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Monday, April 30, 2012

Dwarf pipesnakes

The only photograph of Anomochilus monticola and
when I wrote this article, the only photo of any anomochilid
Photograph by Indraniel Das
Republished from Lillywhite 2014
A contest to be the most enigmatic snake would be like a contest to be the least well-known president serving between Jackson and Lincoln (seriously, name even one). But the dwarf pipesnakes (Anomochilidae) make even vice president Elbridge Gerry look like Marilyn Monroe by comparison.

Ok, not literally
It's hard to overstate how obscure anomochilids are. A paper published in 2007 using morphological and molecular data to examine the phylogeny of snakes was unable to incorporate the anomochilids because no molecular data on these snakes were available. This seems unbelievable in a day and age when it takes only a day and $1000 to sequence an entire human coding genome. Of course, it isn't inadequacies of technology that have kept the genes of anomochilids from us - it's lack of anomochilids, specifically fresh anomochilid tissue samples. In all museums in all the world, the Anomochilidae are represented by fewer than 15 specimens. Bigfoot has been seen more times than that.

But never collected
The first anomochilid was collected by Max Weber in Sumatra and described  in 1890 by Theodorus Willem van Lithe de Jeude, a curator of the Leiden Museum in the Netherlands (not to be confused with Erland of the same name, of Running Man fame). It was named Anomalochilus weberi after its collector, who also edited the volume in which its description was published, and it was one of only three snakes illustrated therein, out of 50 species covered. The spelling of the genus was changed from Anomalochilus to Anomochilus by Berg in 1901, because the former was already in use for a beetle.

Anomochilus weberi on the left (1, 2, & 3); on the right (4, 5, & 6) is Asthenodipsas malaccana, a pareatid 

The second anomochilid specimen was collected in 1915 by Edward Jacobson, also in Sumatra, and again described by van Lithe de Jeude in a 1922 paper in the journal Zoologische Mededelingen. He assigned it to the same species as the first, A. weberi. These two Sumatran specimens, together with one from Borneo, are all that we know of Anomochilus weberi.

Anomochilus weberi line drawing from de Rooij's 1917 book
The Reptiles of the Indo-Australian Archipelago
The second species of anomochilid wasn't discovered until 1940, when its description was published by Malcolm Smith of the British Museum in the Annals and Magazine of Natural History, the same journal in which Alfred Russel Wallace's 1855 paper "On the Law which has Regulated the Introduction of New Species" pre-empted Darwin's theory by four years. Smith named this species Anomochilus leonardi, again after its collector, G.R. Leonard, who may be the only person ever to have collected two anomochilidsIt is today known from five specimens collected in peninsular Malaysia (including the first, or holotype, and second, or paratype, specimens), and one from the Sabah province of northern Borneo. The Sabah specimen was collected by Raymond Goh in 1981, but sat undescribed in the Sabah Museum until 1993.

Figure from Smith 1940
Fast forward to 2002, when a snake collected in 1993 in northern Borneo was described in a book by Rudolf Malkmus and colleagues called Amphibians and Reptiles of Mount Kinabalu (North Borneo). The authors of the book called the snake Cylindrophis ruffus, which is a pipesnake in the family Cylindrophiidae. Although their book included photos of C. ruffus, the snake they described was in fact a third species of anomochilid, which was re-described in 2008 by Indraneil Das and colleagues. They named it Anomochilus monticola, because it was found in a mountainous area, and published the only photos of a living anomochilid known (above, in black and white). Based on the three specimens they had, they noted that A. monticola was far larger than either A. weberi or A. leonardi, and that it also differed in scalation and pattern. Their paper includes a nice history of anomochild discoveries, after which I have based most of this article.

Skull of Anomochilus leonardi imaged using high-resolution X-ray computed tomography
From Digimorph.org

One group of intrepid researchers, led by David Gower at the Natural History Museum in London, recently tried to extract DNA from three Anomochilus leonardi, with mixed success. Two of these were preserved over 50 years prior, and no genes could be recovered from their tissues. From one specimen collected in 2003, partial sequences of 12S and 16S rRNA mitochondrial genes were amplified, for a total of 221 informative sites. In their trees, Anomochilus leonardi formed a clade with Cylindrophis maculatus, rendering the latter's family, Cylindrophiidae, paraphyletic. However, this conclusion is based on limited data, and this study was done before the discovery of A. monticola, from which fresh tissue could presumably be obtained.

