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Sunday, April 30, 2017

The 21st century blindsnake revolution

This post will soon become available in Spanish

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! 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.3nbsp;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.


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


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>

Creative Commons License

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

Friday, March 31, 2017

Snakebite, antivenom research, and basic science

Soon available in Spanish
Pronto disponibile en Español

In the past few weeks, a peculiar congruence of several seemingly-unrelated events took place. (At least) two new scientific papers about snake biology were published, a new video series was announced, some scientists entered contests, and the U.S. executive branch announced a budget proposal with deep cuts to science funding. However, these events aren't as unrelated at they might seem at first glance, and they have something to tell us about where snake biology, and science in general, are going in the future.

The science: part I (puff adders)

A puff adder (Bitis arietans)
Puff Adders (Bitis arietans) are among Africa's most widespread vipers. They are heavy-bodied snakes that are found in savannas and open woodlands. Like most vipers, they eat mostly rodents as adults, which they ambush from carefully-selected sites, which they sometimes occupy for weeks at a time. Recently, Xavier Glaudas and Graham Alexander published a new study showing that, even though Puff Adder strikes last less than two seconds, they can choose to either hold onto or let go of the prey depending on its size. Specifically, they hold onto small mice, shrews, birdstoads, and lizards, but strike & release larger rodents and rabbits, because retaliatory rat bites are dangerous to them. After they let go of these larger prey, which usually run off a short distance before the venom kills them, they track them down again using stereotypic strike-induced chemosensory searching behavior to locate the scent of non-toxic components of their own venom. This is really similar to findings by Bree Putman and Rulon Clark that Southern Pacific Rattlesnakes (Crotalus oreganus) were more likely to hold onto smaller rodents than to larger ground squirrels. You can watch 26 awesome videos selected from an archive of thousands of hours of video taken in the wild over more than two years.1

This research matters because venomous snakes and their prey are in constant evolutionary arms races, leading to:
  1. a mosaic of new biochemical compounds that are often useful in treating disease
  2. a mosaic of new biochemical compounds that can make venomous snakebite really hard to treat
We'll come back to the second one in a minute. The obvious importance of human medicine and venomous snakebite treatment overshadow a third important reason to study snakes and what they eat. Although the beneficial role of snakes in rodent control is taken as gospel by many advocates of snake conservation, the amount of data that we actually have on what snakes eat in the wild is surprisingly small. For many species, we don't even have a general idea of what kinds of prey they like to eat. Given recent estimates that spiders eat about as much meat as people do worldwide, and the potential for snakes to reach very high population densities in certain habitats, it's likely that the top-down effects of snakes as predators are significant ecosystem services that most humans aren't aware of and thus undervalue. Indirect effects on other aspects of the ecology of snake prey species, such as predation release and disease transmission, link snake predation even more strongly to human health. This is particularly timely in light of recent predictions that 2017 will be a big year for white-footed mice and thus for Lyme disease in the northeastern USA, controversy over the reintroduction of Timber Rattlesnakes, one of the white-footed mouse's top predators, to Quabbin Island in Massachusetts2, and the continuation of both the infamous Sweetwater Rattlesnake Roundup3 and the reformed Claxton Wildlife Festival and Lone Star Rattlesnake Days earlier this month.

The science: part II (how cobras got their flesh-eating venoms)

A Mozambique spitting cobra (Naja mossambica) spitting its venom
Spitting cobras are even more well-known than puff adders because of their defensive venom spitting abilities, showcased on the BBC's Life in Cold Blood. They are found in Africa and Asia and are thought to have evolved two or three times from non-spitting cobras. A new paper from the lab of Bryan Fry at the University of Queensland sheds some light on when and why venom spitting evolved. Elapid snakes, including cobras, have venoms rich in neurotoxins, which are highly potent toxins that are very effective at paralyzing their prey. Cobras also have less potent cytotoxins that kill cells directly, which is a bit weird. What is the function of these toxins?

