Life is short, but snakes are long

Many people live in fear of snakes, especially of venomous species that can inflict a lethal bite. There is evidence that our fear of snakes is innate, because our ancestors have been preyed upon by them for millions of years, even before we were primates. Other evidence suggests a significant learned component to ophidiophobia. Either way, few people today are at risk of being eaten by snakes, but bites from venomous snakes are still fairly common. However, in my experience fear of snakes is way out of proportion to the actual risk they pose, especially among my fellow North Americans. It's surprisingly hard to find good information on the prevalence of venomous snakebite (hereafter, just 'snakebite'), but it's getting easier, and I was able to gather almost 100 papers that include data on the subject, which I've synthesized here. As a result, this article has many footnotes, and because I used so many references to prepare this article I've provided a selected list at the end of this post, with a link to the full list.

Map of snake envenomings per year, from Wikimedia Commons

So how dangerous is a snake bite? If you're bitten by the wrong kind of snake and you're far from help, it's pretty dangerous. But the truth about snakebite is that it's a lot less likely to endanger your life than people think. First of all, you're pretty unlikely to ever get bitten. Worldwide, estimates range from 1.2 million to 5.5 million snakebites annually. Remember, there are several billion people out there, so although those numbers are large, each year over 99.92% of people are not bitten by a venomous snake. These bites result in 420,000-1.8 million envenomings leading to 20,000-94,000 deaths. This probably seems really low, until you realize that unlike when they are biting their prey, snakes that are biting in defense don't inject venom every time (i.e., the bite is "dry"). Depending on the species of snake and the context of the bite, estimates for dry bites range from 8% to more than 80%, with North American rattlesnakes, one of the best studied groups, injecting venom only 20-25% of the time when biting in defense, compared to more than 99% of the time for predatory strikes.¹ This behavior is partly because the strike itself may startle attacker sufficiently and wasting expensive venom needed to eat is useless, and partly because even injecting venom into an attacker is unlikely to immediately incapacitate it. Most snake venom is fast-acting, but it's not that fast. As a result of these dry bites, a lot of snakebites go untreated and unreported because they fail to produce symptoms, leading the bitten person to assume (correctly) that they are safe or (incorrectly) that the snake was not venomous. This is one major cause of the wide range of numbers given above for the prevalence of snakebite.

Copperheads (Agkistrodon contortrix) bite
a few hundred people a year in my home state of
North Carolina, more than in any other state.
Fatalities are exceedingly uncommon.

Worldwide, about 1 out of every 20 people envenomated by venomous snakes dies from the bite, according to the best available estimates for the prevalence of bites and resulting deaths between 1985 and 2008. Depending on where you live, your chances of surviving a venomous snakebite are really good, although in a few places they're pretty bad. I'm going to focus on the USA because I live here and because we have some of the best data. In the USA, only 1 out of every 500 people bitten by a venomous snake dies as a result, which includes deaths from bites that take place under several special circumstances that we'll discuss later. You're actually safer from venomous snakebite in the USA than in any other country on Earth where venomous snakes kill people, thanks to our excellent medical care, relatively benign venomous snake fauna, and large proportion of the population that live in urban areas where venomous snakes are scarce. There are some countries, such as Canada² and Norway, where venomous snakebites occur but nobody has apparently been killed by one in recent history, except for people who have been killed by their exotic, captive snakes (more on this later).

Western Diamondback Rattlesnakes (Crotalus atrox)
are large and widespread in the southwestern USA.
A recent study showed rattlesnake size to be among the
most important factors determining bite severity, with the
largest snakes causing the most serious bites.

How about all the people who are bitten and survive? Being bitten by a venomous snake isn't exactly a pleasant experience. It's been described as feeling like “hitting your thumb with a hammer”, “stepping on a bare electrical wire”, or “being repeatedly stabbed with a knife”. This alone is a good enough reason to avoid snakebite. However, not every venomous snakebite is a recipe for a nightmare. In the USA, most people are bitten by pit vipers (copperheads, cottonmouths, and rattlesnakes). Very few people are bitten by coralsnakes, and I'd be surprised if anyone has ever been bitten by a coralsnake that they didn't first pick up. Pit vipers are generally pretty retiring snakes, a fact observed most poignantly by both the herpetologist Clifford Pope, who called them first cowards, then bluffers, then warriors, and also by Thomas Jefferson, who wrote of a rattlesnake: "She never begins an attack, nor, when once engaged, ever surrenders...she never wounds 'till she has generously given notice, even to her enemy, and cautioned him against the danger of treading on her."

Figure from Gibbons & Dorcas (2002)

In a field test of these famous anecdotes, Whit Gibbons and Mike Dorcas molested 45 wild cottonmouths (Agkistrodon piscivorus) in South Carolina swamps and found that only 2 in 5 bit their fake hand when picked up, only 1 in 10 bit a fake foot when it stepped on them, and none bit a false leg that stood beside them. In a similar test, Xav Glaudas and colleagues picked up over 335 pigmy rattlesnakes (Sistrurus miliarius) in Florida and found that only 8% bit the thick glove they were wearing. Further evidence to support the fact that vipers are reluctant to bite potential predators comes from anecdotes from snake biologists radio-tracking snakes to study their spatial ecology, in which the biologist has accidentally stood on Timber and Eastern Diamondback Rattlesnakes and Puff Adders without provoking any responses. This makes sense because striking is a last resort for these snakes, which have a lot to lose and very little to gain by it. Although this isn't a perfect simulation of a typical snake-human interaction (these researchers weren't trying to kill the snakes in their experiments, after all), these findings are a good argument in the snakes' defense - if they bite you, they probably had a good reason.

Russell's Vipers (Daboia russelii) are probably
one of the world's most dangerous snakes,
combining a relatively aggressive demeanor
and relatively potent venom with a habitat
and geographic range that overlaps areas of
very dense, rural human population in south Asia.

Although the above news is hopeful, it is of course impossible to predict whether an individual snakebite will end in tragedy, so it is prudent to avoid snakebite at all costs. Each year in the USA, between 2,400 and 3,500 bites occur, putting your chances of being bitten by a venomous snake in the USA at about 1 in 100,000.³ If you live in southern or southeastern Asia, you're more justified in having a fear of snakes. In India, at least 80,000 and possibly as many as 165,000 people are bitten by snakes each year (1 in 7,000-14,000). India's venomous snake fauna isn't that much more diverse than the USA's, but medical care isn't as good, and it has about 4 times as many people, many of whom live in rural areas and work in agricultural or pastoral professions, both of which really increase your chances of being bitten. Even in India, "only" about 10,000-15,000 people a year die from snakebite (edit: a more recent study that estimated snakebite mortality in India using household surveys instead of hospital records came up with a figure of ~46,000 deaths in 2005, which is probably more accurate because many victims elect to use traditional therapy in their village and most do not die in government hospitals, where the data are collected), meaning that about 4 out of 5 (edit: using the newer data, between 1 in 4 and 1 in 2) snakebite victims survive. Taking into account your chances of being bitten and your chances of dying from the bite, many countries in sub-Saharan Africa, Asia, and Latin America are risky places to live. Snakebite in these places is a legitimate public health concern. The USA is the least risky country in terms of snakebite. The only safer countries are places like Ireland, New Zealand, Madagascar, and oceanic islands in the Pacific & Caribbean, where no venomous snakes occur. Snakebite risk in the USA is thousands of times lower than it is in many parts of the world, and it would be even lower if people modified their behavior in a few key ways, starting with not attempting to kill every snake they see.

