If you need to identify a snake, try the Snake Identification Facebook group.
For professional, respectful, and non-lethal snake removal and consultation services in your town, try Wildlife Removal USA.

Monday, December 25, 2017

Life is Short but Snakes are Long 2017 Year in Review


Life is Short but Snakes are Long turned 5 years old in April, and reached 1 million views on June 26th, 2017. I celebrated with a month-long recapitulation of the "best-of" on Twitter in the spring, and by taking a much-needed break from writing new content during the second half of the year.  I didn't make a formal announcement of this break because I honestly wasn't sure how long it would last (although I knew it wasn't permanent). During the past six months I've focused on settling in to my new job in Germany, traveling around Europe, publishing a key article from my dissertation, and applying to postdocs and "real" jobs. I'm currently waiting to hear whether I'll be starting something new in 2018—if I am, I plan to continue to write Life is Short but Snakes are Long as I have been. If I'm not, I plan to begin revising certain past articles, and writing new ones, for a book. In either case, I'm looking forward to a lot of new content in 2018.

As always, thank you for reading.

Andrew Durso

Vipera berus from Germany

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Thursday, August 31, 2017

How many snakes are venomous and how many are constrictors?


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:
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:
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:
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>
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Location: Jena, Germany

Wednesday, May 31, 2017

Snakes of Morocco


Earlier this month I went to Morocco to attend the 5th Biology of the Vipers conference. The conference was organized by Fernando Martínez-Freiría and Soumia Fahd and featured a fantastic three-day scientific program in Chefchaouen followed by a six-day field excursion to southern Morocco to look for snakes. I learned a lot and got lots of great feedback on Life is Short but Snakes are Long, but unfortunately I didn't have time to finish writing May's article, which I aim to put up next week. On the way back, I also stopped by Jerez de la Frontera and finally met Alvaro Pemartin and Estefania Carrillo, whose dedicated translations have brought Life is Short but Snakes are Long to Spanish-speaking readers around the world!

Montpellier snake (Malpolon monspessulanus)

Saharan horned viper (Cerastes cerastes)

Puff Adder (Bitis arietans)

Egyptian Cobra (Naja haje)
Me on the streets of Chefchaouen

Me looking for vipers in  Toubkal National Park
Estefania and I in Jerez
We also met with an Aisaoua, a member of the traditional brotherhood of snake hunters in Morocco, who collect the snakes that are used by the snake charmers who put on shows. This tradition is at least 800 years old, and possibly as old as 2,000 years, and is an example of a human-reptile interaction with both positive and negative aspects. It was really interesting to see their method for finding snakes—they are very effective! More on this in a future article.

ACKNOWLEDGMENTS

Thanks to Konrad Mebert and Alvaro Pemartin III for allowing me to use their photographs, 

REFERENCES

Bons, J., P. Geniez, A. Montori, V. Roca, and E. Asociación Herpetológica. 1996. Amphibiens et reptiles du Maroc (Sahara Occidental compris) : atlas biogéographique = Anfibios y reptiles de Marruecos (incluido Sáhara Occidental) : atlas biogeográfico = Amphibians & reptiles of Morocco (including Western Sahara) : biogeographical atlas.

Pleguezuelos, J. M., M. Feriche, J. C. Brito, and S. Fahd. 2016. Snake charming and the exploitation of snakes in Morocco. Oryx :1-8 <link>

Tingle, J. L. and T. Slimani. 2017. Snake charming in Morocco. The Journal of North African Studies :1-18 <link>

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Life is Short, but Snakes are Long by Andrew M. Durso is licensed under a Creative Commons Attribution-NonCommercial-NoDerivs 3.0 Unported License.
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Sunday, April 30, 2017