Toxicity of snake venom to human cells grown in culture.
Warm colors indicate higher toxicity.
From Panagides et al. 2017
The hypothesis put forth here is that the first step towards venom spitting was the evolution of hooding behavior and morphology, which happened twice in elapids: once in "regular" cobras and once in King Cobras, which are more closely related to mambas. Only once a conspicuous visual display was present was there selective pressure for cytotoxic venom components delivered to the eyes of potential predators via spitting. Although the venom of both groups is cytotoxic, Hemachatus (rinkhals) and Naja cobras use three-finger toxins, whereas King Cobras use L-amino acid oxidase enzymes, consistent with the undirected, opportunistic nature of our current model of venom evolution by gene duplication and mutation. The authors suggest that further elevations in cytotoxicity are linked to bright bands and other aposematic colors or hood markings, although their paper did not attempt to quantify these attributes of cobra displays, which can be quite diverse even within species. Further evidence in support of the hypothesis is that Naja naja and Naja oxiana seem, based on their nested position, to have lost spitting but to have retained cytotoxicity, and their close relatives Naja atra and Naja kaouthia might represent steps down this evolutionary path, being capable of spitting only in some populations and with less accuracy than the African and southeast Asian clades of true spitting cobras.

This is an extremely cool and popular topic. It was covered by IFLS, The Wire, Gizmodo, and the Washington Post. It goes to show that people worldwide are fascinated by venomous snakes, and the Fry lab has done a great job capitalizing on that interest (among other accolades, Fry's graduate student Jordan Debono recently won the Queensland Women in Science Peoples' Choice Award [a contest that was decided by an online popular vote; more on this later] for her research on global snakebite treatments). One reason for this fascination has to do with the question of who, exactly, these cobras are defending themselves from? The most reasonable hypothesis, given the timing and geography of the diversification of spitting cobras and the precision with which they can target forward-facing eyes and hominoid faces, is primates. Us, and our ancestors, who have eaten and been eaten by snakes for millions of years. Studying spitting cobras is a window into our own evolutionary past, a way for us to learn about ourselves. But, let us not be misled into thinking that interactions between humans and cobras are a thing of the past.

The upshot: the truth about snakebite

You can follow the ASV @Venimologie
If you haven't read the blog by medical toxinologist Leslie Boyer, you really should. Earlier this month she wrote about the vicious circle of antivenom shortage in sub-Saharan Africa, where millions of people are bitten by venomous snakes every year, many of which die or suffer awful injuries because they lack access to good antivenom. This crisis has prompted the creation of the African Society of Venimology and a new series of snakebite training videos in English, French, and Spanish. The politics and economics of antivenom are complicated and reflect larger issues in medicine, education, quality control, supply and demand, and how global economics and corporations have failed to respond to the needs of local communities and consumers. In a nutshell, the issue is that antivenom manufacturers don't make enough good antivenom, because not enough people buy it. People don't buy it because it's expensive, and it's expensive because not that much is made. This is despite a huge need for it—but not everybody with a snakebite goes to a hospital and gets antivenom in Africa, partially because it's not certain there will be any and partially because a lot of patients and doctors don't know about antivenom, because it's not in widespread use (which is mostly because of the reasons above). Other exacerbating problems include that it's often not certified, fake products can price the real antivenom out of the market, and the infrastructure for distributing antivenom and information in Africa is sub-optimal (but improving). Fixing any one or even most of these problems won't fix the whole system—if any one of them break down, supply and demand will be out of balance and people won't get the care they need.

A lot of the same issues used to be present in Mexico, but product improvements, government outreach, and massive education efforts in the 1980s and 1990s dramatically reduced mortality from venomous snakebite and led Mexico to become a major producer and consumer of high-quality, affordable antivenom, so much so that the USA now imports some of these drugs from Mexico. The Mexican government enabled the Mexican antivenom industry to be competitive and reach its market, which is much larger than the domestic market for American antivenom manufacturers—medically-serious venomous snakebites (and scorpion stings) in the USA are mostly confined to the southwest, and the per-capita risk of snakebite is the lowest in the world. This creates its own unique problems. You may have heard about the controversy surrounding the discontinued coralsnake antivenom made by Wyeth, and there are compelling arguments that the Mexican polyvalent antivenoms Anavip (made by Bioclon for humans) and ViperSTAT (made by Veteria Labs for cats and dogs) are more effective and much less expensive (although this is due almost exclusively to the idiosyncrasies of the US healthcare finance system) than the only FDA-approved viper antivenom, CroFab (although BTG, the maker of CroFab, filed a complaint asserting that these Mexican products infringe on its patent).

Finally, the global importance of the availability of high-quality, affordable antivenom for Latin American, African, and other exotic snakes is only going to increase as venomous snakes become more popular as pets and in zoos. This is particularly true in parts of the world completely lacking venomous snakes or with only very benign, non-life-threatening species, such as northern EuropeScandinavia and northern North America, where doctors may be totally unprepared for a snakebite emergency and may not have appropriate antivenom on hand. This is exactly the kind of situation where government funding, in the form of orphan disease R&D grants, could play a role in making it affordable for researchers and doctors to save lives.