As early as 1890, van Lithe de Jeude noticed the similarities and differences between Anomochilus and other basal alethinophidians. He remarked that it was similar to Anilius scytale, a primitive snake from the Amazon rain forest, in that both lacked a mental groove (a structure on the chin that allows the lower jaw to open widely), but that the scalation of the head was more similar to Cylindrophis than Anilius. Respectively, Anilius, Anomochilus, and Cylindrophis are known as the red, dwarf, and Asian pipesnakes, and they were once treated as a single family together with shield-tailed (uropeltid) and sunbeam snakes (look out for future articles!), though today these are all separated into different families. In outward appearance, all of these snakes are have glossy scales, a result of their scale microornamentation, and a pattern of yellow or white spots with a red tail band against a dark ground color. They have blunt tails and few specialized head scales, with mostly undifferentiated ventral scales. These basal lineages have much to teach us about snake evolution, if we can find enough of them to learn from!

Scanning electron microscope photograph of ventral scale
microornamentation of Anomochilus leonardi: BMNH 1946.1.17.4

Despite all the mystery, we do know some intriguing things about anomochilids. Like some basal snakes, but unlike many, Anomochilus has pelvic girdle vestiges. However, it does possess vestiges of pectoral girdle muscle, unusual among snakes, none of which have any vestige of a pectoral girdle bone. In addition, Anomochilus is unique in having lost the left lung entirely, a structure which is vestigial, but still present, in most other snakes. Like other basal snakes, Anomochilus has only a few teeth - 3 in each upper jaw and 5 in each lower jaw. What they eat is a matter of pure speculation, as are most details about how they reproduce (one female specimen contained four eggs, so we know that they are probably all oviparous, with small clutch sizes). Most of these basal alethinophidians eat elongate vertebrates, such as caecilians, amphisbaenians, and other snakes, because they do not have sufficiently flexible skulls to consume the very large prey items eaten by the macrostomate snakes (boas, pythons, and caenophidians).


I would like to thank exactly no photographers, because apparently no one has ever taken a picture of these things, except for Das et al., who thoughtfully published photos of the type specimen of Anomochilus monticola in 2008.

Update, 11 September 2014: Konrad Mebert recently made me aware of a second color photograph of an anomochilid, posted by a mountain biker in Kuala Lumpur on Project NOAH. What a remarkable find!

Anomochilus leonardi
Photo by ImranKz
Update 4 February 2015: I just learned of some relatively new photos of A. leonardi taken in Selangor, Malaysia, by Hock Ping Guek (Kurt/orionmystery). Check out the link for some awesome photos of pareatids, flyingsnakes, and a ton of other awesome southeast Asian snakes.

Anomochilus leonardi photos by Kurt/Orionmystery
Left: close-up of tail; Center: close-up of head with tongue extended; Right: whole snake

Cundall D, Rossman DA (1993) Cephalic anatomy of the rare Indonesian snake Anomochilus weberi. Zoological Journal of the Linnean Society 109:235-273

Cundall D, Wallach V, Rossman DA (1993) The systematic relationships of the snake genus Anomochilus. Zoological Journal of the Linnean Society 109:275-299

Das I, Lakim M, Lim KKP, Hui TH (2008) New species of Anomochilus from Borneo (Squamata: Anomochilidae). Journal of Herpetology 42:584-591

de Rooij N (1917) The Reptiles of the Indo-Australian Archipelago. Il. Ophidia. E. J. Brill, Leiden. 334 pp. <link>

Gower D, Vidal N, Spinks J, McCarthy C (2005) The phylogenetic position of Anomochilidae (Reptilia: Serpentes): first evidence from DNA sequences. Journal of Zoological Systematics and Evolutionary Research 43:315-320

Greene HW (1997) Snakes: The Evolution of Mystery in Nature. University of California Press, Berkeley
<this is the single best book on snakes available - if you don't own it, shame on you>

Lee MSY, Hugall AF, Lawson R, Scanlon JD (2007) Phylogeny of snakes (Serpentes): combining morphological and molecular data in likelihood, Bayesian and parsimony analyses. Systematics and Biodiversity 5:371-389

Malkmus R, Manthey U, Vogel G, Hoffmann P, Kosuch J (2002) Amphibians and Reptiles of Mount Kinabalu (North Borneo). Gantner Verlag, Rugell. 424 pp. <link>

Smith MA (1940) A new snake of the genus Anomochilus from the Malay Peninsula. Annals and Magazine of Natural History, Series 11 6:447-449 <link>

Stuebing RB, Goh R (1993) A new record of Leonard's pipe snake, Anomochilus leonardi Smith (Serpentes: Uropeltidae: Cylindrophinae) from Sabah, northwestern Borneo. Raffles Bulletin of Zoology 42:311-314