You might be surprised to hear that attempting to kill venomous snakes actually increases your risk of snakebite. This masterful post written by David Steen at Living Alongside Wildlife is a good argument for why this is the case. Specifically, the reason is that about 2/3rds of snakebites in the USA are a direct result of intentional exposure to the snake and could be avoided if the people involved had made different decisions. These bites resulted from people who were trying to kill snakes or molest them, or who chose to interact with them for some other reason (ranging from snake handling churches to collection for rattlesnake roundups). Although snakebite is an occupational hazard for some, such as zookeepers and herpetologists, the vast majority of Americans are at extremely low risk of snakebite.

Black Mambas (Dendroaspis polylepis) are among
Africa's most dangerous snakes, but they still kill fewer
people than hippos or mosquitos

Let's take a closer look at those 5 people a year who die from venomous snakebite in the USA. Not all of these people are hikers, fishermen, and gardeners who fall victim to 'legitimate' bites, as you might assume. This number includes deaths that result from a pair of special cases that deserve special attention. The first is people who keep exotic venomous snakes in captivity in their homes. Although this can be done safely, it isn't always, and it is a little unfair to group these cases in with 'legitimate' bites, envenomations, and deaths from native, wild venomous snakes. It inflates USA snakebite statistics both because the risk is not evenly distributed among the entire population and it inflates death statistics because antivenom may not be available for these exotic snakes. About 1 of the 5 deaths each year in the USA can be attributed to these circumstances. The second special case, people who refuse or do not seek treatment after they are bitten, includes some of the bites that also fall under the first case, because some snake owners that keep snakes illegally may not seek treatment out of fear that they will be arrested, fined, or have their animals confiscated. This case also covers religious snake handlers proving their faith, which in many cases entails foregoing treatment. It's harder to put a finger on how many people die in the USA each year from untreated snakebites, but I think it's probably fair to say that most of those people got what was coming to them. Let's not overlook the role of alcohol in people's decisions to interact with venomous snakes: studies show that around 40% of snakebite victims have been drinking. Data on intentionality of exposure to snakes in developing countries is sparse, but I would be willing to bet that exposure in these places is much less intentional, as it once was in the USA.

CroFab antivenom used to
treat most snakebites in the USA

Today in the USA, medical treatment for snakebite is so good (thanks to synthetic antivenoms with few side-effects), and research on snake venom has come so far (with much left to learn!), that there is little justification for the overblown fear bordering on hatred people have of snakes. Progress toward this same goal is being made by some really smart people researching the venom of snakes in developing countries in Africa, south Asia, and Latin America, and figuring out better ways to make antivenom available outside of a hospital setting.

Yet more than 1 in 20 people in the USA have a pathological fear of snakes, as defined by criteria including uncontrollable, greater than justified, and significantly interferes with a person’s routine, occupational or academic functioning, or social activities or relationships. Leading to situations like this recent news story and this bizarre interaction between a man, a gun, and a snake. Risk perception is influenced by many things, including the rarity of the event, how much control people think they have, the adverseness of the outcomes, and whether the risk is voluntarily or not. For example, people in the United States underestimate the risks associated with having a handgun at home by 100-fold, and overestimate the risks of living close to a nuclear reactor by 10-fold. Ironically, evidence suggests that two of these things (how much control you have and how voluntary the risk is) are actually quite high for snakebite, despite popular perception that is it low.

Eastern Brown Snakes (Pseudonaja textilis) are one of
Australia's more dangerous snakes, but even they won't
chase, bite, or attack people without trying to escape
or bluff first. Australia's low population density
also contributes to their low prevalence of snakebite.

Data on fear of snakes in developing countries is lacking, and it is difficult to generalize, but based on the impressions of several people I know who have lived and worked there, most inhabitants of rural areas in developing countries seem to be terrified of snakes. One notable exception is Madagascar, where no venomous snakes occur and it is fady to kill any snake. In contrast, in Australia people seem to have a relatively high level of respect for snakes and don't seem to mess with them solely out of machismo the way they do in the USA. Venomous snakebites are relatively rare, which is remarkable considering that the majority of snakes in Australia are venomous. I heard a story recently about a newly-hired Australian CEO of an American mining company. When the new boss asked about the snake policy, the employees jokingly replied that it was "a No. 2 shovel". The Australian CEO was not amused, because at his previous company Down Under routinely relocated much more dangerous snakes at their job sites. He instituted a company-wide training program to teach safe venomous snake practices. These classes are also available to the general public in some areas, especially in southern Africa.

As people and wildlife come to share more and more space, snake-human interactions are inevitable. The future of conservation will probably be in maximizing compatibility between humans and wildlife rather than preserving pristine areas, we will need to get a lot better about behaving ourselves to keep ourselves safe from the defense mechanisms of wildlife, starting with educating ourselves about the real risks that underlie our fears. Everyone should read these guidelines for snakebite prevention and first aid. I would add to this: don't kill snakes! It only puts you at risk. Don't try to kill them, don't let your friends kill them, don't let your family members kill them. They won't try to kill you. I promise.

1 Venomous snakes that are striking at their prey practically always inject venom, and in fact can precisely meter their venom so that they inject exactly the right amount needed to kill each particular prey item, based on its mass. Fortunately for humans, there are no venomous snakes large enough to consider us prey.^↩

2 Although global snakebite statistics frequently list 0 fatalities out of 200-300 snakebites for Canada, this seems not to be quite accurate. In Ontario, at least two people have been killed by Timber Rattlesnakes (Crotalus horridus), a soldier who was bitten at the battle of Lundy's Lane near Niagara Falls in 1814, and an American Indian chief prior to 1850. Two or three people have been killed by bites from Massasaugas (Sistrurus catenatus) in Ontario, all before 1962, and between 0 and 10 people were bitten annually from 1971-2007, mostly men aged 10-29. In 1981, a man who was "quite intoxicated" was killed by a bite from a Northern Pacific Rattlesnake (Crotalus oreganus) on the Nk’meep reserve near the town of Osoyoos in British Columbia's Okanagan Valley. He was the first person to be bitten by a native venomous snake in BC in over 50 years. The only other Canadian provinces that are home to venomous snakes are the Prairie Provinces of Alberta and Saskatchewan, where no recorded deaths have occurred from Prairie Rattlesnake (Crotalus viridis) bites. So we can conclude that native snakebites in modern Canada are even more infrequent than but follow the same basic pattern as those in the USA.^↩

3 In the US, relative to dying from heart disease (1 in 5), cancer (1 in 7), in a motor vehicle accident (1 in 80), in a fall (1 in 185), from a gunshot (1 in 300), by drowning (1 in 1100), by choking (1 in 4400), from drinking too much alcohol (1 in 10,900), by a sting from a wasp, bee, or hornet (1 in 63,000), from being struck by lightning (1 in 80,000), from a dog bite (1 in 120,000), or in an earthquake (1 in 150,000), you are very unlikely to be killed by a snake (1 in 480,000). The only less-likely causes of death are being trapped in a low-oxygen environment (1 in 548,000), being killed by ignition or melting of nightwear (1 in 767,000), and being bitten by a spider (1 in 960,000). These odds are for your entire lifetime; your annual chance of being killed by a venomous snake is more like 1 in 50 million. Worldwide, they're more like 1 in 200,000, which is a lot higher but still pretty low overall.^↩

ACKNOWLEDGMENTS

Thanks to Julia Riley and James Baxter-Gilbert for providing me with information on deaths from snakebite in Canada, to Wes Anderson, James Van Dyke, and Xav Glaudas for sharing with me with their impressions of people's fear of snakes outside of North America, and to Matt Clancy, John Worthington-Hill, Larsa D., Todd Pierson, and Pierson Hill for the use of their photography.