For a great introduction to and more in-depth coverage of these issues, you should watch The Venom Interviews or read their coverage of the recent video series.

The future: sequence the Temple Pitviper genome

Temple or Wagler's Pitvipers (Tropidolaemus wagleri)
at the famous Temple of the Azure Cloud in Penang, Malaysia
You can vote to sequence their genome here!
Genomics of snakes is taking off in a big way, and we stand to learn a lot more about the evolution and function of snake venoms and the treatment of their effects. But, funding for basic science isn't a priority for many people, and more and more scientists are turning to crowd-funding their research or relying on limited funding from private foundations, which often decide which projects to fund through a crowd-sourced voting process. This isn't necessarily a bad thing; in fact, I think it's a great thing in many cases. But, it's important to realize that government funding for science is different from private funding in two crucial ways: 1) there is a lot more of it (at least for now), and 2) it's not driven by specific, private interests. A great example is the Orianne Society, a non-profit reptile conservation organization whose founding purpose was preventing the extinction of Eastern Indigo Snakes (Drymarchon couperi). Thanks to generous donations from private funding sources, the Society succeeded in purchasing large areas of critical habitat for this endangered snake and protecting them in perpetuity, probably the most effective and laudable conservation goal in existence. Another good example is the work of the Durrell Wildlife Conservation Trust, who have essentially saved a globally-rare snake, Casarea dussumieri, from extinction in the wild. I wish the quality conservation work that these organizations have become well-known for were more common, but to date their donors are some of the only large private backers of reptile research and conservation in the world.

Snakes are part of human economics, albeit to a lesser extent than many insects, fishes, birds, and mammals—they are hunted for food (although there are many issues surrounding better management of unsustainable harvests), kept as pets, their skins made into leather, and their venom harvested to make antivenom and other drugs. But, in their current form, these industries place very little emphasis on finding out more about snake biology in the wild; it just isn't necessary for them to make a profit, even though the information is important for what they do. Antivenom manufacturers are accountable to their shareholders, but trying to block FDA approval of Mexican antivenom is certainly not going to result in better treatment for snakebite victims in the USA, and American companies aren't investing in any research to create new, better products themselves, since drug development is expensive and risky, and they already have a monopoly on antivenom in the USA.

It's no secret that snakes and snake research have a PR problem: even scientific journals are less likely to publish research articles about snakes than about mammals and birds (although the bias is likely subliminal). Many people prefer cute fuzzy animals that are similar to humans, but research into the biology of un-fuzzy animals is equally important. There's a parallel to the divide between funding for basic and applied science. Basic science isn't usually as sexy as the exciting, fun applications that come later, like saving lives, curing diseases, or discovering new complex biological phenomena. However, important applied science like antivenom creation cannot happen without basic science, in particular basic science on snakes. Private companies can't afford to invest in basic science the way they once did. Which leaves government funding and that from a limited number of interested, private backers.

We should support public funding for science and elect politicians who will do the same; better treatment for snakebite should be the least partisan and most universally-agreed-upon goal in the world. I think the path between basic (snake ecology, venomics, and genomics) and applied (antivenom manufacturing and public health) science is shorter and clearer in this context than in many, but the same principles apply—you cannot have medicine, conservation, and the other good parts of civilization without science.

You can vote now through April 5th 2017 for a project sequencing the entire genome of the Temple Pitviper (Tropidolaemus wagleri) co-led by Ryan McCleary.

Stay tuned for more about the role of snake venom proteins in treating human diseases, and the role of snakes as predators in ecosystems.

1 Naturally, I wanted to link to the full-text of the paper so that anyone interested in learning more could read it, but the publisher (Wiley) has a 12-month embargo on posting the PDF anywhere online. They actually expect you to pay between $6 and $38 to read the article. Now, I think it's great research, and it probably cost Glaudas, Alexander, and their university thousands of dollars and thousands of hours to do it. But, if you pay Wiley to read their paper, none of that money will go to them, nor to the scientists who peer-reviewed their work for free. It will go to Wiley, who Xav paid (maybe) to publish. They could have paid $3,000 to make it open access, but you can understand why they didn't. No wonder most most science is read by fewer than 10 people. It's an outdated model that can't go away fast enough. In contrast, the spitting cobra paper is open access, which cost its authors over $1,500. This is typical; academic authors almost always lose money on a publication.

2 Recent update here; you can write the governor of Massachusetts here.

3 Reports suggest that this year, like last year, a much larger number of live rattlesnakes were collected than markets could support, and at least one person died from a snakebite sustained while trying to capture a rattlesnake for a roundup.


