Tibetan Hot-spring Snakes

Everyone likes a good soak in a hot spring now and again, but imagine spending your whole life in one! Now imagine being the size of a pencil and unable to regulate your own body temperature, and you're doing a pretty good approximation of a Tibetan Hot-spring Snake (Thermophis). These tiny snakes reach only 2.5 feet in length and are found at fewer than ten sites on the Tibetan plateau in the Himalayan Mountains of south-central China, all above 14,000 feet elevation. For comparison, that's at least as tall as Mt. Rainier in Washington, Pike's Peak in Colorado, or Mont Blanc in the Alps. To cope with the cold, hot-spring snakes inhabit marshes, rivers, and rocky areas around sulfur-free hot springs, where they eat amphibians and fishes, including the dicroglossid frog Nanorana parkeri, the minnow Schizothorax oconnori, and elongate stone loaches in the genus Triplophysa. As you can see from this video, these are highly charismatic snakes.

Frank Wall

Hot-spring Snakes were first described in 1907 by a physician and herpetologist living in India named Frank Wall. Wall received specimens of this snake sent  from Tibet by Lieutenant F. M. Bailey, who reported that local people familiar with the snake told him that it could be found within half a mile of certain hot springs at any time of the year (although he stated that they did not enter the spring water, which has since been shown to be false). Wall was impressed by the altitude at which the snakes were found, which to date is still higher than any other snake known! Wall named the snake Natrix baileyi after Bailey, and in 1953 herpetologist Edmond Malnate moved it into a newly erected genus, Thermophis, meaning "heat snake" in Greek, giving it the name is has today: Thermophis baileyi. In 2008 a second species of Thermophis was discovered which differs slightly in scale characters and body proportions. Peng Guo of Yibin University named it Thermophis zhaoermii for preeminent Chinese herpetologist Zhao Ermi.

Just how remarkable these snakes are was not fully realized until recently. In the past, analyses of evolutionary relationships were limited to comparisons of morphological characteristics (for snakes, early taxonomists primarily relied on features of the scales and of the male reproductive organs, called hemipenes, to inform their hypotheses on how snakes were related to one another). Modern advances in molecular biology have enabled taxonomists to compare genetic sequences of related organisms and discover the intricate branching pattern of the evolutionary tree of life, essentially the family tree of all life on Earth. Although molecular phylogenetics, as this branch of science is called, is not flawless, it can provide incredible insight into the ancestry of species that have no close living relatives and therefore are very unique morphologically, making them difficult to compare with other organisms. Hot-spring Snakes are in this very situation, and although to a non-specialist they look pretty much like any other snake, their evolutionary history remained a mystery until 2009, when a group of biologists led by Zhao Ermi published two papers on the evolutionary origins of Thermophis.

Thermophis baileyi

As it turns out, Hot-spring Snakes are most closely related to South American snakes called xenodontines. Xenodontinae is one of the largest subfamilies of colubrid snakes, with about 90 genera and more than 500 species known. They are primarily tropical snakes previously thought to be restricted to the Americas, and they include several well-known (and many poorly-known) species, among them the South American Hog-nosed Snakes (genus Xenodon). Similarities of hemipenal morphology had hinted at a relationship between these taxa, but who would have guessed that the closest relatives of Hot-spring Snakes lived nearly 10,000 miles away on the tropical other side of the world? Not I, for one.

Thermophis baileyi

Hot-spring Snakes probably diverged from their "nearest" relatives about 28 million years ago. Despite the strengths of molecular phylogenetics, there is still some uncertainty about the position of Thermophis relative to other colubrid snakes because their branch of the tree arises near the base of a major clade (Xenodontinae), meaning that, as suspected, they have no close living relatives. In some phylogenies, Hot-spring Snakes are clustered with the "relict snakes of North America": Carphophis, Contia, Diadophis, Farancia, and Heterodon. Some of my favorite snakes, these are thought to have dispersed from Asia into North America during the Miocene, about 16 million years ago. (Diligent readers will recall that I've told this story before in my post on Rainbow Snakes, although I didn't know then about the involvement of Thermophis.)

Probably the common ancestor of all modern colubrids (Thermophis and NA relicts included) lived in Asia more than 30 million years ago. When the Bering Land Bridge connected North America and Asia, some of these snakes dispersed eastward across it, just like the ancestors of sabre-toothed tigers, woolly mammoths, and even Tyrannosaurus rex¹. These evolved into a North American snake fauna, now largely extinct except for the few aforementioned relicts, and a hugely successful South American snake fauna, which was isolated from North America for a 5 million year period during the late Miocene-early Pliocene when the Isthmus of Panama was submerged by the ocean. One reason for this disparity is that two other groups of colubrid snakes, which are today the dominant colubrids of North America, the colubrines and the natricines, dispersed from Asia to North America around the same time as the xenodontines. Apparently ancestral colubrines and natricines dispersed more slowly than xenodontines, because they didn't reach South America before it separated. Instead, they only moved into South America following the most recent closing of the Isthmus of Panama in the late Pliocene, in an event known as the Great American Biotic Interchange. The GABI was responsible for allowing toads, treefrogs, opossums, armadillos, hummingbirds, and vampire bats to colonize North America, and salamanders, pit vipers, rabbits, squirrels, raccoons, deer, and jaguars (and colubrine and natricine snakes) to colonize South America. Assuming that Thermophis are all that's left of the original Asian proto-xenodontine snake stock, this pattern explains the evolutionary and biogeographic relationships of the Hot-spring Snakes and their relatives. However, given other recent discoveries in Asia, I wouldn't rule out the future discovery of another Asian proto-xenodontine more closely related to Thermophis than to any other known snake.