The 21st century blindsnake revolution


Brongersma's Wormsnake (Amerotyphlops brongersmianus),
a widespread species from South America
Blindsnakes (Scolecophidia) don't get enough attention. They include the world's most widespread snake species, the world's smallest living snake species, and a diversity of jaw-raking feeding mechanisms unrivaled in bizarreness among land vertebrates. I recently noticed, much to my surprise, the the number of described species of blindsnakes has doubled in the last 13 years, from 305 in 2004 to 599 today; that's 16.5% of all snakes! June 2017 EDIT: This was a big mistake on my part. As of 2017 there are 442 species described instead of 599. I made this mistake because I was confused about the search terms being used on my go-to reference for reptile taxonomy, The Reptile Database. I was assuming that Leptotyphlopidae + Anomalepidae + Typhlopoidea = Scolecophidia, a search term that is no longer available in The Reptile Database, because of several phylogenies that show it to be paraphyletic. If you search for "Typhlopoidea" on The Reptile Database, you get a list of all 442 blindsnakes 442, including Leptotyphlopidae and Anomalepididae, and not only the three families of Typhlopoidea according to Vidal et al. 2010 (Typhlopidae, Xenotyphlopidae, Gerrhopilidae). I thought that Typhlopoidea only returned the latter three families and I added the 139 species of Leptotyphlopidae and 18 species of Anomalepididae to get an incorrect total of 599. Thanks to Claudia Koch of the Alexander Koenig Zoological Research Museum in Bonn for pointing this out to me. There are certainly many undiscovered species of blindsnakes, so it's likely that their numbers will continue to grow (as one recent study put it, "...even our most liberal estimates of species numbers will likely prove to be an underestimate of the true diversity...of secretive blind snakes").

Blindsnake evolutionary tree.
Extinction of the dinosaurs (K-T boundary) was
between the green and pink-shaded areas.
From Vidal et al. 2010
One of the biggest phylogenetic rearrangements within the Scolecophidia was the recognition of two new families in 2010. The new families Gerrhopilidae and Xenotyphlopidae were formerly part of Typhlopidae, but were discovered to be distantly related to other typhlopids and were separated, although these three families are grouped together in the superfamily Typhlopoidea to emphasize their closer relationship to one another than to the other two families of scolecophidians (Leptotyphlopidae and Anomalepididae). The original diversification of blindsnakes is thought to have been caused by the breakup of Gondwana, whereas the later diversification of Typhlopoidea is associated with the breakup of East Gondwana into Antarctica, Madagascar, India, and Australia (with subsequent colonization by typhlopids from West Gondwana [Africa/South America]). Subsequent diversification within the Typhlopidae coincides with the early Paleozoic Era, just after the extinction of the dinosaurs, and includes four major groups: a Eurasian-Australasian one, an African one, a Malagasy one, and a South American-West Indian one. Because sea levels were low at this time, dispersal among continents and islands was relatively easy, at least for a small vertebrate with low metabolism and most likely travelling along with their invertebrate prey. The relationships of blindsnakes track plate tectonics better than those of any other vertebrate group, perhaps because of their tendency to stay put.

Gerrhopilus mirus from Sri Lanka
The two "new" families probably originated on the ancient landmass "Indigascar" (modern India and Madagascar, which were physically connected long after their isolation from other continents and India's subsequent unification with Asia). One family, Gerrhopilidae ("Indo-Malayan blindsnakes"), were formerly known as the Typhlops ater species group. They differ from other blindsnakes in having gland-like structures ‘peppered’ over the head scales. Many species also have a divided preocular and/or ocular scale, and the second supralabialal scale overlaps the preocular in all species but one (G. tindalli). The family contains at least 16 species in the genus Gerrhopilus, and possibly others (the most-recently described species are from 1996 and 2005). This is where it starts to get really weird.

The 1811 Freycinet map of Australia, where
Cathetorhinus melanocephalus was not found
There is another candidate member of the family Gerrhopilidae. The genus Cathetorhinus contains a single species, known from only a single specimen (Natural History Museum, Paris RA-0.138, an adult male). It was collected by French zoologists François Péron and Charles-Alexandre Lesueur on a scientific expedition to Australia led by Nicolas Baudin between 1801 and 1803, and scientifically described (along with an unprecedented and unqeualed number of other new snake species) in the 1844 volume of Duméril & Bibron's opus Erpetologie Générale (the series is also the provenance of the mudsnake plate that I use as a logo for this blog). Cathetorhinus melanocephalus was the only blindsnake they collected, despite visiting the Canary Islands, Mauritius, Timor, and South Africa in addition to Australia (of which members of the expedition later produced the first complete map). Unfortunately, for reasons lost to history and despite their general habits as conscientious collectors1, the location where they found Cathetorhinus melanocephalus was not recorded (I'm speculating here, but it may have been because they were distracted by fearing for their lives—of a total of 24 scientists who went on the expedition, 5 died and 10 disembarked at Mauritius due to illness).

