The 21st century blindsnake revolution

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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.

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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.^↩

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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.^↩

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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>

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

Basics of Snake Taxonomy

A while back, medical-doctor-turned-snake-blog-post-translator-extraordinaire¹ Alvaro Pemartin asked me to write an article covering basic snake taxonomy. Taxonomy is the branch of biology that deals with naming and classifying organisms. Biologists still use the Linnean hierarchical system for taxonomy, which is convenient for grouping organisms, but there is a move towards using phylogenetic systematics and the evolutionary species concept in taxonomy, particularly in the sense that recognizing and giving names to non-monophyletic groups is discouraged.² We'll primarily stick with the Linnean system in this article, which uses particular suffixes to denote the taxonomic level (for example, all animal families end in '-idae' and all subfamilies end in '-inae'). However, I've also included some cladograms, which are the most useful figures for understanding evolutionary relationships. If you haven't read one before, you can read up on them here, here, or here, but just know that they essentially work just like a family tree.

Snake Diversity

My only criticism of this film:
not enough snakes

There are about 3,400 species of snakes in the world. All are placed in the suborder Serpentes (aka Ophidia) of the order Squamata, which also includes lizards, from which snakes evolved about 190 million years ago during the Jurassic Period. Extant (modern or living) snakes are divided into two major groups, the blindsnakes (aka threadsnakes or scolecophidians) and the advanced or true snakes (alethinophidians). Advanced snakes are also divided into two non-monophyletic groups, the "older snakes" (henophidians) and the "recent snakes" (caenophidians). The vast majority of all living snakes, about 77% or 2,650 species, are caenophidians, including most of the snakes you've probably heard of: rattlesnakes, cobras, kingsnakes, and many others. A few well-known snakes are henophidians, namely boas and pythons. Most scolecophidians are poorly known. Let's break down each of these groups in slightly more detail.

Scolecophidians

Ramphotyphlops braminus,
a parthenogenetic blindsnake

There are about 400 species of scolecophidians, divided into five families and found mostly in the tropics. They are commonly called blindsnakes, because many have vestigial eyes as a result of their fossorial lifestyle, or threadsnakes, because most are very thin. Most have unspecialized ventral scales, shed in thick rubbery rings, and have a spine at their tail tip. Many eat termites and ants. Most are probably oviparous, or egg-laying, but their reproductive biology is poorly known. Scolecophidians diverged from alethinophidians about 125 million years ago during the Cretaceous Period. You can read more about a fascinating mutualism between a blindsnake and an owl here, or about basic blindsnake biology here.

Phylogenetic tree showing currently accepted hypotheses of snake relationships. Figure from Lee et al 2007.
Thick lines are supported by both morphological and molecular studies, thin solid lines are supported
primarily by similarity of morphology, dotted lines are supported primarily by molecular analyses.

"Henophidians"

Anilius scytale
Red Pipesnake

"Henophidians" are a diverse, if species-poor, group of snakes. I mentioned earlier that they are non-monophyletic, meaning that some henophidians are more closely related to caenophidians than others, which is why the name of their group is in quotation marks. All henophidians shared a common ancestor about 98 million years ago, during the Cretaceous Period. There is some pretty major uncertainty about how henophidians are related to one another, but many taxonomies divide them into four superfamilies (which end in '-oidea' under the Linnean system). The most primitive, the Uropeltoidea, is comprised of five families (Aniliidae, Tropidophiidae, Anomochilidae, Cylindrophiidae, and Uropeltidae) that lack the ability to open their mouths very widely. These snakes have stout skulls with few lizard-like teeth, short tails, and poorly developed ventral scales. Most are viviparous, meaning that they give birth to live young, except the anomochilids, which are oviparous. There is better evidence linking the former two and latter three groups than there is for combining all five families together into a single superfamily. Also, two enigmatic species in the genus Xenophidion might belong somewhere in here.

Calabaria reinhardtii,
the Cameroon Burrowing Boa,
the only oviparous booid

The rest of the henophidians together with the caenophidians are often called the macrostomatans, because they have the ability to open their mouths (Greek: stomata) very wide and consume very large (Greek: macro) prey items. The most primitive of these are the oviparous Pythonoidea, a superfamily including true pythons (Pythonidae) as well as two small lesser-known groups respectively known as the Asian and Neotropical sunbeam snakes, the xenopeltids and the loxocemids. Pythonoids and a superficially similar but surprisingly unrelated group, the  viviparous booids (consisting of true boas and their less well-known relatives, the ungaliophine dwarf boas and the erycine sand boas),  diverged from other henophidians about 75 million years ago. Finally, the most advanced henophidians, the oviparous splitjaw snakes (aka Round Island "boas" or bolyeriids), diverged just slightly later than or around the same time as the true boas. Because the splitjaw snakes constitute only a single family and were historically considered boas, you don't usually hear them referred to as a fourth superfamily.