One reason we know only a little about Thermophis is its high mountain habitat. Most of the mountain ranges in China run east-west, but the Hengduan Mountains, where Hot-spring Snakes are found, stretch north-south (the name "Hengduan" means "to transect" and "cut downward" in Chinese). Parallel north-south sub-ranges of the Hengduans are separated by deep river valleys through which flow the famous Three Parallel Rivers: the Nujiang (Salween), Lantsang (Mekong), and Jinshajiang (Upper Changjiang or Yangtze). Thermophis baileyi is distributed west of the Salween, whereas T. zhaoermii is distributed east of the Changjiang. Geologic uplift of the intervening region of southern Tibet has lasted for about the last 20 million years, about the same age as the divergence between the two extant species of Thermophis. It is hypothesized that refuges in the Kyi Chu/Lhasa and Yarlung Zhangbo valleys during the last glacial maximum probably allowed T. baileyi to persist in the west, alongside such glacial relicts as neo-endemic ground beetles, juniper trees, and even humans. Following the end of the last Ice Age, they dispersed to other hot spring sites, and today connectivity among these sites is maintained when male snakes make rare movements among them, probably facilitated by the rivers and streams that connect the sites. Female snakes are less likely to disperse, because the plateau's short summers necessitate highly seasonal reproduction. Whether Thermophis are oviparous or viviparous is still unknown.

Although the advantages of living around hot springs at high altitudes, where the temperature is relatively cold, are pretty obvious, recent surveys by Ding-qi Rao found that Hot-spring Snakes also live in fields and other areas far from hot springs, suggesting that the species' ecological niche may be wider than previously thought. This is fortunate, both because the growing exploitation of geothermal energy has led to destruction and degradation of hot spring habitats, and because global climate change will likely continue to cause mountaintop habitats around the world to shrink, necessitating a shift upward in elevation by high-altitude species in order to follow their habitat. This problem has been documented for pikas and for birds and will likely affect Hot-spring Snakes too. Because the ability of mountaintop species to disperse across intervening areas to higher mountain ranges is limited, many may go extinct. Will we one day see the top of Mount Everest as the last foothold for Hot-spring Snakes? Let's hope not.

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1 Not all of these dispersal events happened at the same time. Evidence suggests that the Bering Land Bridge has connected North America with Asia several times over the last seventy million years: at least once during the time of the dinosaurs, again about 55 million years ago, another 20-16 mya, and more recently both 35,000 and 22-7,000 years ago. The ancestors of the New World xenodontines probably came across 20-16 million years ago.^↩

ACKNOWLEDGMENTS

Thanks to photographers Kai Wang, Daniel Winkler, Brian McDiarmant, and Gavin Maxwell for use of their photographs.

REFERENCES

Guo, P, Liu S, Feng J, He M (2008) The description of a new species of Thermophis (Serpentes: Colubridae). Sichuan Journal of Zoology 27:321 <link>

Guo, P., S. Y. Liu, S. Huang, M. He, Z. Y. Sun, J. C. Feng, and E. M. Zhao. 2009. Morphological variation in Thermophis Malnate (Serpentes: Colubridae), with an expanded description of T. zhaoermii. Zootaxa 1973:51-60 <link>

He M, Feng J, Zhao E (2010) The complete mitochondrial genome of the Sichuan hot-spring keel-back (Thermophis zhaoermii; Serpentes: Colubridae) and a mitogenomic phylogeny of the snakes. Mitochondrial DNA 21:8-18 <link>

Hofmann S (2012) Population genetic structure and geographic differentiation in the hot spring snake Thermophis baileyi (Serpentes, Colubridae): indications for glacial refuges in southern-central Tibet. Molecular Phylogenetics and Evolution 63:396-406 <link>

Hofmann S, Fritzsche P, Solhøy T, Dorge T, Miehe G (2012) Evidence of sex-biased dispersal in Thermophis baileyi inferred from microsatellite markers. Herpetologica 68:514-522 <link>

Huang S, Liu S, Guo P, Zhang Y, Zhao E (2009) What are the closest relatives of the hot-spring snakes (Colubridae, Thermophis), the relict species endemic to the Tibetan Plateau? Molecular Phylogenetics and Evolution 51:438-446 <link>

Pinou, T., S. Vicario, M. Marschner, and A. Caccone. 2004. Relict snakes of North America and their relationships within Caenophidia, using likelihood-based Bayesian methods on mitochondrial sequences. Molecular Phylogenetics and Evolution 32:563-574 <link>

Sekercioglu, C. H., S. H. Schneider, J. P. Fay, and S. R. Loarie. 2008. Climate change, elevational range shifts, and bird extinctions. Conservation Biology 22:140-150 <link>

Wall, F. 1907. Some new Asian snakes. The Journal of the Bombay Natural History Society 17:612-618 <link>

Spider-tailed Adders

This species was brought to my attention about two years ago by a friend who, like me, was working on completing her Master's thesis at that time. In the post-script of her message, titled 'Probably the coolest thing I've learned in weeks', she wrote "PS I swear this started out as a legitimate search for information for my thesis." In addition to being a welcome distraction from my writing, the story of the Spider-tailed Horned Viper, Pseudocerastes urarachnoides, is, in my opinion, one of the most interesting recent discoveries in herpetology.