SELECTED REFERENCES
(click here for a full list of references pertaining to snakebite)

Bellman, L., B. Hoffman, N. Levick, and K. Winkel. 2008. US snakebite mortality, 1979-2005. Journal of Medical Toxicology 4:43 <link>

Gibbons, J. W. and M. E. Dorcas. 2002. Defensive behavior of Cottonmouths (Agkistrodon piscivorus) toward humans. Copeia 2002:195-198 <link>

Glaudas, X., T. M. Farrell, and P. G. May. 2005. The defensive behavior of free–ranging pygmy rattlesnakes (Sistrurus miliarius). Copeia 2005:196-200 <link>

Hayes, W. K., S. S. Herbert, G. C. Rehling, and J. F. Gennaro. 2002. Factors that influence venom expenditure in viperids and other snake species during predator and defensive contexts. Pages 207-234 in G. W. Schuett, M. Höggren, M. E. Douglas, and H. W. Greene, editors. Biology of the Vipers. Eagle Mountain Publishers, Eagle Mountain, UT <link>

Isbell, L. A. 2006. Snakes as agents of evolutionary change in primate brains. Journal of Human Evolution 51:1-35 <link>

Janes Jr, D. N., S. P. Bush, and G. R. Kolluru. 2010. Large snake size suggests increased snakebite severity in patients bitten by rattlesnakes in southern California. Wilderness and Environmental Medicine 21:120-126 <link>

Juckett, G. and J. G. Hancox. 2002. Venomous snakebites in the United States: management review and update. America Family Physician 65:1367-1375 <link>

Kasturiratne, A., A. R. Wickremasinghe, N. de Silva, N. K. Gunawardena, A. Pathmeswaran, R. Premaratna, L. Savioli, D. G. Lalloo, and H. J. de Silva. 2008. The global burden of snakebite: a literature analysis and modelling based on regional estimates of envenoming and deaths. PLoS Medicine 5:e218 <link>

Morandi, N. and J. Williams. 1997. Snakebite injuries: contributing factors and intentionality of exposure. Wilderness and Environmental Medicine 8:152-155 <link>

Parrish, H. M. 1966. Incidence of treated snakebites in the United States. Public Health Reports 81:269-276 <link>

Swaroop, S. and B. Grab. 1954. Snakebite Mortality in the World. Bulletin of the World Health Organization 10:35-76 <link>

Tierney, K. J. and M. K. Connolly. 2013. A review of the evidence for a biological basis for snake fears in humans. The Psychological Record 63:919-928 <link>

Van Le, Q., L. A. Isbell, J. Matsumoto, M. Nguyen, E. Hori, R. S. Maior, C. Tomaz, A. H. Tran, T. Ono, and H. Nishijo. 2013. Pulvinar neurons reveal neurobiological evidence of past selection for rapid detection of snakes. Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.1312648110 <link>

Walker, J. P. and R. L. Morrison. 2011. Current management of copperhead snakebite. Journal of the American College of Surgeons 212:470-474 <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.

Rough Green Snakes (Opheodrys aestivus)
mostly eat insects and spiders.
Photo by Kevin Durso

Next week, a few herpetology bloggers, including myself, are putting on a blogging carnival to celebrate the Year of the Snake! The theme is going to be ecosystem services of snakes - from the relatively well-studied relationships between snakes and their ecosystems in some parts of North America, to the basically unknown services rendered by snakes in Madagascar and elsewhere.

Social media has become an important tool for conducting effective science education and outreach, and amphibians and reptiles, especially snakes, have much to gain from this kind of positive exposure. Many reptiles and amphibians occur in large numbers, are top predators, and provide important services to their ecosystems. However, these animals are often cryptic, and the general public seems to overlook their presence and great importance. As a result, we have decided to bring attention to a network of students, naturalists, and professionals that use social media to communicate information about amphibian and reptile natural history, science, and conservation.

Our inaugural event is inspired by Partners in Amphibian and Reptile Conservation’s (PARC) Year of the Snake. On December 9th we will be publishing blog posts about the diversity of ecosystem services provided by snakes. Snakes are generally vilified in the popular media. Our goal is to create new media that accurately portrays snakes’ importance in the hopes of decreasing the negative perception many people hold against them. Leading up to this day, we will be tweeting about snake ecosystem services using the hashtag #SnakesAtYourService. We encourage everyone to follow us on Twitter, visit our blogs on December 9th, and help spread the word about our outreach event, which we hope will be the first of many touching on different themes related to the importance of amphibians and reptiles.

December 9^th2013 Participating Blogs and Authors:

Life is Short But Snakes are Long: Ecology of Snake Sheds by Andrew Durso @am_durso

Living Alongside Wildlife: Kingsnakes Keep Copperheads in Check by David Steen @AlongsideWild

Nature Afield: Pythons as Model Organisms by Heidi Smith @HeidiKayDeidi

Ophidiophilia: Converting Ophidiophobes to Ophidiophiles, One Kid at a Time by Emily Taylor @snakeymama

The Traveling Taxonomist: Snakes of Madagascar: Cultural and Ecological Roles by Mark Scherz @MarkScherz

Social Snakes: Good Neighbors Make a Greater Impact: How Viper Behavior Increases Their Effect on Prey Populations by Melissa Amarello @SocialSnakes

Strike, Rattle, and Roll: Snakes and the Ecology of Fear by Bree Putman @breeput

Australian Museum: When the Frogs Go, the Snakes Follow by Jodi Rowley @jodirowley

Clic aquí para la edición española

Today I am participating in my first Blog Carnival (or blogero, click here for the Spanish edition), which is called #SnakesAtYourService and is about the roles snakes play in ecosystems. Check out the links to the other posts below.

I've already written a series of posts about identifying snake sheds, which is definitely the most common question people ask about them (those three posts make up over a third of all the traffic on this site). People ask other questions about snake sheds much more rarely. In fact, I never stopped to ask some basic questions myself. What are snake sheds made of? What are they used for, and by whom? Where are they found? Do they make substantial contributions to ecology? You might think that because snake sheds are so insubstantial that they don't have much of an impact, but several facts about snakes lead us to believe otherwise.