Caenophidians

Acrochordus granulatus
Little Filesnake

This huge group is divided into two superfamilies, called Acrochordoidea and Colubroidea. The first is small, containing only three species of Acrochordus, the filesnakes of southeast Asia and north Australia. These diverged from other caenophidians about 60 million years ago. The second is huge and there is some uncertainty about the relationships therein, although thanks to recent work by Alex Pyron and his colleagues, the picture is becoming more clear. Traditionally, colubroids have been divided into groups based on their tooth morphology: those with fixed fangs were placed into Elapidae, those with folding fangs into Viperidae, and those without fangs lumped into Colubridae. The first two of these groups have proven to be for the most part monophyletic, certain exceptions notwithstanding. However, a more nuanced and accurate view of colubroid snake taxonomy is emerging thanks to a combination of molecular tools and decades of careful work by snake morphologists. Ready for it? Here it is:

Figure from Pyron et al. 2011

These snakes are exciting! These snakes have venom, excellent color vision, and sophisticated chemosensory, prey acquisition, and antipredator abilities. Also they have spines on their hemipenes. Also they are awesome. Can you tell which group is my favorite?

Dendrelaphis punctulatus
Common Treesnake

The traditional three-family tooth-morphology arrangement of colubroids has been replaced by the seven family arrangement seen above.³ Three of those seven families include several subfamilies. The most primitive colubroids are the xenodermatids, or odd-scaled snakes, which diverged from the others about 47 mya. The snail-eating pareatids are next, a group you'll be familiar with if you've been following this blog since the beginning. Next diverged the viperids or vipers, about 35 million years ago. There are three subfamilies of vipers: the old world viperines, the widespread crotalines (or pit vipers), and the monotypic Azemiopsinae, or Fea's Viper. True colubrids are still a large group, even though many species have been removed to the "new" families. The subfamilies are large and diverse, although most lack dangerous venom (a few species notwithstanding). You can read the story of the evolution of some of the subfamilies here. There are many well-known colubrids, including ratsnakes, kingsnakes, racers, hog-nosed snakes, and many others. Homalopsids, including some that chew their food, are a small but interesting group of semi-aquatic snakes found in southeast Asia. The front-fanged elapids (including cobras and coral snakes) have retained their monophyly, and little support has been found for recognizing the sea snakes as a separate family. Finally, we have the Lamprophiidae, a new family erected to contain former colubrids that turned out to be closer relatives of elapids. Lamprophiids also represent several interesting subfamilies, including the side-stabbing atractaspines, scale-polishing psammophines, and Malagasy pseudoxyrhophiines. I think Darren Naish would agree that there's plenty of fodder for future articles in these groups.

One a closing note, some non-snakes that are commonly mistaken for snakes, primarily because they have no legs, include:

• Legless lizards: There are several groups of legless lizards. The North American glass lizards are among the most familiar. All have external ear openings and most have eyelids. In one sense, snakes are but one very diverse group of legless lizards.
  
• Amphisbaenians: These are also technically lizards, but under some older taxonomies they are referred to as a separate group of reptiles, because they have a vestigial right lung and have a unique skeletal structure.
• Caecilians: These most primitive of amphibians have slimy skin and are found underground in the world's tropics. Many are common prey of coral snakes.
• Eels: Elongate fishes that actually do have limbs in the form of fins. There are several groups of fishes that are all colloquially called eels, including spiny eels, fire eels, electric eels, and true eels (Anguilliformes). Some amphibians are also sometimes called eels, including amphiumas or conger eels, sirens or mud eels, and rubber eels, a kind of caecilian.
• Worms: There are several different major groups of worms, including roundworms (nematodes), flatworms (platyhelminths), and segmented worms (annelids).

Snake taxonomy is a complicated field and there is still much disagreement among experts. I have made several oversimplifications above, so if this is your area of expertise feel free to chime in with a comment or two. I hope you're looking as forward to reading more about many of these groups as I am looking forward to writing about them.

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1 His wife tells me that mediocre is actually more accurate^↩

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2 A monophyletic group is one that contains a common ancestor and all of its descendants. Examples include groups like animals, vertebrates, mammals, birds, amphibians, primates, and snakes. A non-monophyletic group is one that either omits some descendants (e.g., "reptiles", which does not include birds, or "fishes", which does not include tetrapods) or omits the common ancestor (e.g., warm-blooded vertebrates, which includes mammals and birds but not their cold-blooded common ancestor). ^↩

ACKNOWLEDGMENTS

Thanks to ptrick127, Gary Nafis, Tein-Shin Tsai, and Stephen Zozaya for use of their photos.

REFERENCES

Lee, M. S. Y., A. F. Hugall, R. Lawson, and J. D. Scanlon. 2007. Phylogeny of snakes (Serpentes): combining morphological and molecular data in likelihood, Bayesian and parsimony analyses. Systematics and Biodiversity 5:371-389 <link>

Pyron, R. A., F. Burbrink, and J. J. Wiens. 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Biology 13. DOI: 10.1186/1471-2148-13-93 <link>

Pyron, R. A., F. T. Burbrink, G. R. Colli, A. N. M. de Oca, L. J. Vitt, C. A. Kuczynski, and J. J. Wiens. 2011. The phylogeny of advanced snakes (Colubroidea), with discovery of a new subfamily and comparison of support methods for likelihood trees. Molecular Phylogenetics and Evolution 58:329-342 <link>

Zaher, H., F. G. Grazziotin, J. E. Cadle, R. W. Murphy, J. C. Moura-Leite, and S. L. Bonatto. 2009. Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: A revised classification and descriptions of new taxa. Papeis Avulsos de Zoologia (Sao Paulo) 49:115-153. <link>

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