The tail in question

The first specimen of P. urarachnoides was collected in 1968 by the Second Street Expedition, mounted on behalf of Chicago's Field Museum of Natural History by a retired businessman and activist couple, William and Janice Street. The primary purpose of the expedition was to collect mammal specimens, but reptiles were also collected, including the first specimen (also known as a type specimen or holotype) of P. urarachnoides. Because only a single specimen was collected, its unusual tail morphology was thought at first to be a solfugid clinging to the tail. Solfugids (also called solpugids, camel spiders, wind scorpions, or sun spiders) are members of the same arthropod class, the Arachnida, as spiders and scorpions, although they are neither spiders nor scorpions. Upon closer examination, the Field Museum's Steven Anderson found that the tail of the snake bore a peculiar structure with an uncanny resemblance to a solfugid that could have been a tumor, congenital defect, or growth caused by a parasite. The snake was identified as Pseudocerastes persicus, the Persian Horned Viper, and entered into the Field Museum collection, where it was almost, but not quite, forgotten.

Egyptian Giant Solfugid (Galeodes arabs)

The story ended there, until 2001, when Hamid Bostanchi collected a second specimen with identical tail morphology to the first. A third specimen was later discovered in the collection of the Poisonous Animal Section of the Razi Institute in Karaj, Iran, in 2008; it had been misidentified as a Desert Horned Viper, Cerastes cerastes. Together with Anderson, who had described the first specimen, and their colleagues Haji Gholi Kami of Gorgan University and Ted Papenfuss of the Berkeley Museum of Vertebrate Zoology, they described the new species in 2006, naming it Pseudocerastes urarachnoides, from the Greek ura (tail), arachno (spider) and ides (similar to). In their paper, Bostanchi et al. described the structure of the tail, which is formed of the last pair of subcaudal scales, much enlarged, and a single enlarged dorsal scale. The elongated components are modified lateral scales. X-rays taken by the team showed that the caudal vertebrae extend well into this structure and are not deformed or modified. Bostanchi et al. also speculated that the function of the modified tail might be to augment caudal luring behavior exhibited by many vipers. By mimicking a solfugid, birds or other would-be solfugid predators could be enticed to approach within the viper's striking distance.

Behavioral observations made in 2008 of a live P. urarachnoides captured in western Iran and maintained in captivity confirm these ideas. Closed-circuit video was used to record behavior, and the results published in the Russian Journal of Herpetology by Behzad Fathinia of Razi University and his colleagues. They observed the snake, a juvenile male that regurgitated a Crested Lark, using its caudal lure to attract sparrows and baby chickens that they introduced into its enclosure. When the birds approached and pecked the tail, the snake struck and envenomated the birds, a process taking less than one half second. A bird was also found in the stomach of the paratype specimen, further evidence that this species might feed heavily on birds in the wild with the aid of its spectacular caudal lure. The tail of P. urarachnoides probably represents the most elaborate morphological caudal ornamentation known in any snake, with the possible exception of the sound-producing rattles of rattlesnakes.

Within its restricted range in the mountainous terrain of western Iran, P. urarachnoides inhabits rock crevices in the gypsum formations that comprise its hilly, arid habitat. Adaptations of the genus Pseudocerastes to desert life include supralabials (upper lip scales) with a serrated lower margin and a groove to accommodate the lower lip, which provide complete closure of the mouth and prevent sand from entering. The nostrils also have a valvular prominence to the same effect. The other two species of Pseudocerastes, P. persicus and P. fieldi, share these characteristics. These two species are sometimes combined, although differences in venom chemistry and scalation, along with the fact that their ranges are separated by the Zagros Mountains, suggest that they are probably distinct species (and they are certainly distinct morphologically from P. urarachnoides). Both overlap in range with P. urarachnoides in places.

P. urarachnoides

Two other recent and noteworthy discoveries of Old World pitvipers are worth a mention. One, Protobothrops mangshanensis, is a large and beautiful pitviper discovered in 1990 in mountainous regions in southern Hunan and reputed to be the only non-cobra capable of spitting venom. The other, Atheris matildae, discovered in 2011, is a member of an especially popular genus in the pet trade (although this could be said of many of the most beautiful vipers). The exact type locality of A. matildae, in the southern highlands of Tanzania, was concealed in order to limit collection for the pet trade. In addition, a novel strategy is being tested: A. matildae is being bred at a facility in Tanzania and the first few dozen offspring are being given away to collectors in order to reduce the market for illegally collected specimens. Whether this strategy will succeed remains to be seen, but hopefully A. matildae can be saved from the same sad fate as the Lao Newt, Roti Island Snake-necked Turtle, Chinese Leopard Gecko, coelacanth, and other species that have been overcollected almost as soon as they were described.

Atheris matildae

Protobothrops mangshanensis

Check out another amazing new snake discovery at Greg Laden's blog: once thought to be a single deadly sea snake, Enhyrina schistosa is actually two!

ACKNOWLEDGMENTS

Thanks to Heather Heinz for bringing P. urarachnoides to my attention, and to photographers and videographers Michael Kern, Behzad Fathinia, Michael & Patricia Fogden, Omid Mozaffari, and Alireza Shahrdari.