Thanks to Bryan Fry for alerting me in advance of his publication, and to Colin Donahue, Markus Oulehla, and Ian Glover for the use of their photos.


Bonnet, X., R. Shine, and O. Lourdais. 2002. Taxonomic chauvinism. Trends in Ecology & Evolution 17:1-3 <link>

Boyer, L. V. 2016. On 1000-Fold Pharmaceutical Price Markups and Why Drugs Cost More in the United States than in Mexico. The American Journal of Medicine 128:1265-1267 <full-text>

Boyer, L. V. and A.-M. Ruha. 2016. Pitviper Envenomation Guidelines Should Address Choice Between FDA-approved Treatments for Cases at Risk of Late Coagulopathy. Wilderness and Environmental Medicine. 27:341–342 <full-text>

Boyer, L. V., P. B. Chase, J. A. Degan, G. Figge, A. Buelna-Romero, C. Luchetti, and A. Alagón. 2013. Subacute coagulopathy in a randomized, comparative trial of Fab and F (ab′) 2 antivenoms. Toxicon 74:101-108 <full-text>

Cao, N. V., N. T. Tao, A. Moore, A. Montoya, A. Rasmussen, K. Broad, H. Voris, and Z. Takacs. 2014. Sea snake harvest in the Gulf of Thailand. Conservation Biology 28:1677-1687 <full-text>

Chew, M., A. Guttormsen, C. Metzsch, and J. Jahr. 2003. Exotic snake bite: a challenge for the Scandinavian anesthesiologist? Acta Anaesthesiologica Scandinavica 47:226-229 <full-text>

Chippaux, J.-P. 2012. Epidemiology of snakebites in Europe: a systematic review of the literature. Toxicon 59:86-99 <full-text>

Glaudas, X., T. C. Kearney, and G. J. Alexander. 2017. To hold or not to hold? The effects of prey type and size on the predatory strategy of a venomous snake. Journal of Zoology 10.1111/jzo.12450 <abstract>

Glaudas, X. and G. Alexander. 2017. Food supplementation affects the foraging ecology of a low-energy, ambush-foraging snake. Behavioral Ecology and Sociobiology 71:5 <link>

Margres, M. J., J. J. McGivern, M. Seavy, K. P. Wray, J. Facente, and D. R. Rokyta. 2015. Contrasting modes and tempos of venom expression evolution in two snake species. Genetics 199:165-176 <full-text>

McCleary, R. J. and R. M. Kini. 2013. Non-enzymatic proteins from snake venoms: a gold mine of pharmacological tools and drug leads. Toxicon 62:56-74 <full-text>

Natusch, D. J. D., J. A. Lyons, Mumpuni, A. Riyanto, S. Khadiejah, N. Mustapha, Badiah, and S. Ratnaningsih. 2016. Sustainable Management of the Trade in Reticulated Python Skins in Indonesia and Malaysia. IUCN, Gland, Switzerland <full-text>

Nyffeler, M. and K. Birkhofer. 2017. An estimated 400–800 million tons of prey are annually killed by the global spider community. The Science of Nature 104:30 <full-text>

Panagides, N., Timothy N. Jackson, R. Pretzler, M. P. Ikonomopoulou, Kevin Arbuckle, D. C. Yang, S. A. Ali, I. Koludarov, J. Dobson, B. Sanker, A. Asselin, R. C. Santana, I. Hendrikx, Harold van der Ploeg, J. Tai-A-Pin, R. v. d. Bergh, H. M. I. Kerkkamp, F. J. Vonk, A. Naude, M. Strydom, L. Jacobsz, N. Dunstan, M. Jaeger, W. C. Hodgson, J. Miles, and Bryan G. Fry. 2017. How the cobra got its flesh-eating venom: cytotoxicity as a defensive innovation and its co-evolution with hooding and spitting. Toxins 9 <full-text>

Putman, B. J., M. A. Barbour, and R. W. Clark. 2016. The foraging behavior of free-ranging Rattlesnakes (Crotalus oreganus) in California Ground Squirrel (Otospermophilus beecheyi) colonies. Herpetologica 72:55-63 <full-text>

Stock, R. P., A. Massougbodji, A. Alagon, and J.-P. Chippaux. 2007. Bringing antivenoms to Sub-Saharan Africa. Nature Biotechnology 25:173-177 <full-text>

Wade, L. 2014. For Mexican antivenom maker, US market is a snake pit. Science 343:16-17 <full-text>

Willson, J. D. 2016. Indirect effects of invasive Burmese pythons on ecosystems in southern Florida. Journal of Applied Ecology 10.1111/1365-2664.12844 <full-text>

Willson, J. D. and C. T. Winne. 2016. Evaluating the functional importance of secretive species: A case study of aquatic snake predators in isolated wetlands. Journal of Zoology 298:266-273 <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.