Part I: Contributions to nutrient cycling

Oodles of Black Swampsnakes (Seminatrix pygaea)
from Ellenton Bay, South Carolina

Snakes can occur at high densities, although their population density can be difficult to measure because snakes are so hard to find. Some estimates provided by snake population ecologist JD Willson in his dissertation included 4-14 vipers per hectare in Scandinavia, 275 vipers per hectare on Shedao Island in China, and over 1000 ring-necked snakes per hectare in Kansas. Aquatic snakes in Ellenton Bay, South Carolina, where I did my undergraduate field research, can reach densities of 170 snakes/ha. I did a couple of back-of-the-envelope calculations using these estimates, plus those for snake shed frequency and shed energetic content, and found that all snakes shedding across the entire continental United States probably generate close to 1.6 billion pounds of shed skin each year, which contain about 3.6 trillion calories of energy. That's enough for everyone in Alabama to survive eating nothing but snake sheds every day all year long (ma, not this for dinner again!), if they could somehow collect all the snake sheds from the entire country. So it isn't an unimaginably immense amount of energy, but it's not insubstantial either. Given the results of this rather bizarre thought exercise, I think it's safe to say that shed snake skin contributes substantially to nutrient cycling in areas where snakes frequently shed.

A food web showing snakes as top predators

What exactly do I mean by nutrient cycling? Think of it as nature's ultimate recycling. It's one example of the services that ecosystems provide for free, and it's why you have regular access to clean water to drink, air to breathe, food to eat, and other essentials, without having to manufacture or engineer systems to produce these things. The cycles of carbon, nitrogen, sulfur, and other elements in and out of the water, air, soil, and the bodies of plants, animals, and microbes, are critical to maintaining a healthy ecosystem. Perturbations can lead to serious imbalances, like the changes to the global carbon cycle that result from the burning of fossils fuels. Few people have investigated the roles that amphibians and reptiles play specifically in nutrient cycling, but we are beginning to suspect that they are important components of many ecosystems. They may be small, but there are a lot of them. For instance, redback salamanders in forests in the northeastern US outnumber all other terrestrial vertebrates combined. On some Pacific islands, lizards occur at densities of over 67,000 per hectare. Snakes can occur at really high densities as well, partly because they are so efficient at converting food into biomass as a result of being ectothermic (cold-blooded) and partly because feeding as infrequently as they do reduces the effects of competition with other snakes. By one estimate, snakes are 25 times more efficient at turning food into biomass than carnivorous mammals of equal size, and occur at population densities 20 – 1400 times greater, meaning that they probably contribute disproportionately to nutrient cycling. Explicit investigation of this phenomenon is underway in turtles, which have large bony shells that probably contribute to cycling of calcium and phosphorus, but to my knowledge no one has so far studied this in any snake, let alone for shed snakeskin.

A red-tailed green ratsnake (Gonyosoma oxycephalum)
sheds its skin

In the wild, shed snake skins disintegrate in about a week, although if you collect one and put it in a plastic bag, they can last decades. The chemical composition of snake sheds is poorly known, but they contain some keratin and some lipids, among other things. Some fungi feed on keratin, including those that cause athlete's foot and ringworm as well as the chytrid fungus that has caused amphibian declines worldwide (with disastrous consequences for the snakes that specialize on them), but these species mostly grow on living organisms. Although we don't know for sure, it seems likely that numerous fungi and microbes have probably evolved to take advantage of the abundant energy found in snake sheds. Of course, the dead bodies of the snakes themselves also eventually contribute to nutrient cycling, but depending on the source of mortality, many of those are probably eaten by predators, and fewer probably decompose compared with snake sheds.

Part II: Use by other animals

An Eastern Indigo Snake (Drymarchon couperi)
getting ready to shed

Snakes shed their skin in order to grow bigger. You do this too, just not all in one piece. Once a snake sheds its skin, it's typically done with it. However, both snakes and you might be surprised to learn that snake sheds are frequently used by other animals for a variety of purposes. As I mentioned previously in my article on conservation successes with Eastern Indigo Snakes, snake sheds are really smelly, and specially-trained dogs can sniff out even individual scales left over from a decomposing snake shed. This might be one reason that, although snakes usually spend several days inactive at their shedding site prior to shedding, they don't normally hang around for long afterwards - their predators might have an easier time finding their stinky sloughs than they would finding the snakes themselves. This could be especially true when those predators are other snakes. Some evidence suggests that dogs have an easier time sniffing out snake skins than actual snakes - the indigo-snake -sniffing dogs correctly identified a concealed snake 4 out of 5 times, but they got the sheds right every time. Dogs have also been used to help search cargo on Guam for hitchhiking Brown Tree Snakes, an invasive species which has spread around the Pacific. No word on whether the Brown Tree Snakes were shedding or how this affected the dogs' ability to smell them.

Most shedding sites are protected in some way, because snakes are vulnerable prior to shedding - they cannot see and other functions may be impeded as well. Shed sites used by Black Ratsnakes in Ontario include old barns, old mining machinery, cracks in building foundations, old hay piles, large hollow logs, rock crevices, and standing dead trees. Most of these things sound like something somebody might want to "clean up", but the fact is that they are important habitat features that many amphibians and reptiles use for shedding and also for hibernation. Many burrowing snakes come to the surface to shed, and shedding snakes may remain on the surface even during cold weather, when other snakes have retreated underground.

Sometimes other animals exploit the stink of snake sheds. Ground squirrels in California use them to scent themselves - first they chew up shed rattlesnake skins, then vigorously lick their own fur, which results in a type of olfactory camouflage that reduces a rattlesnake's ability to correctly identify snake-scented ground squirrels as prey. Rattlesnakes and ground squirrels in California a partners in a coevolutionary relationship that goes back millions of years and has been well-studied by scientists from both the predator's and the prey's point-of-view.

A Great-crested Flycatcher nest with several
snake sheds

Birds use snake sheds in their nests, something people have noticed since at least as far back as the 1800s. Although birds cannot smell, ornithologists (who should study snakes more often) wondered whether the shed skins helped protect eggs or nestling birds by deterring would-be predators. Recently, two experiments have helped determine which predators might be frightened off and whether the strategy really works. Ecologists at Arkansas State University conducted a study to test whether snake skin is an effective deterrent to predators. They found that flying squirrels, a major nest predator, ate the eggs out of 20% of nests without sheds, but didn't depredate any nests with sheds. Because flying squirrels are themselves vulnerable to predation by snakes, this makes intuitive sense. Interestingly, they also noticed that the deterioration rate of the snake skins in their experimental nest boxes (which were not occupied by birds) was much faster than that in real nests, where birds were actively raising chicks. Many of the sheds were eaten by ants, which would probably have been eaten by birds maintaining active nests. Ornithologists in Slovakia found opposing results - nests of great reed warblers festooned with snake sheds were no more or less likely to be depredated by birds and small mammals. However, over a third of reed warblers incorporated grass snake (Natrix natrix) sheds into their nests. When given a choice, two thirds of female reed warblers elected to use sheds left near their nests, whereas only 10% used ribbons of a similar length and color. If they weren't deterring predators, what were they for? The researchers suggested that because snake skins were mainly incorporated by female birds early in the nest-building process, they may have functioned as a signal to male reed warblers that the nest-builder was good at finding rare nest materials, which might lead the male to invest more heavily in helping share the duties of parental care later on in the nesting season.