REFERENCES

Bostanchi H, Anderson SC, Kami HG, Papenfuss TJ (2006) A new species of Pseudocerastes with elaborate tail ornamentation from western Iran (Squamata: Viperidae). Proceedings of the California Academy of Sciences 57:443-450 <link>

David P, Tong H (1997) Translations of recent descriptions of Chinese pitvipers of the Trimeresurus-complex (Serpentes, Viperidae), with a key to the complex in China and adjacent areas. Smithsonian Herpetological Information Service 112:1-31 <link>

Fathinia B, Anderson SC, Rastegar-Pouyani N, Jahani H, Mohamadi H (2009) Notes on the natural history of Pseudocerastes urarachnoides (Squamata: Viperidae). Russian Journal of Herpetology 16:134-138 <link>

Fathinia B, Rastegar-Pouyani N (2010) On the Species of Pseudocerastes (Ophidia: Viperidae) in Iran. Russian Journal of Herpetology 17:275-279 <link>

Menegon M, Davenport T, Howell K (2011) Description of a new and critically endangered species of Atheris (Serpentes: Viperidae) from the Southern Highlands of Tanzania, with an overview of the country’s tree viper fauna. Zootaxa 3120:43-54 <link>

Stuart BL, Rhodin AGJ, Grismer LL, Hansel T (2006) Scientific description can imperil species. Science 312:1137 <link>

Fea's Pitless Pitvipers

Leonardo Fea

Late one spring night in 1887 in the Kakhyen Hills of Burma, 35-year-old Italian explorer Leonardo Fea crested a karst outcrop and entered a bamboo thicket. He barely noticed the rain, because before him lay a two-foot long snake of indescribable beauty. It was shiny, dark purplish-black and marked with thin, widely-spaced neon orange bands so bright they almost  looked white. The head bore a striking symmetrical pattern of orange, gold, and black. When Fea picked the snake up, he saw that it had a plain purple belly. It appeared to be a harmless colubrid, and luckily for Fea, he wasn't bitten, so he had no opportunity to find out that it wasn't.

Fea was among the many European explorers and natural historians who were pouring into the newly-annexed nation of Burma, whose cultural roots date back to the 2nd century BCE. He collected thousands of vertebrates there for the Genoa Civic Museum, but perhaps none so unique or amazing as that snake. When Belgian-British herpetologist George Boulenger received a loan of Fea's reptiles from the museum, he declared of the single specimen "I may well say that Azemiops is the most interesting ophiological discovery made since that of Dinodipsas [Causus]¹". Boulenger described it as a new genus and species in his 1888 report on Fea's expedition, writing "it affords me great pleasure to connect with [this snake] the name of the courageous and highly successful explorer to whom science is indebted for this and so many other additions." Azemiops feae was the first species named for Fea, who was soon to also receive the honors of an eponymous petrel, tree rat, and muntjac, collected with his "untiring zeal" in southeast Asia and the Cape Verde islands.

Azemiops feae. Notice the enlarged head scales
and the absence of a heat-sensing facial pit.

The enigmatic “pitless pitviper,” Azemiops feae or Fea's Viper looks almost nothing like other vipers, with its elliptical head, enlarged head scales, and smooth dorsal scales. In fact, it is so unusual that at times it has been classified as an elapid or a colubrid instead, of which its enlarged head scales in particular are reminiscent. Morphological and molecular evidence point to an ancient relationship between Fea's viper and other old world vipers ("viperines"), which last shared a common ancestor over 56 million years ago. Rather, Fea's viper is more closely related to the crotaline vipers, or "pit vipers", a predominantly New World clade that includes rattlesnakes, copperheads, and bushmasters (although even from these it is distinct, having diverged over 32 million years ago). Although there are a few other Asian crotalines, such as Hypnale and Trimeresurus, even these are more closely related to their New World counterparts than they are to Fea's viper, all sharing an infrared-sensitive facial pit. Indeed, Azemiops occupies a lonely branch of the snake family tree.

We know a little of the natural history of Fea's viper. It is found primarily in karst systems in the tropical uplands of northern Burma, northern Vietnam, and south-central China. Adults are active predominantly during cool, rainy summer nights, when they move slowly through deep leaf-litter in bamboo and tree fern thickets interspersed with well-lit clearings. They spend much of their lives in the holes and crevices of karst outcrops and in open and underground streams. Juveniles are most active on cool, wet fall nights. Like other vipers, Fea's viper hibernates in winter, so presumably they are fairly predictable in space and time when entering and leaving their hibernacula. Only a few prey items have been recorded, all of which have been rodents and shrews abundant in karst outcrops associated with swift mountain streams, although these snakes will also eat geckos in captivity.

This specimen's head shows more than the usual amount
of white. In preservative, the head turns completely white,
causing some to call them "White-headed Vipers".

Fea's vipers are rare and difficult to keep in captivity. In 1986, the price list for Scales & Tails Trading Company in Hong Kong offered five Azemiops feae as "White Head Vipers" for $300 a piece, the most expensive item on the list. Observations of captive individuals indicate that these snakes do not tolerate dry conditions, and develop skin problems when maintained at less than 100% humidity. Ideal temperatures are between 60 and 68°F, surprisingly cool for a reptile (but a little warmer than those preferred by Rubber Boas). In the words of one reptile keeper, they are "so boring & difficult to keep" that he sent his off to a zoo. If widely held, this sentiment may actually bode well for Fea's vipers if it renders them unlikely to become overcollected for the pet trade, especially if the low demand can be met by captive breeding. Mating behavior involves courtship of females by males and is similar to that of other vipers in most respects. Fea's vipers lay small clutches of eggs, a characteristic they share with most viperines but not their closer relatives, the crotalines.