Tuesday, February 28, 2017

Shield-tailed snakes (Uropeltidae)

Large-scaled Earth Snake (Uropeltis macrolepis)
Shield-tailed snakes (family Uropeltidae) are poorly studied, fossorial snakes endemic to montane regions of peninsular India & Sri Lanka. Together with the families Cylindrophiidae (14 species) and Anomochilidae (3 species) they make up the superfamily Uropeltoidea, which is named for them because they are the most diverse subgroup, with 55 species in 8 genera (9 until recently, more below). Most phylogenetic studies suggest that Uropeltoidea is the sister group to Pythonoidea, although these two lineages share only a few obvious features and likely diverged at least 60 and possibly up to 85 million years ago. If it's true, this relationship is pretty interesting because it means that the familiar giant pythons are more closely related to the ~18" long burrowing uropeltoids than they are to their most obvious ecological analogues, the giant Neotropical boas. However, this kind of relationship is not unprecedented: the emerging picture of henophidian taxonomy is that constriction and large gape size have evolved at least three or four times within snakes, a good example being the sister relationship now widely accepted between the "pipesnake" family Aniliidae and the "dwarf boa" family Tropidophiidae (the "Amerophidia"), both of which were formerly considered members of the Uropeltoidea. Even some species of Cylindrophis (and, possibly, Anilius) immobilize their prey with their coils, although they have small gapes.

The southern Western Ghats
Uropeltids are the Darwin's Finches of snakes. They have radiated spectacularly across an archipelago of "sky islands", reaching their highest diversity and endemism in the mountain ranges of India's southern tip. These volcanic mountains run parallel to the coast, creating a rain shadow of dry plains to the east and generating torrential rainfall within their hills as trade winds blow monsoonally wet air northeast from the Arabian Sea. Known as the Great Escarpment of India, these mountains are an ancient coastline, formed during the break-up of the supercontinent Gondwana some 150 million years ago. Uropeltids are especially diverse in the high, wet 'shola' forests of the Anai Malai Hills (also known as the Elephant Hills), but are also highly diverse in the the Pothigai (Agasthyar Malai), Nilgiri, and Cardamom Hills, as well as the northern and central Western Ghats, the Eastern Ghats, and on Sri Lanka. Many of these mountain ranges are part of the UNESCO World Network of Heritage Sites and are among the "hottest hot-spots" of biological diversity in the world. They're home to the world's largest wild population of Indian Elephants, the second largest wild tiger population, and even more critically-endangered, endemic mammals such as Nilgiri tahr and Malabar large-spotted civets. Sixty-five percent of reptile species in this area are found nowhere else. In addition to uropeltids, the Ghats are home to diverse radiations of endemic freshwater crabs and shrimps, minnows and carps, tree frogs, and caecilians. Other endemic reptiles include the cane turtle (Vijayachelys silvatica) and travancore tortoise (Indotestudo travancorica), two genera of skinks (Ristella and Kaestlea), spiny tree lizards (genus Salea), and wood snakes (genus Xylophis, also named by Beddome, which were thought to be xenodermids but from which we have just recently obtained the first DNA sequences, placing at least one species with pareids and another with natricines). Besides Xylophis and uropeltids, there are at least 29 other species of endemic snakes, ranging from blindsnakes to sand boas, vine snakes, coral snakes, and vipers.

Col. Richard H. Beddome
Perhaps it isn't surprising that most species of uropeltids "were described in a burst of activity in the 19th century", because British colonials cleared large swaths of mountain forest for timber and tea, coffee, and teak plantations between 1860 and 1950. Forty percent (22) of the known species were discovered and described by Colonel Richard Henry Beddome, a naturalist who "…exploited the South Indian Hills, including the Palni Hills, to such purpose in the seventies and eighties of the last century, that he has hardly left a snake for any later enthusiast to discover" wrote distinguished herpetologist Frank Wall in 1922.1 Perhaps somewhat ironically, Beddome's 1911 obituary states that his career as a naturalist and forester coincided with "the first systematic steps to save the forests of Southern India from the denudation at the hands of the rural population to which they had long been exposed". However, Beddome used his tours in the montane forests to carefully document, describe, and make exhaustive and useful collections of plants, land snails, amphibians, and reptiles. In his lifetime Beddome described over a thousand species of animals and plants, and many others have been named for him.2