Tsuihiji T, Kearney M, Rieppel O (2006) First report of a pectoral girdle muscle in snakes, with comments on the snake cervico-dorsal boundary. Copeia 2006:206-215

van Lidth de Jeude TW (1890) Reptilia from the Malay Archipelago. II. Ophidia. In: Weber M (ed) Zoologische Ergebnisse einer Reise in Niederlandischost-Indien, vol 1. E. J. Brill, Leiden, The Netherlands, pp 178-192; PL XV-XVI <link>

van Lidth de Jeude TW (1922) Snakes from Sumatra. Zoologische Mededelingen 6:239-253 <link>

Yaakob N (2003) A record of Anomochilus leonardi Smith, 1940 (Anomochilidae) from Peninsular Malaysia. Hamadryad 27:285-286

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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.

Saturday, April 28, 2012

Round Island splitjaw snakes

Adult female Casarea dussumieri 
Not to be confused with the unfortunate Round Island burrowing boa (Bolyeria multocarinata), last seen in 1975, the Round Island keel-scaled boa is still with us, although just barely. In 1996, less than 250 adult individuals remained alive, although recent captive breeding efforts have raised that to about 1000. Together, Casarea and Bolyeria made up the strange and intriguing family Bolyeriidae. Although they're sometimes called 'boas', they are distinct from the Boidae, or true boas, in not having any vestiges of a pelvic girdle. In fact, they are more closely related to the advanced snakes (Caenophidia) than to the true boas, although their phylogenetic relationship to other snakes is not quite certain. Some have advocated calling them 'splitjaw snakes' instead of boas. Due to their remote range (and the extirpations they suffered), few herpetologists have been lucky enough to see a living specimen, especially a wild one. I hope to cover what is known about these two species in this short article.

Mauritius and surrounding islets
Round Island is a herpetologically interesting volcanic islet, 151 ha (just over half a square mile) in size, located approximately 22.5 km NNE of Mauritius, in the Indian Ocean east of Madagascar. Round Island and Mauritius are part of the Mascarene archipelago, which formed between 35 and 2 million years ago as a result of the Réunion hotspot. Before the 16th century, no humans inhabited the islands, which were covered in unique tropical moist broadleaf forest. All of the Mascarene flora and fauna arrived by oversea dispersal, possibly using prehistoric islands of the Mascarene plateau, now submerged by the sea, as 'stepping stones'. Round Island is also home to an endemic skink (Leiolopisma telfairii) and an endemic day gecko (Phelsuma guentheri). Both snakes used to be found on Mauritius and other nearby islets, from which they were first extirpated. Microhabitats include fallen palm fronds and the burrows of nesting pelagic birds such as shearwaters. Captive breeding efforts are hindered by the fact that these two endangered lizards constitute the sole natural prey of Casarea, so they must be enticed to eat mice in captivity, which is more easily said than done. A few parasites of the taxon have been described, mostly by Peter Daszak of the EcoHealth Alliance.

What certainly hasn't helped clarify their taxonomy is that relatively few specimens and tissue samples are available for study. Twenty-eight genes have been sequenced for Casarea, but (unsurprisingly) none for Bolyeria, which is represented in museums by only seven specimens. Scientists are understandably reluctant to collect fresh Casarea specimens for study (DNA is far easier to sequence from fresh tissue), and the number of snakes in captivity is relatively few. Only in 2005 did we learn, posthumously, that Bolyeria probably laid eggs, rather than give live birth like many boas.

Casarea dussumieri in captivity
The skull of Casarea, which was described using high-resolution X-ray computed tomography by Masiano & Reippel (2007), is unique in having the maxilla subdivided into two movably jointed parts. That's right - the maxilla - the upper jaw. Snakes are renowned for the highly kinetic skulls, but no other snakes (or vertebrates, for that matter) have a kinetic maxilla. This jaw and its associated musculature are the basis for classifying Casarea and Bolyeria in a family of their own. Other lizard-eating snakes have analogous adaptations for grasping their hard-bodied prey, but no group takes this adaptation to such extremes as the bolyeriids. But think - on an island with no mammals and few birds, with little else but lizards to eat, selection is stronger than anywhere else for adaptations to saurophagy.