This holiday season, you can choose from a variety
of snake shed jewelry for that special someone

Humans use snake sheds too. Because of their many similarities with the outermost layer of human skin, shed snake skins are used as model membranes in membrane permeability research, which primarily includes studies of ways to better transport pharmaceuticals into target cells, including some drugs that are inspired by or derived from snake venom (another ecosystem service). Snake sheds are a good alternative to using human, mouse, or synthetic skin, because they are cheap, large, and lack hair. This work is just one of many examples of snakes being used as model organisms to study general concepts in biology. Snake sheds can also be very aesthetically pleasing - many people have taken to creating beautiful snake shed jewelry.

Finally, snakes are themselves very olfactory creatures. Skin lipid pheromones have been shown to play important roles in male combat and in mating behavior, which could mean that sexual selection could act on these chemicals, creating species-specific diversity and dimorphism between males and females, which is mostly lacking in other snakes (except for a few species, including Langaha from Madagascar, where snake play many important cultural and ecological roles). Because most of these pheromones are in the skin, what's the potential for snakes to use their shed skins to mark territories, communicate information about their reproductive stage, select ambush sites, or perform other functions? Really, no one knows. Although territoriality is not the norm in snakes, some species have been suggested to be territorial and others may exhibit other types of social behavior. I hope that by understanding more about the important roles snakes play in ecosystems, people attending this carnival will be more likely to see them as valuable and less likely to fear them. As I hope I've been able to communicate, the old axiom that 'the only good snake is a dead snake' is just not true.

ACKNOWLEDGMENTS

Thanks to JD Willson, Angie Luebben, and Volker Wurst for their photographs and to everyone who helped publicize this blog carnival. A special thanks to the other #SnakesAtYourService blog carnival participants. Be sure to check out their contributions:

Social Snakes: Good Neighbors Make a Greater Impact: How Viper Behavior Increases Their Effect on Prey Populations by Melissa Amarello, @socialsnakes

Living Alongside Wildlife: Kingsnakes Keep Copperheads in Check by David Steen, @AlongsideWild

Nature Afield: Pythons as Model Organisms by Heidi Smith, @HeidiKayDeidi

Ophidiophilia: Converting Ophidiophobes to Ophidiophiles, One Kid at a Time by Emily Taylor, @snakeymama

The Traveling Taxonomist: Snakes of Madagascar: Cultural and Ecological Roles by Mark Scherz, @MarkScherz

Strike, Rattle, & Roll: Snakes and the Ecology of Fear by Bree Putman, @breeput

Australian Museum: When the Frogs Go, the Snakes Follow by Jodi Rowley, @jodirowley

SnakeBytes: The Brown Tree Snake of Guam by Brian Barczyk (@SnakeBytesTV)

REFERENCES

Blem, C. R. and M. P. Zimmerman. 1986. The energetics of shedding: energy content of snake skin. Comparative Biochemistry and Physiology Part A: Physiology 83:661-665 <link>

Blouin-Demers, G. and P. Weatherhead. 2001. Habitat use by black rat snakes (Elaphe obsoleta obsoleta) in fragmented forests. Ecology 82:2882-2896 <link>

Clark, R. W. 2007. Public information for solitary foragers: timber rattlesnakes use conspecific chemical cues to select ambush sites. Behavioral Ecology 18:487-490 <link>

Clucas, B., D. H. Owings, and M. P. Rowe. 2008. Donning your enemy's cloak: ground squirrels exploit rattlesnake scent to reduce predation risk. Proceedings of the Royal Society B: Biological Sciences 275:847-852 <link>

Engeman, R. M., D. V. Rodriquez, M. A. Linnell, and M. E. Pitzler. 1998. A review of the case histories of the brown tree snakes (Boiga irregularis) located by detector dogs on Guam. International Biodeterioration & Biodegradation 42:161-165 <link>

Itoh, T., J. Xia, R. Magavi, T. Nishihata, and J. H. Rytting. 1990. Use of shed snake skin as a model membrane for in vitro percutaneous penetration studies: comparison with human skin. Pharmaceutical Research 7:1042-1047 <link>

Medlin, E. C. and T. S. Risch. 2006. An experimental test of snake skin use to deter nest predation. The Condor 108:963-965 <link>

Stevenson, D. J., K. R. Ravenscroft, R. T. Zappalorti, M. D. Ravenscroft, S. W. Weigley, and C. L. Jenkins. 2010. Using a wildlife detector dog for locating Eastern Indigo Snakes (Drymarchon couperi). Herpetological Review 41:437-442.

Trnka, A. and P. Prokop. 2011. The use and function of snake skins in the nests of Great Reed Warblers Acrocephalus arundinaceus. Ibis 153:627-630 <link>

Willson, J. D. 2009. Integrative approaches to exploring functional roles of clandestine species: a case study of aquatic snakes within isolated wetland ecosystems. PhD dissertation, University of Georgia, Athens, GA <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.

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.

Click here to read this post in Spanish!

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Wolf Snakes (Lycodon aulicus) have become established
on Mauritius, where they threaten native skinks and geckos

Reptiles have been moving around the globe for a long time, often assisted by humans. Skinks and geckos had dispersed to the remotest Pacific islands by about 1600 BCE, at least partly thanks to the aid of the first human colonists of those regions. Brown Tree Snakes (Boiga irregularis) were brought from Australasia to Guam during World War II. In more recent decades, Burmese Pythons (Python molurus) have reached the Everglades, California Kingsnakes (Lampropeltis californiae) the Canary Islands, and Indian Wolf Snakes (Lycodon aulicus) the island of Mauritius in the Indian Ocean. In many cases, these introduced populations of snakes have become invasive, disrupting the native ecosystem in numerous ways, mostly by eating their way through populations of native prey. The indirect effects of these dramatic population declines are unpredictable and profound. For example, on Guam the loss of native forest birds as a result of snake predation led to an explosion of spider populations, with a 40-fold increase in the number of webs compared with nearby islands without invasive snakes that still harbored a native bird community. Although species have been colonizing new ecosystems for a long time, the rapid rate at which they are now being facilitated by global trade is a serious ecological concern. But how new is this problem, exactly?

Where was the first recorded population of introduced snakes? Incredibly, three species of snakes were introduced to the Balearic Islands in the western Mediterranean as far back as 2200 years ago. Having won the Second Punic War, the Roman Republic was expanding west into the Iberian peninsula, which they had taken from Carthage. As a result, transport and trade between the western and central Mediterranean were more regular than ever before, which may help explain the introduction of several species of amphibians and reptiles native to either the European or African mainland to the Balearics. The native people of the Balearics had served as mercenaries under both Rome and Carthage and were renowned for their skill with the sling, but Rome conquered their archipelago anyway shortly after the war and purposefully settled over 3,000 Spanish and Roman colonists there. It's likely that many of these people, understandably, missed their mainland homes, including the native plants and animals to which they were accustomed. They probably brought pet chameleons and tortoises with them, and surprisingly, keeping snakes as pets was also common, so they may have purposefully or accidentally introduced snakes from mainland Europe and Africa for this reason.

Ladder Snake, Rhinechis (Elaphe) scalaris
Their name reflects their dorsal pattern rather than their climbing prowess.

