Fea's Pitless Pitvipers

Click here to read this post in Spanish!

Haga clic aquí para leer este blog en español!

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.

---

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

Fry BG, Wuster W, Ryan Ramjan SF, Jackson T, Martelli P, Kini RM, 2003. Analysis of Colubroidea snake venoms by liquid chromatography with mass spectrometry: evolutionary and toxinological implications. Rapid Commun Mass Spectrom 17:2047-2062 <link>

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

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

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.

---

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>

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

Screech Owls and Blindsnakes: An Unlikely Mutualism

Click here to read this post in Spanish!

Haga clic aquí para leer este blog en español!

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>

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

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

---

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>

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

Africa's Giant Gaboon Vipers

For as long as I can remember, I've been impressed by Gaboon Vipers (Bitis gabonica). These western African behemoths can reach 5 3/4 feet in length and over 14.5 inches in girth, and weigh up to 25 pounds with an empty stomach. They are the heaviest vipers and possess the longest fangs, up to one and a half inches in length! Furthermore, their geometric dorsal pattern, as intricate as it is beautiful, is ideally suited to camouflaging them against the leafy forest floor, where they lie in wait for their endothermic prey: birds, rodents, rabbits, monkeys, small antelope, porcupines.

A Gaboon Viper, beautifully camouflaged

Like many vipers, Gaboon Vipers are ambush predators, a lifestyle to which they are supremely adapted. Long folding fangs and deadly venom allow them to kill their prey while keeping a safe distance from it. A very low metabolism permits them to wait in one spot for weeks, until the perfect opportunity presents itself. They spend between three-quarters and 95% of their time just sitting quietly, sometimes for up to three months at a time. Every so often, a viper, particularly a male during the breeding season of March through May, will embark on a long-distance movement of one quarter to two thirds of a mile, sometimes in a single day.¹ The preferred habitat of Gaboon Vipers is a mosaic of forest, thicket, and grassland, although they will sometimes enter sugarcane fields and rural gardens. As with most snakes, life as a Gaboon Viper is probably pretty dull.

The impressive fangs of a Gaboon Viper

In spite of its impressive size, or perhaps because of it, Gaboon Vipers are, like many of their kin, docile and retiring. "On two occasions, I accidentally stepped directly on B. gabonica during the course of radiotracking, only becoming aware of this after feeling squirming movement beneath my foot. At no point during either encounter did the snake hiss or show aggression in any manner", writes Jonathan Warner in his dissertation, which also contains evidence that hippos, elephants, and leopards may walk right by Gaboon Vipers without noticing them. Being stepped on and squashed by these large herbivores might be the primary cause of mortality for adult vipers, which are not vulnerable to many natural predators.

You can see why

Although Gaboon Vipers produce prodigious amounts of venom (nearly 10 mL), the toxicity is rather low compared to other venomous snakes, and there are only a few detailed clinical reports of bites. They are undoubtedly dangerous snakes, but envenomations are few compared to such infamous species as the Russell's Viper. Like most snakes, particularly slow-moving ones with good camouflage, Gaboon Vipers usually sit still and remain unnoticed whenever a human comes nearby (so in other words, pretty much the exact same thing they were already doing).

Gaboon Viper plate from Duméril, Bibron, & Duméril's Erpétologie Générale;
unfortunately, this is one of the only plates not in color

Like most vipers, female Gaboon Vipers give birth to a litter of live young once every two to three years, usually between 20 and 40. Females do not eat while pregnant. Little is known about their reproductive behavior, but males combat one another over females, which must be an impressive sight. Much recent research on Gaboon Vipers has taken place in South Africa, where they are known as Gaboon Adders. In the southernmost populations, which are disjunct from the main range of the species, the climate is subtropical and seasonal differences in activity are observed, but radiotelemetry studies conducted in tropical areas of Cameroon and Nigeria show no seasonal changes in behavior.²

East African Gaboon Viper (B. g. gabonica)

What's the thing on their nose for? It is much larger in the West African subspecies than in the East African one. Hypotheses range from enhancing crypsis to doing nothing at all. Darren Naish at Tetrapod Zoology has addressed this question, but it seems he met with about the same amount of success as I did in finding a compelling, well-supported reason why these snakes have horns. I couldn't find any studies that examined whether the horns had a sensory function, although it certainly seems possible.

West African Gaboon Viper (B. g. rhinoceros)

I learned something new about these vipers recently. It seems that, among other heavy-bodied snakes, they have evolved the ability to retain their feces for incredibly long periods of time - months to years, after which time 5-20% of the body weight of a single snake may be feces. While this would kill a human, retained fecal material may be functioning as metabolically inert ballast in these species, which require a stationary inertial base for striking. Available data suggest that enhanced uptake of water and nutrients can also be achieved in snakes retaining feces - the poisonous urates (read: pee) are excreted more frequently. Amazing.