Plate from Boulenger's 1888 Account of the Reptilia obtained in Burma,
north of Tenasserim, by M. L. Fea, of the Genova Civic Museum

Skull of a Fea's Viper, showing the solenoglyphous fang,
the definitive viper characteristic.

How dangerous are Fea's vipers? Few bites have been reported, but these are described as "mild", causing few serious consequences. There are similarities between Fea's viper venom and that of viperines, especially Wagler's Temple Viper, except that Azemiops venom has no blood clotting, hemorrhagic, or muscle-destroying activity. The venom gland itself is similar to a viperine's, but Fea's viper fangs possess a ridge at the tip and a blade on the back seen only in some opisthoglyphous and atractaspid snakes. One venom component, dubbed azemiopsin, has been identified as a potential model in neurotransmitter research, adding to the pharmacopoeia of medicinally-useful compounds found in snake venom. Although discovered 125 years ago, Fea's viper has much still to teach us about evolution, neurology, and much else. Let us hope we can learn from it.

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1 The genus Causus consists of six species of viper from sub-Saharan Africa commonly known as night adders. Night adders were once considered the most primitive vipers due to their round pupils and enlarged head scales, which is why Boulenger found them remarkable. They are oviparous and are now known to be more closely related to viperines than to Azemiops and crotaline vipers. Look out for an article on them up here one day!^↩

ACKNOWLEDGMENTS

Thanks to Gernot Vogel, David Nixon, and Michael and Patricia Fogden for use of their photographs.

REFERENCES

Andreone, F. 2000. Herpetological observations on Cape Verde: a tribute to the Italian naturalist Leonardo Fea, with complimentary notes on Macroscincus coctei (Duméril & Bibron, 1839) (Squamata: Scincidae). Herpetozoa 13:15-26

Boulenger, G. A. 1888. An account of the Reptilia obtained in Burma, north of Tenasserim, by M. L. Fea, of the Genova Civic Museum. Annali del museo civico di storia naturale di Genova, Seria 2 6:593-604

Kardong, K. V. 1986. Observations on live Azemiops feae, Fea's Viper. Herpetological Review 17:81-82

Liem, K., H. Marx, and G. B. Rabb. 1971. The viperid snake Azemiops: its comparative cephalic anatomy and phylogenetic position in relation to Viperinae and Crotalinae. Fieldiana: Zoology 34:189-196

Mebs, D., U. Kuch, and J. Meier. 1994. Studies on venom and venom apparatus of Fea's viper Azemiops feae. Toxicon 32:1275-1278 <link>

Orlov N, Ananjeva N, Khalikov R (2002) Natural history of pitvipers in eastern and southeastern Asia. In: Schuett GW, Höggren M, Douglas ME, Greene HW (eds) Biology of the Vipers. Eagle Mountain Publishers, Eagle Mountain, UT, pp 345-360 <link>

Utkin, Y. N., C. Weise, I. E. Kasheverov, T. V. Andreeva, E. V. Kryukova, M. N. Zhmak, V. G. Starkov, N. A. Hoang, D. Bertrand, J. Ramerstorfer, W. Sieghart, A. J. Thompson, S. C. R. Lummis, and V. I. Tsetlin. 2012. Azemiopsin from Azemiops feae viper venom, a novel polypeptide ligand of nicotinic acetylcholine receptor. Journal of Biological Chemistry 287:27079-27086 <link>

Wüster, W., L. Peppin, C. Pook, and D. Walker. 2008. A nesting of vipers: Phylogeny and historical biogeography of the Viperidae (Squamata: Serpentes). Molecular Phylogenetics and Evolution 49:445-459 <link>

Zhao, E.-M. and G. Zhao. 1981. Notes on Fea's Viper (Azemiops feae Boulenger) from China. Acta Herpetologica Sinica 5:66-71

Non-toxic venoms?

This article is part of a series highlighting new research in snake biology presented by herpetologists at the World Congress of Herpetology VII in Vancouver, British Columbia. If you want to learn more about the WCH, check out the June 2012 issue of Herpetological Review, or follow the Twitter hashtag #wch2012, with which I will tag all posts in this series.

A while back we heard about reasons why rattlesnakes frequently miss strikes at their squirrel prey. When they do hit their target, however, the prey tend to run off a little ways before kicking the bucket. This is because, although snake venoms are quick-acting, they mostly do not incapacitate immediately (although there are some sea snake venoms that are very, very quick). As a result, snakes that hunt using venom must be able to track down their prey after it has been bitten. This necessity has led Anthony Saviola, Steve Mackessy, and their colleagues at the University of Northern Colorado to an answer for a question that snake biologists have been asking for a long time: why do snake venoms contain molecules that are non-toxic?

Venom is a complex mixture of over one hundred proteins, peptides, enzymes, and small organic and inorganic molecules, many of which are toxic. It is essentially very strong saliva, capable of both breaking down food and chemically incapacitating or killing it. The evolution of venom has allowed many species of advanced snakes to utilize chemical rather than mechanical means of dispatching prey, which helps them avoid retaliation from sharp teeth and claws. Yet a few venom components serve neither to digest nor to kill prey. What on earth is their function?

Timber Rattlesnake, Crotalus horridus

Observations back to the 1960s suggest that rattlesnakes prefer the scent of envenomated mice over non-envenomated ones. When a rattlesnake strikes a prey item, a stereotypic behavior known as strike-induced chemosensory searching (SICS) is induced. This behavior is a fixed-action pattern that involves tongue-flicking to collect chemical information and a stereotyped searching movement pattern that allows the snake to determine which of the many chemical trails in its vicinity should be followed to find the envenomated prey.