Heads and tails of uropeltids. 
The blade-like, "boomerang rostral" and polygonal eye shield
of Rhinophis punctatus (top left [top] and top right [side]).
Shield-like tail of Uropeltis rubromaculata (bottom left)
 Rhinophis philippinus (bottom right). From Pyron et al. 2016
Uropeltids are supremely adapted for burrowing, perhaps more so than any other snake. They construct a network of burrows during the rainy season, when the soil is soft, and wander through them after they harden. They can dig as deep as two meters and for extended periods of time. They have stout, relatively lizard-like skulls with few teeth, and conical, slender heads that are much narrower than their thick bodies. The eyes of some species are protected by polygonal scalesRhinophis and some Uropeltis have keeled, blade-like rostral scales that give the head a distinct pointed appearance. Uropeltids have narrow ventral scales similar to their dorsal scales, and short, blunt, often shield-like tails, from which they get their common name. Uropeltid tail morphology ranges from relatively normal (in Brachyophidium, Platyplectrurus, and Teretrurus) or somewhat compressed with a multi-pointed scute on the end (in Melanophidium, Plectrurus, and Pseudoplectrurus), through decidedly unusual, including tails terminating in a projecting, rugose, keratinous disc (in Rhinophis and Pseudotyphlops), to the classic, highly modified “shield” tail of some Uropeltis, in which the body appears to have been sliced off at a ~45° angle, leaving a flattened disc covered with rugose scales. However, the real specializations for burrowing are hidden within.

Diagram of  a dissected Rhinophis drummondhayi
showing the extent of red and white muscle along the body
and in 
two cross-sections. From Gans et al. 1978
Firstly, the heads of uropeltids are battering rams that are used against the soil. They are the only amniotes whose skulls are supported at the base by two vertebrae: that is, both the first and second vertebra (the human atlas and axis) articulate directly with the occipital condyle at the base of the skull. Furthermore, their braincases are reinforced and many other skull bones are strong and stout, especially for a snake. The anatomy and physiology of the anterior third of a uropeltid's body is adapted for driving this strong head forward into the soil. The muscles along the anterior portion of the trunk are large, thick, deep red, and rich in myoglobin, catalytic enzymes, and mitochondria, all biochemical or cellular adaptations that permit sustained activityThese muscles are loosely attached to the rest of the body, so they can simultaneously push the sides of the body against the tunnel walls and move the head forward, without pushing the rest of their bodies backwards. To accomplish this, muscles in the posterior body squeeze the anterior vertebral column into a sequence of hairpin turns, not unlike those formed in the vertebrae of large, elongate prey when they are eaten by snakes.3 Because the tip of the nose creates a narrow burrow that is later widened by the flexing of the body, uropeltids can burrow effectively among rocks and roots.4 Like a freight train, the anterior fifth of the body is like a locomotive in that it contains almost all of the propulsive machinery, and pulls along behind it the mostly-inert posterior trunk like the other train cars, containing viscera, embryos, food, etc., all protected on the end by a caboose-like caudal shield.  You can get some idea of how it works in this video (compare the forceful muscle contractions here with how the rest of the body is simply dragged underground here).

Schematic diagram of a uropeltid burrowing, from Gans et al. 1978.
The dark black areas between the snake and the tunnel wall indicate
firm contact. In A) the snake's vertebral column is curved and pushing
against the sides of the tunnel. In B) the firm contact between the curved spine
and the tunnel walls acts as a base against which the head can push,
extending the tunnel forward. The widened body narrows as the spine uncurves.
In C) the snake pulls its vertebral column forward and reintroduces
the curves, which widen the body and the tunnel. The rest of the body
is pulled along without doing any work or needing to resist any force.
This division of labor is similar to that seen in some caecilians, which burrow in a similar way and thereby create tunnels that are wider than their bodies.  And, unlike scolecophidians and amphisbaenians5, they can burrow without pushing against their tails, which leads to the question of what exactly their weird, shield-like tails are for, if not being pushed against? It is thought that the function of these eponymous tails is to collect dirt as the snakes burrow, forming a "plug" that protects the snake from behind. The scale texture of the tail shield scales is deeply ridged, in sharp contrast to the texture of the body scales, which instead bear regular microstructure that inhibits wetting, sheds dirt, reduces friction, and produces iridescent colors. There is also evidence that the tail disc develops over the lifetime of some species, because juveniles do not have modified tails (although they do have large, deep red axial muscles like those of adults).