High-resolution X-ray computed tomography image of Casarea skull
Juvenile Casarea
Round Island keel-scaled boas reach 1 to 1.5 meters in length. Color changes ontogenetically (with age). According to observations made in captivity, Casarea are primarily nocturnal. Donald McAlpine, a researcher at the Jersey Wildlife Preservation Trust, where captive C. dussumeri are bred and studied, published a paper in 1983 showing data that captive specimens changed color every day, from light at night to dark during the day, reminiscent of another island-living boa, the Hog Island race of Boa constrictor from Cayos Cochinos in Honduras. Physiological color change in snakes has also been documented in the southeast Asian snake Enhydris gyii. Whether the purpose is cryptic, thermoregulatory, or something else entirely, we can only speculate. McAlpine ended his paper with the statement: "Hopefully this interesting phenomenon will be examined before Casarea becomes extinct." McAlpine's paper has been cited only twice, and as far as I can tell no research on this topic has been done since. An expedition to look for Bolyeria in 2001 was unsuccessful.

Painting of Bolyeria - no photos of living animals are known
Update 11/2/2013: I have just learned of an effort by the Mauritius Reptile Recovery Programme to reintroduce Casarea dussumieri to Gunner's Quoin, a nearby island where invasive rats and rabbits have been extirpated and to which the boa’s key prey item, the Telfair’s skink, was reintroduced from Round Island in 2007. In October of 2012, six months after this article was published, 60 C. dussumieri were released on Gunner's Quoin after 150 years of absence. If I learn the results of efforts to monitor this new population, I will post them here.


Thanks to photographers Richard Gibson, Gregory Guida, Mike Pingleton, Drymarchon32, and Jim.


Bauer A, Günther R, 2004. On a newly identified specimen of the extinct bolyeriid snake Bolyeria multocarinata. Herpetozoa 17:179-181.

Cundall D, Irish FJ, 1989. The function of the intramaxillary joint in the Round Island boa, Casarea dussumieri. Journal of Zoology 217:569-598.

Frazzetta T, 1971. Notes upon the jaw musculature of the Bolyerine snake, Casarea dussumieri. Journal of  Herpetology 5:61-63.

Hallermann J, Glaw F, 2005. Evidence for oviparity in the extinct bolyeriid snake Bolyeria multocarinata (Boie, 1827). Herpetozoa 19:82-85.

Korsós Z, Trócsányi B, 2002. Herpetofauna of Round Island, Mauritius. Biota 3:77-84.

Korsós Z, Trócsányi B, 2006. The enigmatic Round Island burrowing boa (Bolyeria multocarinata): survival in the wild remains unconfirmed. African Herp News 40:2-7.

Maisano JA, Rieppel O, 2007. The skull of the Round Island boa, Casarea dussumieri Schlegel, based on high-resolution X-ray computed tomography. Journal of Morphology 268:371-384.

McAlpine DF, 1983. Correlated physiological color change and activity patterns in an Indian Ocean Boa (Casarea dussumeri). Journal of Herpetology 17:198-201.

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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.

Thursday, April 26, 2012

Utah's boa

When most people think of boas, images of South American tropical rain forests come to mind, home to iridescent rainbow boas, brightly colored emerald tree boas, and enormous boa constrictors. Few people think of the canyons of northern Utah, which are home to one of only two native North American boas, the rubber boa (Charina bottae). Discovered in California and described by the French zoologist Henri Blainville in 1835, rubber boas range from northern Utah and western Wyoming to southern British Columbia and central California. An adult rubber boa is about the size and shape of a polish sausage, and juveniles aren’t much bigger than a crayon. A rubber boa’s leathery skin is a similar color to creamy coffee, and its small scales give it a rubbery texture. These boas have countersunk jaws to prevent dirt from entering their mouths while burrowing. Other unusual anatomical features include a vestigial pelvic girdle, similar to those of other boas, with sexually dimorphic 'spurs' (actually reduced femur bones) that males use to titillate females during mating, and a blunt tail covered in a large, shield-like scale.

Rubber boas are active at night during the summer, as evidenced by their vertically elliptical pupils. They can be among the first snakes to come out of hibernation in the spring. In Cache County, Utah, where I live, rubber boas are found as early as March and as late as November. Rubber boas hibernate in talus slopes and deep rock crevices. Gravid females use these same habitats for thermoregulation between April and August, maintaining body temperatures around 88° Fahrenheit. They give live birth to an average of four young once every two to three years in late summer, so the survival of juveniles must be very good in order for populations to remain stable. They must also be relatively long-lived in the wild - some have lived over 30 years in captivity, and it's not unheard of for other boas to reach 40 or 50.