---

1 One exception is that these snakes always move following shedding, which occurs about twice a year, perhaps to distance themselves from potential predators attracted by the sloughed material or to avoid external parasites in the old skin that could reattach to the snake.^↩

---

2 Snake biologists in Africa face challenges unfamiliar to we North Americans: "In several instances, I had to abort tracking efforts due to B. gabonica locations in close proximity to potentially dangerous game; namely [Water Buffalo, Rhinoceros, Elephant, Hippopotamus, and Crocodile]", writes Jonathan Warner in his dissertation.^↩

ACKNOWLEDGMENTS

Thanks to Tim Vickers, Wolfgang Wuster, Ivica, Markus Oulehla, and Jonathan Warner for their photos.

REFERENCES

Lillywhite HB, de Delva P, Noonan BP (2002) Patterns of gut passage time and chronic retention of fecal mass in viperid snakes. In: Schuett GW, Höggren M, Douglas ME, Greene HW (eds) Biology of the Vipers. Eagle Mountain Publishers, Eagle Mountain, UT, pp 497-506

Linn I, Perrin M, Bodbijl T (2006) Movements and home range of the gaboon adder, Bitis gabonica gabonica, in Zululand, South Africa. Afr Zool 41:252-265

Luiselli L (2006) Site occupancy and density of sympatric Gaboon viper (Bitis gabonica) and nose-horned viper (Bitis nasicornis). J Trop Ecol 22:555-564

Marsh NA, Whaler BC (1984) The Gaboon Viper (Bitis gabonica): Its biology, venom components and toxinology. Toxicon 22:669-694

Warner JK (2009) Conservation Biology of the Gaboon Adder (Bitis gabonica) in South Africa. PhD dissertation, School of Animal, Plant, and Environmental Sciences, University of the Witwatersrand, Johannesburg, South Africa.

This Gaboon Viper quilt was made for me by
my mother on my 21st birthday.
The geometric pattern lends itself perfectly
to quilting.

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

Galápagos Racers

For answers to your questions about the Galápagos Racer/Marine Iguana chase scene from Planet Earth II, click here!

Sadly, snakes are inactive this time of year in northern Utah. With lower-than-average temperatures dipping below 0° F every night, I've had a lot of time indoors to read and daydream about snakier times and places. You can imagine my envy of my colleagues Susannah French, Nick Kiriazis, and Lori Neuman-Lee, who are currently in the Galápagos Islands studying Marine Iguanas. Nick, a student teacher at South Cache Middle School in Hyrum, Utah, is blogging about their research experiences at his blog, The Learning Scientist, which you should check out. Before they left, I instructed them that they were not to pass up an opportunity to observe the endemic racers of the Galápagos, the only snakes to inhabit the famous archipelago (other than one sea snake species, found offshore).

Galapagos Snake from Bartholome Island

Before I began the research for this article, I was under the impression that there was only a single species of Galápagos Racer. But speciation is quick to act in the birthplace of research on evolutionary principles, and in fact there are five species, each inhabiting different groups of islands. This isn't too surprising. As with most organisms inhabiting the Galápagos (and archipelagos in general), new species evolve on different islands over a relatively short period of time. Archipelagos are natural classrooms for evolutionary biologists, each island differing slightly in a number of qualities: size, rainfall, elevation, isolation. These differing characteristics, combined with long periods of reproductive isolation from populations on other islands, result in the evolution of endemic species to each island or group of closely spaced islands. Many groups of organisms have colonized the volcanic Galápagos from South America since the islands rose from beneath the sea some 8 million years ago. In that time, many of the plants and animals have diversified and speciated, leaving behind a pattern of relationships so telling that the idea of evolution by natural selection was formulated based on observations Charles Darwin made of the islands' fauna (for a recap, follow the link above to see a video to which my friend Rosemary Mosco contributed artwork).

Galapagos Snake eating a lava lizard (Microlophus sp.)

Although one might think that Darwin probably discovered most of the species native to the Galápagos Islands, others had been there before him. The first mention of these snakes in the scientific literature came 80 years before Darwin was born, by explorer William Dampier, a natural historian whose scientific accomplishments have been largely overshadowed by his reputation as a buccaneer. In his 1729 memoir, New Voyage Round the World, he wrote "There are some Green Snakes on [the Galápagos]; but no other land-animal that I did ever see." (Although they are hardly green.) In 1839 Darwin wrote "There is one snake which is numerous; it is identical, as I am informed by [French herpetologist Gabriel] Bibron, with the Psammophis Temminckii from Chile." This turned out not to be true, and the snakes were officially described as a new species in 1860 by Albert Günther, who named it Herpetodryas biserialis, a snake "light brown with a dark brown dorsal band" and having "maxillary teeth...of moderate size,...nearly equal length,...and entirely smooth". In 1912 John Van Denburgh, Curator of the Department of Herpetology at the California Academy of Sciences, wrote a monograph on the snakes of the Galápagos as part of a report on an expedition taken by the Academy in 1905-06. In it, he gave what is still the most complete account of the snakes' (by then moved to the genus Dromicus) natural history and ecology, and described four additional species (one of which was later synonomized with an earlier description by Austrian biologist Franz Steindachner). In accordance with the prevailing geologic thinking of the day, Van Denburg suggested that the snakes, along with the other Galápagos fauna, had reached the Galápagos via a land bridge, rather than by oceanic dispersal.