To what chemical cues are rattlesnakes responding when they perform SICS? Mackessy separated Western Diamondback Rattlesnake (Crotalus atrox) venom into distinct fractions, each containing molecules of different sizes. This is accomplished by exploiting differences in the weight of each molecule, using techniques that allow different molecules to travel different distances through a gel medium based on how heavy they are. In the same amount of time, smaller, lighter molecules travel farther than larger, heavier ones. When Mackessy injected mice with the fractions containing the larger exonucleases, metalloproteinases, and phospholipases (classes of enzymes that break down, respectively, DNA, proteins, and fatty acids - so, the venom components that are active in digestion and incapacitation), the snakes showed little interest. Together, these well-known active compounds comprise about 85% of the total venom by mass, and they are responsible for all of the venom's digestive and killing activity, so it's a little surprising that snakes should show no interest in mice injected with them.

Structure of disintegrin heterodimer from Echis carinatus

However, when Mackessy injected mice with a venom fraction containing smaller molecules, called crotatroxin disintegrins, not known to have any enzymatic or toxic activity, the snakes behaved as they normally would have when scent-trailing mice injected with whole venom. Although disintegrins make up less than 10% of the venom by mass, they are clearly critical for the snake to find its prey following envenomation. What's more, the disintegrins alone don't induce trail-following behavior in snakes; rather, it is the product of the interaction of the disintegrins with the dead prey tissue that causes snakes to follow their trail.

Crotalus oreganus lutosus

Disintegrins are abundant in the venoms of most Western Rattlesnakes (Crotalus viridis sensu lato)¹, and are also found in other rattlesnakes, in Copperheads (Agkistrodon contortrix) and other snakes of the genus Agkistrodon (where they may be undergoing rapid evolution), and in most adult vipers. However, in juvenile rattlesnakes, and in many elapid snakes (cobras, coralsnakes, and other proteroglyphous snakes) disintegrins are present only at low levels or are absent entirely. Why should this be? One possible explanation is that elapids and juvenile vipers are more likely to hold onto their prey following a strike, so they don't need a chemical tracer to follow it because it doesn't usually get that far away. Some elapids do have disintegrins, however, and there is evidence that disintegrins in vipers also function to inhibit blood coagulation. In fact, a disintegrin molecule from Copperhead venom has been shown to slow the spread of breast and ovarian cancer in mice, so there could be much more to this story. One thing is sure: the Mackessy lab is one to watch if you're interested in snake venoms, and this won't be my last post on their fascinating research.

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1 Many of the nine previously recognized subspecies of the Western Rattlesnake (Crotalus viridis sensu lato) occur in the southwestern United States, and the complex has been subject to several molecular studies to reevaluate the taxonomic status of these subspecies. The consensus opinion largely follows Ashton and de Queiroz (2001), which recognized two species: C. viridis (Prairie Rattlesnake, two subspecies) and C. oreganus (Western Rattlesnake, six subspecies). This is the only species of rattlesnake that occurs where I live, in northeastern Utah.^↩

ACKNOWLEDGMENTS

Thanks to Todd Pierson for his photograph and to Steve Mackessy and Anthony Saviola for their coordination on this article, which was delayed in its release to coincide with the publication of their paper in BMC Biology.

REFERENCES

Ashton KG, de Queiroz A (2001) Molecular systematics of the western rattlesnake, Crotalus viridis (Viperidae), with comments on the utility of the D-loop in phylogenetic studies of snakes. Molecular Phylogenetics and Evolution 21:176-189. <link>

Calvete J, Sanz L, Juárez P, Mackessy S (2009) Snake venomics and disintegrins: portrait and evolution of a family of snake venom integrin antagonists. In: Mackessy S (ed) Handbook of Venoms and Toxins of Reptiles. CRC Press, Boca Raton, Florida, pp 337-357

Finn R (2001). Snake Venom Protein Paralyzes Cancer Cells. Journal of the National Cancer Institute 93:261-262 <link>

Furry K, Swain T, Chiszar D (1991) Strike-induced chemosensory searching and trail following by prairie rattlesnakes (Crotalus viridis) preying upon deer mice (Peromyscus maniculatus): chemical discrimination among individual mice. Herpetologica 47:69-78. <link>

Mackessy SP, Tu AT (1993) Biology of the sea snakes and biochemistry of their venoms. In: Tu AT (ed) Toxin-related Diseases: Poisons Originating from Plants, Animals and Spoilage. Oxford & IBH Publishing Co., New Delhi, pp 305-351 
<link>

Saviola AJ, Chiszar D, Busch C, Mackessy SP. 2013. Molecular basis for prey relocation in viperid snakes. BMC Biology 11 <link>

Soto JG et al. (2006) Genetic variation of a disintegrin gene found in the American copperhead snake (Agkistrodon contortrix). Gene 373:1-7. <link>

Screech Owls and Blindsnakes: An Unlikely Mutualism

Adult Eastern Screech Owl at a nest box

In the 1970s and 80s, a pair of biologists at Baylor University in Waco, Texas, Fred Gehlbach and Robert Baldridge, were studying screech owl nesting ecology. These small owls nest in tree cavities and eat a variety of small animals, from insects to mice. Like most raptorial birds, Eastern Screech Owls usually kill their prey before bringing it home to feed to their nestlings. Gehlbach and Baldridge observed some of the screech owls in their study carrying live Texas Blindsnakes (Rena [formerly Leptotyphlops] dulcis) to their nests in experimental nest boxes like those used by wood ducks and bluebirds (pictured at right). When they checked the nests the next day, they found, to their surprise, between one and fifteen live blindsnakes living among the owl chicks in fourteen different nests! In some cases, the snakes lived with the baby owls for at least a week! Many of the blindsnakes bore scars from adult owl beaks, but few had been killed.