Spurs of a male rubber boa
It’s hard to imagine these docile, slow-moving snakes as predators, but rubber boas are known to eat mammals, as well as birds, other reptiles, and their eggs. When foraging at night, rubber boas enter mammal burrows to consume litters of nestling mice, voles, moles, shrews, and pocket gophers. Rubber boas fend off protective mothers with their short, blunt tails, which often bear scars from rodent bites. The roughly contemporaneous Eocene origins of rubber boas and rodents suggest that these small boas might have been depredating rodent nests ever since they evolved, as suggested by Javier Rodríguez-Robles, Christopher Bell, and Harry Greene in their 2006 Journal of Zoology paper.

Dorcas and Peterson (1998) described six patterns of thermoregulation in rubber boas from Idaho. These snakes were active at very low temperatures for a snake: an average of 57° F. In fact, rubber boas foraging at night frequently emerged from their warm burrows into cooler air temperatures, which is very unusual for a reptile. Thermoregulation is commonplace among gravid adult females, which use rock outcrops to select temperatures optimal for their developing offspring. In cool years, no rubber boa reproduction may take place. Because they cannot forage to feed when gravid, female rubber boas might go for up to 18 months without eating.

Listen for a shortened version of this post to be read on Utah's NPR segment Wild About Utah!


Thanks to photographers Todd PiersonKaren Petersen, and Anna.


Dorcas ME, Peterson CR (1998) Daily body temperature variation in free-ranging rubber boas. Herpetologica 54:88-103. <link>

Dorcas ME, Peterson CR, Flint MET (1997) The thermal biology of digestion in rubber boas (Charina bottae): physiology, behavior, and environmental constraints. Physiological Zoology 70:292-300. <link>

Rodríguez‐Robles JA, Bell CJ, Greene HW (1999) Gape size and evolution of diet in snakes: feeding ecology of erycine boas. Journal of Zoology 248:49-58.

Rodríguez-Robles JA, Stewart GR, Papenfuss TJ (2001) Mitochondrial DNA-based phylogeography of North American rubber boas, Charina bottae (Serpentes: Boidae). Molecular Phylogenetics and Evolution 18:227-237. <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.

Monday, April 9, 2012

Asymmetrical snakes

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

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

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

That's one sinister snail

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

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

Mandibles (lower jaws) of Pareas iwasakii 
Dorsal view of skull of Pareas iwasakii

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

Data from Pareas iwasakii

Data from 297 specimens

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

Aplopeltura boa

Asthenodipsas malaccanus

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

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

Stills from the video

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

Satsuma is one of the snail genera examined

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

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

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

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

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

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

Asthenodipsas laevis from Malaysia

Aplopeltura boa from Borneo

Pareas formosensis from Taiwan

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



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

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

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

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

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

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

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

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

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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.

Saturday, April 7, 2012

Eel mocassins

In all likelihood, you'll never find me.
If you held a gun to my head (or anyone's) and told me to find you a rainbow snake, even just a single one, I guarantee I wouldn't be able to do it without extraordinary luck. And yet, there are tens, possibly hundreds of thousands of rainbow snakes out there in the rivers and wetlands of the southeast. So it's not a problem of rarity per se. Why is it, then, that these snakes are so seldom seen, even by avid snake hunters?

Rainbow snakes epitomize several of the qualities that make studying snakes challenging. For this reason and others, they have long been among my favorite snakes, a Holy Grail of sorts. They really are worthy of further study, because we know so little about their natural history.

You might ask me: have you ever found a rainbow snake? And I don't mean to brag, but yes, I have. Three times (two were the same snake), I have been smiled upon by the herping deities. At first glance, it doesn't seem that difficult to find one: they are bright pink, yellow, and blue violet. They reach lengths of over six feet long. A snake like that should stick out like a sore thumb. Additionally, they occur throughout the southeastern Atlantic and Gulf coastal plains, areas well-populated by snake hunters and herpetologists.

Range of the rainbow snake - SEGAP 

But in reality, very few people are lucky enough to see even one, and finding a rainbow snake is a watershed event in the life of a herper. What, then, causes the apparent rarity of this species?

Let's start by reviewing what we know about the natural history of this snake. It is one of two species in the genus Farancia, the other being Farancia abacura, the mud snake. While the common names of the two species conjure quite different images, the two snakes are actually quite similar in appearance and morphology.