Cathetorhinus melanocephalus
From Wallach & Pauwels 2008
This wouldn't be such a problem (lots of type specimens have vague or missing type localities; Linnaeus correctly attributed fewer than half of his snakes to the right continent "Indiis") except that no other specimens have ever been found. It is taxonomically unique based on its morphology, descriptions of which have been rather inconsistent over the decades, partially because blindsnakes are really small and their scales are really hard to count, especially given the crummy optics of the 19th century. Except for the head glands, Cathetorhinus shares more anatomical characteristics with Gerrhopilus than with any other blindsnakes. A 2008 study reviewed the history of the Baudin expedition and concluded that “the provenance of this species remains unknown: it is certainly Old World, and may be from (in order of probability) Timor, Australia, Mauritius or Tenerife”. And so it would have remained, if not for some really excellent bibliographical sleuthing by biologist and scholar Anthony Cheke, an expert on Mascarene fauna. Cheke reviewed the unpublished original notes made by Lesueur on the voyage, and found a reference to "a very small [snake] species 4–5 inches maximum...the only one found during our stay [on Mauritius in 1803]...found amongst stones while clearing some land...about 8 inches be-low the soil surface". This tantalizing description suggests a blindsnake in size, habitat, and behavior, and although Cheke himself had assumed that it referred to the Brahminy Blindsnake (Indotyphlops braminus), he later realized that the first records of introduction of this widespread species were from 1869, 66 years later.2 Although this isn't concrete proof, it's highly suggestive that Lesueur's blindsnake was Cathetorhinus melanocephalus, since it was the only blindsnake collected on the entire journey.3 Fossils of an endemic Mauritian typhlopid were discovered around 1900 and described as Typhlops cariei, but direct comparison of the bones with those of Cathetorhinus has not been made. Could Cathetorhinus still survive in the wild? Many non-native blindsnake predators were already introduced to Mauritius when Lesueur and Péron visited, including rats, shrews, and tenrecs, and others have since become established, such as mongeese. Only time, and further field work on Mauritius, will tell.

Malayotyphlops luzonensis (L), M. denrorum (C), and M. andyi (R)
From Wynn et al. 2016
As if that wasn't strange enough, there is a third possible candidate member of Gerrhopilidae: the species known as either Typhlops manilae, Malayotyphlops manilae, or Gerrhopilus manilae. The taxonomic status of this species is currently unclear. It was described by American herpetologist and spy Edward H. Taylor in 1919, from a specimen that was "discovered in the Santo Tomas Museum" in Manila, although even then nobody knew when, where, or by whom it was collected. It appears to have been barely mentioned in the scientific literature until 2014, when its morphological distinctiveness from other members of the Typhlops ater species group/Gerrhopilidae was noted as part of a massive review of typhlopid snakes led by Pennsylvania State University blindsnake specialist and evolutionary biologist Blair Hedges. They suggested it belonged instead to another new genus, Malayotyphlops, also mostly from the Philippines, because it has 28 scale rows (vs. 18 in Gerrhopilus) and a short tail, and because a subocular scale is not unique to Gerrhopilus. Later the same year, a different study disagreed and moved the species back to Gerrhopilus based on the statement from the original description that it has a subocular. However, yet a third study took a close look at Taylor's original description, which contains no illustration, and noted several areas of potential confusion, concluding that without examination of the original specimen, which is still in Manila, "it is not possible to determine to which genus, or even family, T. manilae...belongs".

The three reptile species originally described by Mocquard
and re-discovered at Baie de Sakalava in northern Madagascar
after more than 100 years without records.
The blindsnake Xenotyphlops grandidieri (pink), and two
legless skink species: Paracontias minimus (brown with
longitudinal lines of dark spots) and P. rothschildi
(beige with black flanks). From Wegener et al. 2013
Before you get too discouraged, remember that snake biology is replete with tales of rediscovery. Case in point: the other "new" family, Xenotyphlopidae. This bizarre snake has completely lost any traces of visible eyes. It was known solely from the type specimens, described by French zoologist François Mocquard in 1905 and 1906, for more than 100 years. Their precise locality was unknown. However, Hanna Wegener and a term of German, Belgian, and American herpetologists rediscovered Xenotyphlops in 2013 on a coastal dune under a piece of wood in the sand in a littoral forest at Baie de Sakalava in northern Madagascar, along with two endemic legless skinks in the genus Paracontias also described by Mocquard. Because the new specimens of X. grandidieri overlapped the other species in this genus (X. mocquardi) in most morphological characteristics, the two have now been synonymized, making the family Xenotyphlopidae monotypic (for now). These blindsnakes are unique in having a greatly enlarged and nearly circular rostral scale and an enlarged anal shield, and in lacking a tracheal lung.