Uropeltids from Duméril, Bibron, & Duméril's
1854 Erpetologie Générale

Top left and top right: Rhinophis philippinus
Center left and center right: Rhinophis saffragamus
(formerly Pseudotyphlops philippinus)
Bottom left and bottom right: Uropeltis ceylanica
Center top and center bottom: Plectrurus perroteti
A new phylogeny, the most comprehensive yet, nevertheless includes DNA from just five of the eight genera of uropeltids. The most diverse and well-known genera are Uropeltis and Rhinophis, containing 24 and 19 species respectively. These are also the most highly specialized for burrowing. Rhinophis is so bizarre that it was originally described as a subgenus of the legless lizard genus Anguis. In contrast, the smaller and more poorly-known genera Brachyophidium (1 species), Melanophidium (4 species), Platyplectrurus (2 species), Plectrurus (4 species), and Teretrurus (1 species) have less highly modified heads, tails, and body musculature. Apparently these species are unable to tunnel in dry grassland soils, instead remaining belowground until rain softens the soil. Although the 'shola' forests have been greatly reduced, in recent years many of the remnants have been protected. In contrast, the high-altitude grasslands favored by certain species have, like grasslands all over the world, been largely ignored from a conservation standpoint. A single species in an eighth genus, Pseudoplectrurus, is known only from the original specimens collected by Beddome in 1870, from atop the 6000' Mount Kudremukh. It seems that uropeltids first evolved in India at least 37 million years ago, and crossed only once onto Sri Lanka, an island with one of the most phylogenetically diverse snake faunas in the world, but which has maintained its distinctiveness from the Indian mainland despite several extended periods of land connection during the past 500,000 years.

Uropeltis macrolepis eating an earthworm
Unfortunately, we still know precious little about the ecology of uropeltids. Most species eat 80-90% earthworms, but they may snack upon the occasional earwigs, termites, or caterpillars. They are eaten by kraits (genus Bungarus) and vinesnakes (genus Ahaetulla), as well as wild boars, mongoose, owls, and galliform birds. They mate during the rainy season and females give birth to 3-9 live young at a time. Like many fossorial snakes, some species are brightly colored on the underside, especially on the tail and neck. These colors may send warning signals to predators, including possibly mimicking the coloration of some venomous kraits or centipedes. It's likely that a high amount of diversity remains to be described. If you want to read about the current state of our knowledge of uropeltid diversity and taxonomy, including outlines of the genus-level groups that are supported by molecular and morphological phylogenies, not to mention numerous color photographs, you can do so here.

1 In the same issue, sandwiched between "Alpine Orthoptera from central Asia" and "Hand-list of the Birds of India, Part IV", appears an article with the nonchalant title "A few hints on crocodile shooting (with two Plates)", as well as a short note by a Miss Kennion called "Crocodile shooting in Nepal". Sport hunting of predators was common during the British colonial period, and evidently human babies were sometimes used as bait. It's a good thing Beddome and Wall were paying attention to uropeltids back then, because nobody else was.

2 Interestingly, a children's book written in 1947 by Vera Barclay contains a possible description of Col. Beddome. The book is called "They Met a Wizard" and the titular wizard is a zoologist living in colonial India with a special interest in snakes. Ms. Barclay was the great niece of Col. R.H. Beddome and it's likely that she knew him growing up and based her description of the zoologist in the story at least in part on her memories of him.

3 As a result, some early descriptions of uropeltids, such as Günther's The Reptiles of British India or Wall's Ophidia Taprobanica, contained erroneous claims that the neck was "swollen and knuckled" or that the head was very frequently bent to one side, as a result of the snake being preserved with the axial muscles contracted and unconstrained by tunnel walls.

4 I cannot improve upon the ingenious phrasing used by Carl Gans to describe the burrowing of uropeltids: "The burrowing method provides an ideal tunneling device for an unpredictably inhomogeneous substratum. The initial divot driven by the head is quite narrow and will be deflected by roots or rocks. When it passes close to such effectively nondeformable and nondisplacable objects, the opposite wall of the tunnel will be compressed unevenly so that the final tunnel achieves its full if meandering diameter by extra asymmetric compression of the softer zones."

5 Most amphisbaenians bite pieces out of their prey rather than swallowing it whole, so they are less likely to be impeded by a food bolus while burrowing.