Farancia abacura (left) and F. erytrogramma (right) 

The mud snake is a bit better known and a bit more commonly encountered, but finding one is still an event, and as little is known about mud snake natural history as about rainbow snakes. Although the two species were once considered to be in different genera (Abastor for erytrogramma), they are clearly sister taxa. The ease of classifying them stops there, however. In order to understand the broader phylogenetic position of Farancia, we need to look at the historical biogeography of North America. Although the dates in question are a matter of some debate, the order of the events I am about to chronicle is fairly solid. The colubroid snake fauna that inhabited the continent 16 million years ago were called the xenodontine snakes. Before the more recent invasion from Asia by and radiation of many of the familiar North American snakes (natricines like garter and watersnakes, colubrines like rat and kingsnakes, elapids such as coral snakes, and vipers), xenodontines had the continent mostly to themselves, save for a few boas and blindsnakes. There is no question that there are fewer xenodontine species alive today than there were at that time. Whether the xenodontines were never very abundant, or whether they have been pushed to marginal niches by more competitive colubroids, their ancestors' common descendants survive in South America, in the hyper-diverse radiation known as dipsadines (including many unfamiliar snakes, but a few semi-familiar ones, such as the goo-eating Dipsas, coral-snake mimicking Eyrthrolamprus, and pencil-thin Imantodes). The reason the xenodontines and dipsadines have separate names despite sharing a common ancestry is that they developed in isolation for several million years, when North and South America were separated by ocean (though the separate names , like much else in herpetology, aren't universally accepted, applied, or used). A few dipsadines have re-invaded North America following the recent reconnection of NA and SA (~3.5 million years ago), including the desert nightsnake, Hypsiglena torquata, in the west, and the pine woods snake, Rhadinaea flavilata, in the southeast. In a few places they have met the descendants of their great-great-grandparents, the relict North American xenodontines. It is to this group that the two Farancia belong, together with a few other interesting North American snakes, including the hog-nosed snakes (Heterodon), ring-necked snake (Diadophis), worm snakes (Carphophis), and sharp-tailed snakes (Contia). The convergence between these xenodontines and some dipsadines is remarkable, but that's a story for a different article.

Farancia erytrogramma
Pseudoeryx plicatilis

So just what is the niche of the rainbow snake? Any field guide will tell you that they are completely aquatic, in part due to their highly specialized diet of American eels (Anguilla rostrata), which they forage for at night (see this video). But a 1964 review by Wilfred T. Neill, herpetologist extraordinaire of Florida and the southeastern US, provides more insight and detail than is typically found in a field guide. Neill had a keen eye for natural history, and it shows in his publication on the rainbow snake.

In his article, Neill states that alkaline (basic) aquatic habitats are inhabited by rainbow snakes, whereas mud snakes tend to inhabit more acidic streams, bogs, and ponds. This is not strictly true - but in general, it serves as a good rule for ecologically separating the two species. Another consideration is that the prey of the mud snake generally inhabit isolated wetlands, which tend to be more acidic, whereas the prey of the rainbow snake can only be found in watercourses with a permanent connection to the ocean. This is because American eels are catadromous fishes, meaning that they spawn in the ocean but live much of their lives in fresh water, sort of the inverse of a salmon, lamprey, or sturgeon. Rainbow snakes are so particular about their diet as adults that they are often called the 'eel moccasin' by "rural residents of the Georgia Coastal Plain" because "ever' time you see one, he got a eel tail a'hangin' out his mouth" (quotations from Neill).

A video still of a rainbow snake eating an eel
Now, you may be familiar with the problems inherent when migrating fishes, like salmon or eels, encounter man-made impoundments along river courses. In the Pacific northwest, anadromous salmon are unable to move upstream past the dam to spawn, which has led fisheries managers to construct 'fish ladders' to help salmon bypass dams. Baby salmon can then move downstream through the dam, although many are certainly obstructed on their journey to the ocean. The situation for the eel is a little different, because they begin life in the ocean instead of at the headwaters of a stream, but the challenges faced during the life of the fish are the same. Upstream of dams along southeastern rivers, eel populations have dwindled to almost nothing, and it's likely that rainbow snake populations in those areas have been affected. In addition to being largely unable to move past dams in either the up or downstream direction themselves, rainbow snakes living upstream of a dam surely have to contend with slowly dwindling eel populations. However, data on rainbow snake population declines are nonexistent. Why? 

Who wouldn't want to study a snake like that? 