If you're not familiar with blindsnakes (aka scolecophidians), don't worry; few people are. There are about 400 species of these 'seriously strange serpents', as Darren Naish calls them over at TetZoo, distributed chiefly in the world's tropical regions (the Texas Blindsnake is one of the few temperate exceptions). Most have small eyes (or none at all, as their name suggests), smooth round scales, and eat invertebrates. Their jaw architecture is entirely unique: their jaws act like little scoops to effectively shovel ant and termite larvae and pupae into their mouths. Check out the video from BBC's Life in Cold Blood below, or visit the homepage of blindsnake biologist Nate Kley at Stony Brook University.

Almost as cute as baby snakes

How does this help baby screech owls? Gehlbach and Baldridge wanted to find out, so they measured the diversity and abundance of invertebrates in the owl nests with and without live blindsnakes, as well as the health and survival of the baby owls (which they were already measuring). They found that nests with blindsnakes had significantly fewer mites, insects, and arachnids, and that baby owls from these nests were 25% more likely to survive and grew as much as 50% faster; in other words, the presence of the blindsnakes improved the health of the baby owls and the fitness of the adults. The effects were more pronounced for the youngest owl babies, which hatch as many as six days later than their oldest sibling. As the nail in the coffin, Gehlbach and Baldridge tested whether or not the blindsnakes actually ate the invertebrates they found in the owl nests, and sure enough, they chowed down on the soft-bodied fly larvae that kill baby owls in nearly 30% of nests.

Texas Blindsnake (Rena dulcis)

They also noticed that blindsnakes were more likely to be found in nests after it rained, probably because the mother owls had an easier time of finding the blindsnakes when they were crawling around on the surface, which many fossorial snakes tend to do when rainwater fills their burrows. Gehlbach and Baldridge also found that blindsnakes could only survive about two weeks in owl nest boxes that did not contain baby owls, suggesting that they were dependent on insect larvae that entered the nest inside food brought by the mother owl. These snakes can climb trees, so presumably it isn't too challenging for them to climb down out of a nest box after it is vacated by owls; one gravid female blindsnake was found in a nest box, so it is possible that they lay their eggs there before leaving. Some nests contained dead blindsnakes, which Gehlbach and Baldridge hypothesized had been eaten by the baby owls after their food supply had run out. In feeding experiments, baby screech owls readily consumed dead blindsnakes as well as other snakes of similar size, such as Rough Earthsnakes (Virginia striatula).

Skull architecture of Rena dulcis

The skulls of blindsnakes are just amazing, and it's thanks to the research efforts of blindsnake anatomist Nate Kley of Stony Brook University that we know so much about them. Kley has characterized the feeding behavior of two families of blindsnakes, the Leptotyphlopidae, which use  scooping motions of the lower jaw known as mandibular raking, and the Typhlopidae, which use similar motions of the upper jaws, called maxillary raking. It's remarkable how similar the two strategies are given that the snakes are using entirely different parts of their bodies to employ them and that they are separated by about 110 million years of evolution. High-resolution CT scans of the skill of Rena dulcis are also available from the good people at UT Austin's DigiMorph project. The jaws (upper in typhlopids, lower in leptotyphlopids) move about independently of the skull to a remarkable degree. You can get a really good idea of that motion by watching videos of leptotyphlopids here, here, and here, and of typhlopids here and here. As soon as they're in the mouth, those larvae are goners! These snakes are unlike all others in that they eat  huge numbers of prey items very quickly, thanks to their unique jaw architecture. One Blackish Blindsnake (Austrotyphlops nigrescens) from Australia was recorded to have eaten over 1,431 ant larvae/pupae in one sitting! Some blindsnakes have cloacal secretions that aid in repelling attacking ants or chemically camouflaging the blindsnakes, which live inside ant mounds. The list of amazing attributes goes on and on - and there is much more for scientists to find out!

ACKNOWLEDGMENTS

Thanks to Count_Strad, Toby Hibbits, Gary Nafis, and Nate Kley for use of their photos and figures.

REFERENCES

Gehlbach, F. and R. Baldridge. 1987. Live blind snakes (Leptotyphlops dulcis) in eastern screech owl (Otus asio) nests: a novel commensalism. Oecologia 71:560-563. <link>

Kley, N. J. 2001. Prey transport mechanisms in blindsnakes and the evolution of unilateral feeding systems in snakes. American Zoologist 41:1321-1337. <link>

Malagasy Leaf-nosed Snakes

Langaha madagascarensis male

Madagascar has been called the "eighth continent" as a result of its large size, unique habitats, and high faunal and floral (not to mention cultural and linguistic) endemism. Of the ninety-six species of snakes inhabiting the island, only two are found anywhere else: one is a sea snake (the widespread Pelamis platura) and the other is a ubiquitous introduced species (the parthenogenetic blindsnake Ramphotyphlops braminus). Most of the rest belong to the subfamily Pseudoxyrhophiinae, and each deserves its own article. But one has to start somewhere, and perhaps the best place to start is with one of the most unique Malagasy snakes, and one of my favorites: Langaha madagascarensis, the Malagasy Leaf-nosed Snake.