Thanks to Sara Ruane, Satyen Mehta, and M for the use of their photos, and to the Rare, Endangered and Threatened Plants of Southern Western Ghats database for sharing their beautiful map.


Extremely similar head (top) and tail (bottom) of
Uropeltis macrorhynchus
Beddome, R. H. 1886. An account of the earth-snakes of the peninsula of India and Ceylon. Annals and Magazine of Natural History 17:3-33 <Biodiversity Heritage Library>

Bossuyt, F., M. Meegaskumbura, N. Beenaerts, D. J. Gower, R. Pethiyagoda, K. Roelants, A. Mannaert, M. Wilkinson, M. M. Bahir, K. Manamendra-Arachchi, K. L. N. Peter, C. J. Schneider, V. O. Oommen, and M. C. Milinkovitch. 2004. Local endemism within the Western Ghats-Sri Lanka biodiversity hotspot. Science 306:479-481 <download>

Comeaux, R. S., J. C. Olori, and C. J. Bell. 2010. Cranial osteology and preliminary phylogenetic assessment of Plectrurus aureus Beddome, 1880 (Squamata: Serpentes: Uropeltidae). Zoological Journal of the Linnaean Society of London 160:118-138 <ResearchGate>

Gans, C. and D. Baic. 1977. Regional specialization of reptilian scale surfaces: relation of texture and biologic role. Science 195:1348-1350 <abstract>

Gans, C., H. C. Dessauer, and D. Baic. 1978. Axial differences in the musculature of uropeltid snakes: the freight-train approach to burrowing. Science 199:189-192 <abstract>

Ganesh, S. 2010. Richard Henry Beddome and south India’s herpetofauna—a tribute on his centennial death anniversary. Cobra 4:1-11 <link>

Ganesh, S. 2015. Shieldtail snakes (Reptilia: Uropeltidae)–the Darwin’s finches of south Indian snake fauna? Pages 13-24 in P. Kannan, editor. Manual on identification and preparation of keys of snakes with special reference to their venomous nature in India. Proceedings by Govt. Arts College, Udhagamandalam, Tamilnadu, India <ResearchGate>

Ganesh, S. R. and S. R. Chandramouli. 2013. Endangered and Enigmatic Reptiles of Western Ghats – An Overview. Pages 35-61 in N. Singaravelan, editor. Rare Animals of India. Bommanampalayam Bharathiyar University (Post), Tamil Nadu, India <Google book>

Gaymer, R. 1971. New method of locomotion in limbless terrestrial vertebrates. Nature 234:150-151 <abstract>

Gower, D. J. 2003. Scale microornamentation of uropeltid snakes. Journal of Morphology 258:249-268 <full-text>

Günther, A. 1864. The Reptiles of British India. Robert Hardwick, London <Biodiversity Heritage Library>

Olori, J. C. and C. J. Bell. 2012. Comparative skull morphology of uropeltid snakes (Alethinophidia: Uropeltidae) with special reference to disarticulated elements and variation. PLoS ONE 7:e32450 <full-text>

Smith, M. A. 1943. The Fauna of British India. Volume III. Serpentes. Taylor & Francis, London <full-text>

Pyron, R. A., S. R. Ganesh, A. Sayyed, V. Sharma, V. Wallach, and R. Somaweera. 2016. A catalogue and systematic overview of the shield-tailed snakes (Serpentes: Uropeltidae). Zoosystema 38:453-506 <link>

Rajendran, M. 1985. Studies in uropeltid snakes. Madurai Kamaraj University, Madurai.

Rieppel, O. and H. Zaher. 2002. The skull of the Uropeltinae (Reptilia, Serpentes), with special reference to the otico-occipital region. Bulletin of the Natural History Museum: Zoology 68:123 <download>

Shanker, K. 1996. Nature watch: secrets of the shieldtails. Resonance 1:64-70 <full-text>

Wall, F. 1921. A new snake of the family Uropeltidae. Journal of the Bombay Natural History Society 28:41-42 <Biodiversity Heritage Library>

Wall, F. 1921. Ophidia Taprobanica, or the Snakes of Ceylon. H. R. Cottle, Govt. Printer, Colombo <Biodiversity Heritage Library>

Wall, F. 1922. Acquisition of four more specimens of the snake Brachyophidium rhodogaster Wall. Journal of the Bombay Natural History Society 28:556-557 <Biodiversity Heritage Library>

Williams, E. E. 1959. The occipito-vertebral joint in the burrowing snakes of the family Uropeltidae. Breviora 106:1-10 <Biodiversity Heritage Library>

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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.