling with and eventually dropping a sinistral snail here.

Stills from the video

Not only does this feeding adaptation benefit the snakes, but it has actually been shown to drive speciation in the snails. Because pareatids are so well-adapted for eating dextral snails, sinistral snails are at a significant survival advantage in regions where pareatids occur. Incompatibility between dextral and sinistral snails during mating has prevented both forms from occurring simultaneously, and the dextral form seems to be predominant. It isn't that there is an advantage to being dextral over sinistral - it's just that they all had to be either one or the other in order to be able to mate compatibly, and dextral is just what they all happened to be. But the same researchers who did the first study, plus some of their colleagues from Japan's Tohoku University in Japan and Taiwan's Taipei Municipal University of Education and National Taiwan University, discovered that right-left reversals in shell chirality were under the control of a single gene, so that changes in the allele of that gene could result in immediate speciation. The reason that speciation is immediate is the reproductive incompatibility, and therefore isolation, between dextral and sinistral snails. As long as there are a few other sinistral snails around to mate with (snails are hermaphrodites, so they aren't picky about things like sex), the new sinistral species can take off, free from predation by slug snakes, who cannot grip them with their dextral-snail-adapted jaws. Of course, it's probably only a matter of time before one or more of the slug snakes evolves a sinistral-adapted jaw, but it isn't as quick as it is for the snail because tooth and jaw development are controlled by more than just a single gene. However, the selection in favor of a sinistral-adapted snake jaw will continue to grow as the frequency of sinistral snail species increases. Already, southeast Asia harbors more sinistral snail biodiversity than any other region (12% as opposed to 5% worldwide), likely in part due to selection against dextral and for sinistral shells from snake predation.

Satsuma is one of the snail genera examined

The red lineages are the sinistral snails, many are sympatric with pareatids 

This hypothetical frequency-dependent reversal of snake jaw asymmetry is intriguingly similar to the situation with Lake Tanganyika cichlid fishes. One species of cichlid, Perissodus microlepis, eats the scales off other fishes. It sneaks up from behind and has an symmetrical mouth that allows it to grab scales from either the left or the right side of the prey fish - right-handed individuals snatched scales from the prey's left side and vice versa. Frequency-dependence of prey alertness causes the predominant form of P. microlepis to oscillate between dextral and sinistral. So when dextral P. microlepis predominate, the prey fishes are especially wary of attacks from the left side, and the few P. microlepis with sinistral mouths have an advantage. Eventually, more P. microlepis survive that are sinistral, prey wariness shifts sides accordingly, and the process reverses. You could imagine this happening with pareatids and snails, albeit much more slowly.

Dextral P. microlepis on top, sinistral P. microlepis on bottom

Interestingly, directional asymmetry of the snail-feeding apparatus has been found in other gastropodovores, such as crabs and other aquatic invertebrates. But, even among other snake species that specialize on snail prey in North America, South America, and Africa, pareatids are the only group of snakes to have evolved asymmetric jaws. Perhaps it has something to do with the ontogeny of their feeding - that is, how what they eat changes from when they're young to when they get old. The authors found no differences in the asymmetry index with body size, so small snakes were as asymmetrical as large ones. You might also have noticed that the X-ray of the skull on the right above was from an unhatched pareatid embryo, indicating that asymmetry is an innate, rather than an acquired, trait. This means that baby pareatids must also eat dextral snails - and in fact this was shown experimentally, by Masaki Hoso, who hatched some eggs of Pareas iwasakii in captivity and fed them baby snails. While he couldn't observe the babies feeding on snails directly (they feed at night, remember?), he found the empty shells they left behind.

Oh, the carnage

So although other snakes feed on snails as adults, they might not do so as juveniles, so selection might not be as strong on their jaw asymmetry. Of course, it could also be that pareatids have been feeding on snails for longer than these other lineages (they probably are the oldest lineage of snail-specialist snakes, although fossils are apparently unknown), or that they are more specialized on snails than the other groups, or that some kind of evolutionary constraint keeps the other snake groups from evolving asymmetry.

I'll leave you with a few photos of the other species of pareatids, which are as graceful and beautiful as they are evolutionarily intriguing.

Asthenodipsas laevis from Malaysia

Aplopeltura boa from Borneo

Pareas formosensis from Taiwan

Pareas carinatus from Laos

For more information about current research on pareatids and their prey, see Dr. Masaki Hoso's webpage.

ACKNOWLEDGMENTS

Thanks to photographers Martin Hauskrecht, Skink Chen, Thomas Calame, Paul Bertner, Björn Lardner, and Rob.

REFERENCES

Götz M, 2002. The feeding behavior of the snail-eating snake Pareas carinatus Wagler 1830 (Squamata: Colubridae). Amphibia-Reptilia 23:487-493.

Hirata T, Ota H, 1993. Predation on snails by the pareatine snake Pareas iwasakii. Japanese Journal of Herpetology 15:90-91.

Hori M, 1993. Frequency-dependent natural selection in the handedness of scale-eating cichlid fish. Science 260:216-219

Hoso M, 2007. Oviposition and hatchling diet of a snail-eating snake Pareas iwasakii (Colubridae: Pareatinae). Current Herpetology 26:41-43.

Hoso, M., T. Asami, and M. Hori. 2007. Right-handed snakes: convergent evolution of asymmetry for functional specialization. Biology Letters 3:169-172. <link>

Hoso M, Hori M, 2006. Identification of molluscan prey from feces of Iwasaki’s slug snake, Pareas iwasakii. Herpetological Review 37:174–176.

Hoso M, Kameda Y, Wu SP, Asami T, Kato M, Hori M, 2010. A speciation gene for left-right reversal in snails results in anti-predator adaptation. Nature Communications 1:133.

Ota H, Lin JT, Hirata T, Chen SL, 1997. Systematic review of colubrid snakes of the genus Pareas in the East Asian Islands. Journal of Herpetology 31:79-87.

Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.