One species, the Ladder Snake (Rhinechis [Elaphe] scalaris), is endemic to the Iberian peninsula. It is a large, adaptable snake that eats mostly small mammals, similar to a North American ratsnake. Although it is easy to see how these snakes could have stowed away on ships, perhaps boarding to eat rats or mice that fed on grain or other goods, it has also been suggested that the Ladder Snake was introduced partly because it played a totemic purpose in mythology and religion. People encouraged non-venomous mammal-eating snakes to take up residence in and near their homes to keep populations of rats and mice under control, and having snakes around the home was thought to maintain the sexual potency of the home's male inhabitants. There is also some evidence that mammal-eating snakes were gathered up and released in areas where epidemics were rampant to help control rat or mouse vectors. This may have led to the association between the Roman god of healing, Aesculapius, whose staff is still a symbol of medicine today, and the Aesculapian Snake (Zamenis [Elaphe] longissimus), a relative of the Ladder Snake.

False Smooth Snake (Macroprotodon mauritanicus)

A smaller species, the False Smooth Snake (Macroprotodon mauritanicus [formerly cucullatus]), is native to northern Africa and southern Spain, where it preys upon small lizards. It might have been introduced to the Balearics accidentally, but no one is really sure how it got there. Apparently, False Smooth Snakes are at least partially responsible (introduced weasels, cats, and genets probably also contributed) for the extinction of an endemic species of lizard, Lilford's Wall Lizard (Podarcis lilfordi), a ground-dwelling, frugivorous species that once dispersed the seeds of a perennial shrub, Daphne rodriguezii. Since the wall lizards began to disappear from the large islands of the Balearics about 2000 years ago, the plants have suffered from a lack of seed disperal, a service formerly provided by the lizard, which would eat the fruit and crap out the seeds. On tiny offshore islets this relationship is still going strong, but on Menorca and Mallorca, where there are many snakes and no lizards, seedlings of D. rodriguezii sprout only underneath their parents, a losing strategy for a young plant.

Viperine Watersnake (Natrix maura)

Finally, the Viperine Watersnake (Natrix maura), a semi-aquatic natricine native to both southwestern Europe and northwest Africa, was introduced to both Menorca and Mallorca in ancient times. During naval battles, both the Phoenicians and the Carthaginians apparently used to throw open jars full of snakes into enemy warships to cause panic among the combatants (apparently even back then nobody could tell the difference between venomous and harmless snakes), which possibly led to or reinforced its populations on the islands. In the Balearics, these watersnakes eat endemic Mallorcan Midwife Toads (Alytes muletensis) (which they consume with impunity despite the frogs' toxins thanks to the snakes' immunity to a wide range of toxins), so a program of active eradication within the range of the frog has been enacted. The Viperine Watersnake could also have been responsible for the extinction of other endemic species of midwife toads never described but historically present.

Snakes may actually be some of the most problematic potential invasive species because they are difficult to detect and almost impossible to eradicate. Research has shown that if you're going to stop an invasive species, you had better stop it early or not at all, a tall order in the face of snakes' impressive crypsis and secretive behavior. Snakes' low energetic requirements allow them to persist through lengthy periods of resource scarcity, and their flexible metabolism allows them to quickly take advantage of resources when they are available, both adaptations to eating infrequent large meals. This scenario is ideal for an individual animal in transit or freshly introduced to a novel environment, who may need to have the ability to remain motionless without feeding or reproducing for long periods of time. Given snakes' long history with people, it's no wonder that Northern and Banded Watersnakes have become established in California, Aesculapian Snakes in Britain, Cornsnakes in the Cayman Islands, Catsnakes in Malta, Monocled Cobras and Habus in the Ryukyu Islands, and many other examples.

ACKNOWLEDGMENTS

Thanks to Rob, Javier Gállego, Aviad Bar, and Jose Zuñiga for the use of their photos.

REFERENCES

Austin, C. C. 1999. Lizards took express train to Polynesia. Nature 397:113-114 <link>

Bruna, E. M., R. N. Fisher, and T. J. Case. 1996. Morphological and genetic evolution appear decoupled in Pacific skinks (Squamata: Scincidae: Emoia). Proceedings of the Royal Society of London. Series B: Biological Sciences 263:681-688 <link>

Lazenby, F. D. 1947. Greek and Roman household pets. The Classical Journal 44:245-252 <link>

Fisher, R. N. 1997. Dispersal and evolution of the Pacific Basin gekkonid lizards Gehyra oceanica and Gehyra mutilata. Evolution 51:906-921 <link>

Pleguezuelos, J. 2002. Las especies introducidas de Anfibios y Reptiles. Pages 501-532 in J. Pleguezuelos, R. Márquez, and M. Lizana, editors. Atlas y Libro Rojo de los Anfibios y Reptiles de España. Dirección General de Conservación de la Naturaleza-Asociación Herpetológica Española, Madrid <link>

Rocha, I. R. S. 2012. Patterns of biological invasion in the herpetofauna of the Balearic Islands: Determining the origin and predicting the expansion as conservation tools. MS thesis. Universidade do Porto <link>

Rogers, H., J. Hille Ris Lambers, R. Miller, and J. J. Tewksbury. 2012. ‘Natural experiment’ demonstrates top-down control of spiders by birds on a landscape level. PLoS ONE 7:e43446 <link>

Traveset, A. and N. Riera. 2005. Disruption of a plant‐lizard seed dispersal system and its ecological effects on a threatened endemic plant in the Balearic Islands. Conservation Biology 19:421-431 <link>

In continuing association with the group that brought you the #SnakesAtYourService December blog carnival, this post is part of the new Reptile & Amphibian Blogging Network's first event, #HerpsAdapt. Starting on February 12th (in honor of Charles Darwin’s birthday), this event will showcase the remarkable evolutionary abilities of reptiles and amphibians.

Click here to read this post in Spanish

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One of several excellent new science mnemonics
from the popular webcomic xkcd

Virgin birth (a form of asexual reproduction) has fascinated humans for centuries. Recently, biologists have uncovered many of the mysteries associated with the ability of some animals to produce offspring without ever mating. This phenomenon is common in bacteria, most fungi, many plants, and some invertebrate animals, where it takes many forms. It is relatively uncommon in vertebrates, although a few species of fishes, amphibians, and reptiles reproduce using a form of asexual reproduction called parthenogenesis, which is when an embryo develops from an unfertilized egg cell. Parthenogenesis can be facultative or obligate. Species with facultative parthenogenesis can also reproduce sexually (and usually do), whereas species with obligate parthenogenesis cannot and are usually all-female. Both types of parthenogenesis are found in snakes, and several new examples have been documented in the past few years.

Brahminy Blindsnake (Ramphotyphlops braminus)

Only one species of snake is known to have obligate parthenogenesis. It is a member of the Scolecophidia, or blindsnakes, called the Brahminy Blindsnake or Flowerpot Snake (Ramphotyphlops braminus). This tiny egg-laying species is made up only of females and is extremely widespread, partially thanks to the ability of just a single individual to colonize new areas. Unlike mammals, most reptiles (and birds) have a ZW chromosomal sex determination system, so instead of the males being XY and the females XX (click here for a review), male snakes are ZZ and female snakes are ZW. However, in common with other obligate parthenogenetic species, Brahminy Blindsnakes are triploid, meaning that they have three sets of chromosomes rather than two. Examination of the karyotype (a picture of one complete set of chromosomes) of Brahminy Blindsnakes has revealed evidence of hybridization, which has also played a role in the origin of other polyploid obligate parthenogenetic vertebrates, including certain lizards, salamanders, and fishes.