One big challenge is the inherent uncertainty in estimating what a species' population size is, given incomplete detection of all individuals. The stochasticity associated with these kinds of estimates is controllable to an extent dependent on the detectability of the species in question (i.e., you can get more accurate population size estimates for highly detectable, recapturable species like watersnakes than you can for undetectable species like rainbow snakes). Because we rely on recapture rate to inform our estimates of population size, animals that are never recaptured don't do much good, which is all of them when detectability is low enough (advances in models using presence/absence data have somewhat mitigated this problem). What's more, detectability varies with species life history, with time of year, with survey method, with spatial scale, with observer experience and bias, and with environmental variables such as temperature, moon phase, rainfall, other species interactions, basically anything that affects animal activity is going to impact detectability. So it's really hard to separate environmental effects that extirpate or reduce the size of a species population (i.e., affect species occupancy) from those that influence their activity (i.e., affect species detectability). Also, anthropogenic environmental effects are often spatially and temporally autocorrelated, so it's hard to assign a decline, if you can find one, to just one cause. These problems are particularly bad for animals whose natural history we don't know that much about, like rainbow snakes.

Some colleagues and I did a study to measure just how hard it was to catch a rainbow snake. We compared the rate of capture to that of six other aquatic snake species that also inhabit isolated wetlands in the South Carolina coastal plain. We used robust presence-absence based models that estimate the probability of detecting a species rather than the population size of that species, so that recapturing the same individual animals was unnecessary. We set minnow traps overnight in different wetlands for the entire summer, and recorded all the snakes that got caught in them. We also recorded information on environmental variables, such as the prey community at each wetland, the wetland hydroperiod, and the wetland's connectivity to other wetlands. We put this data into the model, and asked it to tell us which site features best predicted a high probability of capturing snakes of different species.

Figure from Durso et al. 2011 

As you can see, the likelihood of catching a rainbow snake can be quite low, but it improves in wetlands located close to the nearby Savannah River floodplain. This actually isn't too surprising, considering that their prey live only in rivers. The Savannah has relatively few dams along it, because lowering the water level in certain spots would expose Cesium-contaminated sediments that resulted from the nuclear reactors on the Savannah River Site, where the research was conducted. So, in an indirect way, the radioactive waste might actually be helping the rainbow snake, although how it impacts them directly is difficult to say.

One more enigma about rainbow snakes - it turns out that the conventional wisdom that they are entirely aquatic isn't entirely accurate. You see, unlike most of the aquatic snakes in North America, Farancia lay eggs (remember, they are xenodontines, which are oviparous, as opposed to natricines, like garter and watersnakes, which are viviparous). To do this, they must go onto land, much like a sea turtle must also return to land to lay her eggs. Actually, I think turtles are a good ecological analogy for Farancia. The male Farancia may never leave the water, but the females, when they reproduce, must. Rainbow snakes have sometimes been found in dry, sandy fields, and observations from 1940s Virginia assert that they are "the most abundant snake" and "more often seen on land, [but] equally at home in the water". Many were turned up by plowing fields, but some were found crawling on the surface as well. Nests have been found in the same dry, sandy fields, among mud turtle, slider, and cooter nests. At the aforementioned Virginia site, young rainbow snakes were found under boards in spring and fall, suggesting that some may migrate to the water soon after hatching, whereas others may overwinter in the nest, again in the manner of many turtles.

The mud snake has the largest recorded clutch size of any North American snake, but the rainbow snake is no slouch in the egg department, laying clutches up to 52 eggs in size. Some females may remain with the eggs until they hatch, but this phenomenon is poorly studied.

Juvenile rainbow snake captured in a drift fence 
Wilfred Neill, indefatigable field naturalist and publisher that he was, described two populations of distinctively colored rainbow snakes from brackish water habitats in Florida, with very deep red coloration replacing the yellow on the chin and throat. Neill also described the South Florida Rainbow Snake, Farancia erytrogramma seminola, a supposedly now-extinct subspecies, from three specimens he collected and placed in the collection of Ross Allen (of Reptile Institute fame). These specimens were collected in Fisheating Creek in Glades County near Lake Okeechobee, and they differed from other rainbow snakes in having predominantly black ventral scales. Neill considered this, but not the saltwater populations, distinct because the biogeographic history of south Florida, which was a large island in an archipelago during the Pleistocene, would have allowed some degree of divergence and concomitant isolation, whereas the saltwater populations probably were not isolated from other populations. Argue all you want about what a subspecies is supposed to be (I think they're often relatively meaningless), but recently several conservation groups seized upon the South Florida Rainbow Snake as a posterchild for snake conservation. Now, the rainbow snake can use all the publicity it can get among lawmakers and the general public, and I would eventually like to see a concerted effort to survey and monitor all rainbow snakes rather than just this single population. However, one has to start somewhere, and when it's rainbow snake surveying you're talking about, anywhere is about as good as anywhere else. I spoke with Cameron Young, the director of the Center for Snake Conservation, about his recent expedition to Fisheating creek to look for F. e. seminola. He reported excellent habitat, a creek full of eels, and reliable stories from local folks of rainbow snakes seen recently - so hopes are high for a rediscovery, and an opportunity to learn more about the biology of this remarkable snake.