The number of less-phylogenetically-distinct but poorly-known blindsnakes is not small. These have received renewed attention due to their placement in new families, but the 21st century blindsnake revolution is just getting started.


1 Péron and Lesueur also collected the first and some of the only specimens of Bolyeria multicarinata from Mauritius, which is now thought to be extinct, although they mistakenly labeled it as being from Australia.↩

2 Today, only I. braminus and another introduced species, I. porrectus, are found on Mauritius; the latter may have also been introduced in the 1800s but was first conclusively documented only in 1993.↩

3 A few pieces of evidence against: a length of 4–5 French inches corresponds to 109–136 mm, which is just right for I. braminus but a tad small for the Cathetorhinus specimen, which measures 178 mm (6.6 French inches). Cheke thought that "Lesueur appeared to be writing from memory without the specimen actually before him, so, impressed by its small size, he may have exaggerated how tiny his snake actually was.", maybe the last time in history that somebody underestimated the size of a snake. The other point of confusion is over the exact locality: Lesueur and Péron were clearing land with an upland planter, Toussaint de Chazal, at whose estate in the area now known as Mondrain they were staying. Mondrain is on a plateau adjacent to the Tamarin Gorge, which is 9 km from Grand Bassin, where Lesueur stated that they found the snake.↩

ACKNOWLEDGMENTS

Thanks to Tim Colston, Ruchira Somaweera and Sumaithangi Ganesh for the use of their photos.

REFERENCES

Cheke, A. 2010. Is the enigmatic blind snake Cathetorhinus melanocephalus (Serpentes: Typhlopidae) an extinct endemic species from Mauritius? Hamadryad 35:101-104 <full-text>

 Duméril, C., G. Bibron, and A. Duméril. 1854. Erpetologie Générale on Histoire Naturelle Compléte des Reptiles. Librairie Encyclopédique de Roret, Paris <link to Cathetorhinus description>

Hedges, S., A. Marion, K. Lipp, J. Marin, and N. Vidal. 2014. A taxonomic framework for typhlopid snakes from the Caribbean and other regions (Reptilia, Squamata). Caribbean Herpetology 49:1-61 <full-text>

 Kraus, F. 2005. New species of blindsnake from Rossel Island, Papua New Guinea. Journal of Herpetology 39:591-595 <abstract>

Pyron, R. and V. Wallach. 2014. Systematics of the blindsnakes (Serpentes: Scolecophidia: Typhlopoidea) based on molecular and morphological evidence. Zootaxa 3829:1-81 <full-text>

Taylor, E. H. 1919. New or rare Philippine reptiles. Philippine Journal of Science 14:105-125 <full-text>

Vidal, N., J. Marin, M. Morini, S. Donnellan, W. R. Branch, R. Thomas, M. Vences, A. Wynn, C. Cruaud, and S. B. Hedges. 2010. Blindsnake evolutionary tree reveals long history on Gondwana. Biology Letters 6:558-561 <full-text>

 Wallach, V. 1996. Two new Blind snakes of the Typhlops ater species group from Papua new Guinea (Serpentes: Typhlopidae). Russian Journal of Herpetology 3:107-118 <full-text>

 Wallach, V. and O. Pauwels. 2008. The systematic status of Cathetorhinus melanocephalus Duméril & Bibron, 1844 (Serpentes: Typhlopidae). Hamadryad 33:39-47 <full-text>

Wegener, J. E., S. Swoboda, O. Hawlitschek, M. Franzen, V. Wallach, M. Vences, Z. T. Nagy, S. B. Hedges, J. Köhler, and F. Glaw. 2013. Morphological variation and taxonomic reassessment of the endemic Malagasy blind snake family Xenotyphlopidae. Spixiana 36:269-282 <full-text>

Wynn, A. H., R. P. Reynolds, D. W. Buden, M. Falanruw, and B. Lynch. 2012. The unexpected discovery of blind snakes (Serpentes: Typhlopidae) in Micronesia: two new species of Ramphotyphlops from the Caroline Islands. Zootaxa 3172:39–54 <full-text>

Wynn, A. H., A. C. Diesmos, and R. M. Brown. 2016. Two new species of Malayotyphlops from the northern Philippines, with redescriptions of Malayotyphlops luzonensis (Taylor) and Malayotyphlops ruber (Boettger). Journal of Herpetology 50:157-168 <full-text>

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


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