Boa constrictor (Boa constrictor)

Facultative parthenogenesis has been documented in a number of species of snakes that normally reproduce sexually. Most of the time this takes place when someone has kept a female snake in captivity for a long period of time. Although it can be difficult to distinguish parthenogenesis from long-term sperm storage, which is possible in snakes over periods of up to at least 5 years, new molecular methods have allowed biologists to differentiate offspring that were produced parthenogenetically from those that were produced from sexual reproduction following prolonged sperm storage. Looking back at supposed cases of lengthy sperm storage may reveal facultative parthenogenesis in unexpected places.

In snakes, there is a wide variety of cellular mechanisms by which parthenogenesis can occur. Evidence for the exact type of facultative parthenogenesis can be gained by examining the sex and karyotype of the offspring, and appears to be correlated with the higher taxonomic group. Captive booid snakes such as rainbow boas (Epicrates maurus) and boa constrictors (Boa constrictor) have given birth to viable female offspring that have a WW sex chromosome pair, which is different from any other known chromosome combination. Why the parthenogenetically-produced offspring of these species are not a 50:50 mix of ZW and WW (the two combinations a female boa is capable of making via meiosis) is unknown.

Burmese Python (Python bivittatus)

Burmese python (Python bivittatus) females are capable of making exact ZW female clones of themselves, using a mechanism that is functionally similar to but distinct from that used by obligate parthenogenetic species like the Brahminy Blindsnake. The python offspring are all females and are mostly viable, having suffered no loss of genetic information. In both boas and pythons, the sex chromosomes are monomorphic, meaning that the Z and the W chromosome are approximately equal in size and indistinguishable from one another. It has been suggested that this method of reproduction might help species circumvent limitations on lifespan and establish new populations when individuals are isolated for long periods of time, although this claim will require more evidence to evaluate because parthenogenesis has not been observed in wild boas or pythons. However, new data from molecular ecologist Warren Booth calls into question some of the conclusions of the original description of parthenogenesis in pythons.

Cottonmouth (Agkistrodon piscivorus)

In contrast, facultative parthenogenesis in caenophidians is fraught with difficulties. Most of the offspring produced this way are not viable because they have suffered a loss of some genetic information. Many are stillborn or have deformities or other abnormalities. All are males, and the litters are unusually small. Nevertheless, parthenogenesis has been documented in both captive and wild Cottonmouths (Agkistrodon picivorus) and Copeprheads (Agkistrodon contortrix), and in captive Eastern Diamondback (Crotalus adamanteus), Timber (C. horridus), and Aruba Island (C. unicolor) Rattlesnakes, four species of gartersnakes (Thamnophis couchii, T. elegans, T. marcianus, and T. atratus), and Arafura filesnakes (Acrochordus arafurae). Most of these species are commonly kept in captivity, and they span the gamut from the most basal caenophidians to the most derived, but the infrequent occurrence and low viability of facultative parthenogenesis in these species suggests that although all caenophidians may be capable of parthenogenesis, it is probably not very ecologically or evolutionarily significant. The reproductive potential of the few captive-born parthenogenetically-produced Copperheads that have survived is currently being assessed.

The next steps in this area of herpetology are to discover more about the different cellular and developmental mechanisms that control and influence parthenogenesis, document parthenogenesis in species and taxonomic groups where it is not so far known, and understand more about the hybrid origins of obligate parthenogenetic species. We still don't know what is required to induce parthenogenetic reproduction in either facultative or obligate species - some lizards require copulation with other females, and many salamanders require egg activation by the sperm of a male salamander of a different species. Who knows what bizarre adaptations parthenogenetic snakes await discovery?

Next month: the story of the most widespread snake in the world!

ACKNOWLEDGMENTS

Thanks to xkcd, JD Willson, Todd Pierson, and Pierson Hill for their drawings and photographs.

REFERENCES

Booth, W., D. H. Johnson, S. Moore, C. Schal, and E. L. Vargo. 2011. Evidence for viable, non-clonal but fatherless Boa constrictors. Biology Letters 7:253-256 <link>

Booth, W., L. Million, R. G. Reynolds, G. M. Burghardt, E. L. Vargo, C. Schal, A. C. Tzika, and G. W. Schuett. 2011. Consecutive virgin births in the New World boid snake, the Colombian Rainbow Boa, Epicrates maurus. Journal of Heredity 102:759–763 <link>

Booth, W., C. F. Smith, P. H. Eskridge, S. K. Hoss, J. R. Mendelson, and G. W. Schuett. 2012. Facultative parthenogenesis discovered in wild vertebrates. Biology Letters 8:983-985 <link>

Germano, D. J. and P. T. Smith. 2010. Molecular evidence for parthenogenesis in the Sierra garter snake, Thamnophis couchii (Colubridae). The Southwestern Naturalist 55:280-282 <link>

Groot, T., E. Bruins, and J. Breeuwer. 2003. Molecular genetic evidence for parthenogenesis in the Burmese python, Python molurus bivittatus. Heredity 90:130-135 <link>

Kearney, M., M. K. Fujita, and J. Ridenour. 2009. Lost sex in the reptiles: constraints and correlations. Pages 447-474 in I. Schön, K. Martens, and P. van Dijk, editors. Lost Sex: The Evolutionary Biology of Parthenogenesis. Springer, Dordrecht, Holland <link>

Reynolds, R. G., W. Booth, B. M. Fitzpatrick, G. W. Schuett, and G. M. Burghardt. 2012. Successive virgin births of viable male progeny in the checkered gartersnake, Thamnophis marcianus. Biological Journal of the Linnean Society 107:566–572 <link>

Schuett, G., P. Fernandez, W. Gergits, N. Casna, D. Chiszar, H. Smith, J. Mitton, S. Mackessy, R. Odum, and M. Demlong. 1997. Production of offspring in the absence of males: evidence for facultative parthenogenesis in bisexual snakes. Herpetological Natural History 5:1-10 <link>

Wynn, A. H., C. J. Cole, and A. L. Gardner. 1987. Apparent triploidy in the unisexual brahminy blind snake, Ramphotyphlops braminus. American Museum Novitates 2868:1-7 <link>

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Figure from Laszlo 1975

Recently somebody asked me "Why do snakes have two penises?" When I tried to answer, I realized that I didn't really know. I did know that they only use one at a time, and I had once heard that it was so that they could copulate with a female no matter which side she was on, but that doesn't really seem to make sense to me any more, especially considering that lizards also have two penises. Together, the two penises of squamates (snakes and lizards) are called hemipenes, and each individually is called a hemipenis. Each hemipenis is associated with a single testis, meaning that sperm produced in the right testis are ejaculated through the right hemipenis, and those produced on the left come out of the left. Hemipenes are normally stored inside out in the base of the tail, forming a pocket into which a probe can be, well, probed to check the sex of a lizard or snake. This is shown nicely in the above diagram. During mating, one hemipenis or the other is everted in a manner similar to taking off a sock. Sexual dimorphism is rare in snakes, except that male snakes almost always have longer, thicker tails than females, because they need someplace to store their hemipenes.