If you have found a rainbow snake, leave a comment below! You're a member of an elite club, and I'd love to know about it. 

Thanks to photographers John White, Pierson Hill, JD Willson, Todd Pierson, Nathanael Herrera, Cameron Young, and Antoine Baglan, and to Cameron Young for an advance synopsis of his results from Fisheating Creek in March 2012.

Durso AM, Willson JD, Winne CT, 2011. Needles in haystacks: estimating detection probability and occupancy of rare and cryptic snakes. Biological Conservation 144:1506-1513. <link>

Gibbons, J. W., J. W. Coker, and T. M. Murphy, Jr. 1977. Selected aspects of the life history of the rainbow snake (Farancia erytrogramma). Herpetologica 33:276-281.

Haro A, Richkus W, Wahlen K, Hoar A, Busch W, Lary S, Brush T, Dixon D, 2000. Population decline of the American Eel: implications for research and management. Fisheries Management 25:7-15.

Neill, W. T. 1964. Taxonomy, natural history, and zoogeography of the rainbow snake, Farancia erytrogramma (Palisot de Beauvois). American Midland Naturalist 71:257-295.

Palisot de Beauvois, A. 1801. Mémoire sur les Serpens.in C. S. Sonnini and P. A. Latreille, editors. Histoire naturelle des reptiles. Imprimerie de Crapelet : Chez Deterville, Paris.

Powell C, Stevenson DJ, Smith M, Jensen JB, 2010. A new clutch size record for the Mud Snake (Farancia abacura). Southeastern Naturalist 9:177-178.

Richmond ND, 1945. The habits of the rainbow snake in Virginia. Copeia 1945:28-30.

Semlitsch RD, Pechmann JHK, Gibbons JW, 1988. Annual emergence of juvenile mud snakes (Farancia abacura) at aquatic habitats. Copeia 1988:243-245.

Steen, D., C. Guyer, and L. Smith. 2012. Box 9: Relative abundance in snakes: a case study. Pages 287-294 in R. McDiarmid, M. Foster, C. Guyer, J. Gibbons, and N. Chernoff, editors. Reptile Biodiversity: Standard Methods for Inventory and Monitoring. University of California Press, Berkeley, CA.

The taxonomic history of Farancia erytrogramma is not overwhelmingly complex, but it is somewhat interesting, at least to me (which is why this part is in the appendix). The species was originally described as Coluber erotrogrammus, placed in the catch-all non-venomous snake genus Coluber as most snakes were in the early 1800s, only a few short decades after Linnaeus. The description was published in Sonnini & Latreille's "Histoire Naturelle des Reptiles", but the actual author was Palisot de Beauvois, whose "Memoire sue les Serpents" constituted the snakes chapter of HNdR. None of these guys were specifically herpetologists, but the distinction between herpetology and entomology was still pretty hazy back in those days, with most people tending to lump all the creeping things together. They were all three explorers, naturalists, and probably really fun guys. Supposedly Latreille, an orphan who discovered isopods, created the concept of a type species, and was generally considered the foremost entomologist of his time, escaped prison and execution by identifying a rare species of beetle in his cell and so impressing the prison doctor that he secured Latreille's release.

So Palisot de Beauvois gets the naming credit (called the authority) for F. erytrogramma - but he kind of misspelled it. The Latin prefix erythro- means red, but PdB left out the h for some reason, which Neill derided as "etymologically poor" but not an "inadvertent error". Many authors inadvertently gave credit to Sonnini & Latreille or to Latreille alone, and the date of the work was frequently miscited as 1802 (the correct year is 1801). Neill cleared this up in his 1964 review, and synonymized Farancia and Abastor, both named by J.E. Gray of the British Museum, who was "well known for inventing many apparently meaningless scientific names." The only other change in need of explaining is the gender change of erytrogrammus to erytrogramma, to agree with the feminine Farancia instead of the masculine Coluber or Abastor.

In my research for this article, I came across the German words for these species, which I think are just wonderful: schlammnatter for mudsnake and regenbogen-schlammnatter for rainbow snake. Natter means snake, schlamm means mud, and regenbogen means rainbow (from regen: rain, and bogen: arc).

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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.