Plate from Steindachner 1876

Galápagos racers mating

Today these five species are known as Pseudalsophis biserialis (which occurs in two phases, dark and light, and is found on most islands), P. dorsalis (which is striped and found on Santiago, Rábida, Baltra, Santa Cruz, and Santa Fé), P. hoodensis (which is striped and found only on Gardner and Española, formerly known as Hood Island), P. slevini (which is banded and found on Fernandina, Isabela, and Pinzón), and P. steindachneri (which is striped and found on Santiago, Rábida, Baltra, and Santa Cruz). One interpretation is that these five species comprise a clade closely related to the mainland species P. elegans, found in Ecuador and Peru and supporting Bibron's suggestion via Darwin that Galápagos racers are related to and descended from mainland snakes. Variation in pattern and scalation is present but relatively minor. Another is that there were two independent colonizations of the Galápagos by South American snakes: one by Philodryas chamissonis from Chile (this is Bibron's Psammophis temminckii) that gave rise to P. hoodensis, and the other, by P. elegans, responsible for the other species. Others have suggested that P. slevini and P. steindachneri are descended from one ancestor (possibly a species of Antillophis from the Caribbean), P. hoodensis from another (P. chamissonis), and P. biserialis and P. dorsalis from yet a third (P. elegans, which might have invaded more than once). These hypothesized dispersal pathways are similar to those suggested for Tachysphex wasps from Chile, Microlophus lizards from Peru, and shrubs of the family Nolanaceae from Peru and Chile.

A Galápagos Snake among some Marine Iguanas

To me, the first explanation seems the most parsimonious; that is, it is simplest to assume that all snakes on the Galápagos archipelago are descended from a single ancestor (P. elegans), and this is what the most up-to-date taxonomy reflects. Similarities in ecology might account for the morphological similarities that led earlier herpetologists to suggest Chilean and Caribbean ancestry. Although on some islands multiple species are found, this could be explained by multiple movements among islands of the archipelago following clonization and subsequent speciation. A 2008 review by University of Texas evolutionary biologist Christine Parent and her colleagues found that most of the Galápagos terrestrial fauna with known phylogenies (family trees), such as tortoises and finches, have diversified in parallel with the geological formation of the islands, supporting the idea that they colonized the islands only once. Because no detailed molecular phylogeny is available for Galápagos snakes, the final answer to the question of their origin and relationships has not yet been revealed.

Galápagos snake eating a small iguana

I was surprised to find how poorly known these snakes were given the infamy of the islands they inhabit. Because they are probably important predators on Galápagos finches, mockingbirds, and small lizards, as well as on non-native rodents, they deserve more study (although as Nick has pointed out, permission to study animals in the Galápagos can be difficult to obtain). Along with many of the Galápagos' other reptiles and birds, the snakes were probably almost driven to extinction by introduced cats and rats, against which they had not evolved defensive behaviors. Their natural predators probably include Galápagos mockingbirds. Today, tourism and development, although limited in the Galápagos, probably threatens these snakes as much as invasive species, which are beginning to be brought under control. Nick, Lori, and Susannah are busy studying the effects of tourism on the Marine Iguanas - who is studying the Galápagos snakes?

Even in the Galápagos, snakes are not immune to vehicular manslaughter

ACKNOWLEDGMENTS

Special thanks to Nick Kiriazis for inspiring me to write this article with his blog, and thanks to Lori Neuman-Lee, Manuel Mejia, Dave Irving, Jim Moulton, Rosalind Gomes, and Phillip Marsh for their pictures.

REFERENCES

Grehan J (2001) Biogeography and evolution of the Galápagos: integration of the biological and geological evidence. Biol J Linn Soc 74:267-287 <link>

Günther A (1860) On a new snake from the Galápagos islands. The Annals and Magazine of Natural History 3:78-79

Parent CE, Caccone A, Petren K, 2008. Colonization and diversification of Galápagos terrestrial fauna: a phylogenetic and biogeographical synthesis. Philosophical Transactions of the Royal Society B: Biological Sciences 363:3347-3361 <link>

Steindachner F (1876) Die schlangen und eidechsen der Galapagos-inseln. Zoologisch-botanischen Gesellschaft, Wien, Germany. <link>

Thomas R, 1997. Galápagos terrestrial snakes: biogeography and systematics. Herpetol Nat Hist 5:19-40 <link>

Van Denburgh J (1912) Expedition of the California Academy of Sciences to the Galapagos Islands, 1905-1906. IV. The snakes of the Galapagos Islands. Proceedings of the California Academy of Sciences (Series 4) 1:323-374 <link>

Zaher H, Grazziotin FG, Cadle JE, Murphy RW, Moura-Leite JC, Bonatto SL, 2009. Molecular phylogeny of advanced snakes (Serpentes, Caenophidia) with an emphasis on South American Xenodontines: A revised classification and descriptions of new taxa. Pap Avulsos Zool (Sao Paulo) 49:115-153 <link>

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