Langaha madagascarensis female

Langaha is so unique that it has been placed in its own genus ever since it was described, and was one of only eight¹ genera recognized in Bonnaterre's 1790 Ophiologie, a book that covered 224 species of snake. That's right: at a time when snakes as different as wormsnakes, saw-scaled vipers, sea snakes, and blunt-headed tree snakes were being grouped together as "typical snakes" in the genus Coluber, Langaha was considered unusual enough to justify its own genus! Today there are three recognized species of Langaha, but the most is known about L. madagascarensis.

Left: Captive juvenile Langaha madagascarensis exhibiting hanging behavior; photo from Krysko 2003
Right: Seed pods of the Ophiocolea floribunda, a Malagasy legume whose genus is Greek for 'hollow snake'

As their name implies, Leaf-nosed Snakes have bizarre nasal appendages. What's more, these structures are sexually dimorphic to a degree unusual among snakes. Female Leaf-nosed Snakes have a more elaborate, serrated nasal appendage, whereas males bear a longer, pointier one. These structures are present at birth, suggesting that they have some function beyond sexual signaling between rival males or potential mates. Often, these snakes are seen hanging from branches with their heads pointing towards the ground - perhaps the structures serve to drain water off the snake? Several Malagasy plants, including some legumes and bignonias, have long pointed seed pods that hang down from the plant, providing possible models that the snake may imitate with its posture and nasal appendage. No one knows for certain.

Male (right) and female
(left) L. madagascarensis 

This is a timely post in that it comes on the heels of newly published research on Malagasy Leaf-nosed Snakes. An article by recent Cornell University graduate Jessica Tingle has just appeared in the journal Herpetological Conservation and Biology documenting novel aspects of the behavioral ecology of this unusual snake. Everything known about the behavior of Langaha to date has been learned from observing captive individuals. Tingle's paper presents the first data collected on the behavior of Langaha in the wild. She observed several of these snakes foraging for and eating lizards, although one sentence in her paper stands out to me as typical of snake behavior studies: "The vast majority of their time (90%) was spent not moving at all." Although this sounds boring, it provides evidence that these snakes are primarily ambush predators, rather than active foragers (although Tingle did observe one Langaha chasing skinks on the ground). Spending months in Madagascar, Tingle was able to observe only a few snakes, and much remains to be learned about their natural history and ecology.

Plate showing a male Langaha madagascarensis from Bonnaterre's 1790 Ophiologie

From observations made on Langaha in captivity by Kenney Krysko of the Florida Museum of Natural Sciences, we know that Leaf-nosed Snakes lay eggs. When they hatch, the nasal appendages of juveniles are folded up so that their egg tooth can be used to break out of the egg. The appendage gains its normal shape after 36 hours. Juveniles exhibit the same vertical 'hanging' behavior as adults, which Krysko also suggests helps them mimic the seed pods of Malagasy plants (and perhaps deter predation, though by what predator is unclear).

Hatchling Langaha madagascarensis, from Krysko 2003

The other two species of Langaha are very poorly known. In Darren's TetZoo article, he states that only female Langaha alluaudi have nasal appendages, but I have been unable to find another source corroborating this fact, although I did find a photo on Flickr purported to be a male L. alluaudi (it looks similar to a male L. madagascarensis, also sometimes called L. nasuta, to me). Female L. alluaudi have longer, straighter nasal appendages than L. madagascarensis, and female L. pseudoalluaudi have shorter, more upturned ones (no word on what male L. pseudoalluaudi might look like). Why these differences? Perhaps differences in microhabitat or sexual preference are the cause. Who can say?

Female (left) and male(?, right) Langaha alluaudi

Female L. pseudoalluaudi

Although Madagascar is unique, it is similar to the rest of the world in at least one sad way: its natural places are disappearing quickly. Most of its forests have already been logged or converted to slash and burn agriculture, and what little remains is dwindling daily. If more effective conservation measures are not taken,  including supporting the human communities that depend on the rich natural resources of this hottest of biodiversity hotspots, we may never find out what Langaha's nose is for.

Male L. madagascarensis consuming Chalarodon madagascariensis
Photo from Herp. Con. Bio. gallery for Tingle 2012

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1 Three of these eight genera turned out not to be snakes at all: the limbless lizards Anguis and Amphisbaena, and  the limbless amphibian Caecilia.↩

ACKNOWLEDGMENTS

Thanks to Dick Bartlett, Jessica Tingle, David d'O, Bernard Dupont, Russell Speight, and G.E. Schatz for use of their photos.

REFERENCES

Bonnaterre PJ (1790) Ophiologie, in Tableau encyclopédique et méthodique des trois règnes de la nature. Panconoke, Paris <link>

Krysko KL (2003) Reproduction in the Madagascar leaf-nosed snake, Langaha madagascariensis (Serpentes: Colubridae: Pseudoxyrhophiinae). African Journal of Herpetology 52:61-68 <link>

Krysko KL (2005) Feeding behaviour of the Madagascar leaf-nosed snake, Langaha madagascariensis (Serpentes: Colubridae: Pseudoxyrhophiinae), with an alternative hypothesis for its bizarre head structure. African Journal of Herpetology 54:195-200 <link>

Tingle JL (2012) Field observations on the behavioral ecology of the Madagascan Leaf-nosed Snake, Langaha madagascariensis. Herpetological Conservation and Biology 7:442-448 <link>