Some examples of snake hemipenes; photo by Robert Jadin

Hemipenes are one of the shared derived characters of squamates (snakes and lizards), distinguishing them from other reptiles (tuataras, turtles, crocodilians, and birds), all of which have either a single or no penis. In general, snake hemipenes are endowed with a groove, called the sulcus spermaticus, down which the sperm runs. Think of a canal rather than a pipe, although during mating the wall of the female's reproductive tract forms the other part of the tube that we mammals have. Hemipenes often have various spines, knobs, branches, and other projections, which typically correspond with the cloacal anatomy of female snakes of the same species, forming a sort of 'lock-and-key' mechanism that isolates species by discouraging mating among unrelated individuals. The amazingly variable structure of the hemipenes has often been used in snake taxonomy for this reason.

Hemipenes of:
top: Mountain Pit-viper
(Ovophis monticola)
middle: Spotted Slug-eater
(Pareas macularius)
bottom: Siamese Spitting Cobra
(Naja siamensis)
photos by Sjon Hauser

But why two? Wouldn't one penis do just as well, since male snakes only use one at a time anyway? Let's take a quick look at the timeline of snake reproduction. Boy snake meets girl snake. They spend some time together, intertwine their tails, and the male inserts one hemipenis so that his sperm find their way safely from cloaca to cloaca. But unlike in humans, female snakes have a lot of control over whether or not they get pregnant after mating. Because the best conditions for mating are not necessarily the best for ovulation and gestation, female snakes can store sperm for a long time, up to 5 years and possibly longer. They have specialized pockets in their reproductive tract where they do this. It can actually be rather difficult to distinguish between long-term sperm storage and facultative parthenogenesis (a form of asexual reproduction) without using molecular techniques to determine whether the offspring share all or just some of their genes with their mother. This is because in the former case, a female snake sometimes gets pregnant long after mating. If she has mated with multiple males, her clutch (in egg-laying species) or litter (in live-bearers) of offspring might be a mixture of offspring from multiple fathers. Amazingly, she can control which fathers' sperm she uses to fertilize her eggs, although exactly how she does this is still unclear. Because of this potential for delayed fertilization, sperm competition and cryptic female mate choice is thought to be more intense in reptiles than in species that usually follow insemination quickly with fertilization. Female snakes can mate with multiple males, and can then choose at their leisure among their sperm each time they reproduce over the next several years, so some male snakes might mate with many females but never produce offspring because their sperm are always judged to be inferior. This can also result in bizarre situations such as male snakes becoming fathers after they have died.

All this can complicate life for male snakes, because their paternity is even less certain than it is for other male vertebrates. As a result, a male snake's reproductive success is probably tied to the number of sperm he transfers to a female (although this is difficult to measure). This is probably a big part of why male snakes and lizards have two penises. Because each testis is dedicated to a single hemipenis, an alternating pattern of hemipenis use would allow a male a second chance to transfer a fresh batch of sperm if he has just mated recently. In humans and most other mammals, sperm from both testes is mixed together prior to ejaculation, so these species have just one chance to inseminate before they enter a refractory period (you know what I mean, guys). In fact, an alternating pattern is what we see when the kind of experiments every snake dreams of being a part of are conducted (in the spirit of full disclosure, most of these experiments were conducted with lizards, but the principle is similar). A male lizard mates with one female, which depletes sperm from that side of his reproductive tract, but he can then use his other hemipenis to inseminate a different female. He only alternates if the second mating opportunity comes during the refractory period, which lasts a few days. If mating opportunities are frequent and he is prevented from alternating (by placing a small piece of tape over one side of his cloaca), his sperm count is much lower on his second and third mating attempt.

Mating Western Diamondbacks, Crotalus atrox (from Clark et al. 2014)

It's advantageous for a female snake to mate with as many males as she can, so that she has a wide variety of sperm to choose from. Female adders with more mates have higher offspring survival, probably due to less inbreeding and more genetic diversity to choose from, especially in regions of the genome where diversity is important, such as the MHC, which codes for proteins involved in recognizing pathogens and initiating an immune response. Many species, including humans, select their mates at least partly on the basis of MHC dissimilarity (which they can judge by smell), and this may also be the case in snakes. However, many male and female snakes often have pretty limited time to get together, since they're only in the same place at the same time for short periods in spring and fall when they're entering and leaving hibernation sites, which might mean that they have to make rapid decisions about who to mate with. However, a recent paper by Rulon Clark and others showed that male Western Diamondback Rattlesnakes have distinct mating strategies depending on their body size. Larger males were more likely to guard their mates throughout the active season. Curiously, this behavior did not result in their fathering more offspring, possibly due to sperm the females had stored from previous years. In one of the most extreme examples of clustered mating, Common Gartersnakes in Canada emerge in huge numbers in spring and mate immediately upon emergence. Unlike in most snakes, there is conflict between males and females over how each sex best maximizes their reproductive success. There's also some evidence that male gartersnakes are "right-handed", preferring to use their right hemipenis unless they have just used it recently (it's connected to the larger right testis in this species). There are fewer studies of the mating systems of tropical snakes, which do not hibernate at all, but I suspect there is more diversity in parts of the world where it is always warm (we just don't know about it yet). One study found that larger male Slatey-grey Snakes (Stegonotus cucullatus) from tropical Australia fathered more offspring than smaller males, which is similar to the situation in many temperate snakes, but the exact evolutionary causes of this phenomenon are complex and have yet to be explained.

Hemipenes of:
top: Indo-chinese Ratsnake
(Ptyas korros)
middle: Banded Kukrisnake
(Oligodon fasciolatus)
bottom: Common Blackhead
(Sibynophis collaris)

All this raises some questions regarding the evolution of penises in vertebrates. I looked but could not find a single instance where a species of squamate had lost their hemipenes. The closest I came are snakes in the African subfamily Psammophiinae (which also includes the enigmatic scale-polishing snakes), which have small hemipenes and peculiar copulatory behavior, the causes and consequences of which are only two of the many things we don't know about psammophiines. The asymmetrical testes of male gartersnakes might be another example, but their left and right hemipenes are of equal size. Because penises don't fossilize well, we don't know very much about the anatomy of ancient snakes and lizards, but it's safe to assume that the common ancestor of all squamates had hemipenes. Although several other reptiles have lost their penises (and in some cases re-evolved some truly bizarre structures, such as the penises of ostriches, emus, ducks, alligators, turtles, and maybe even dinosaurs), there are some similarities between squamate hemipenes and the male reproductive organs of some of the most primitive mammals, the monotremes. Like snakes but unlike other mammals, echidnas have internal testes connected separately to a four-headed penis, similar to the hemipenes of snakes and lizards but joined at the base. Male echidnas only use one side (bearing two heads) at a time (video here), alternate sides just like snakes, and their sperm work cooperatively to reach the egg. The other monotremes, platypuses, have a forked penis, but only the left side is functional, because only the female's left ovary is functional. Many marsupials also have bifurcated penises, with scrotums that hang down in front of them. This suggests that a bifurcated penis might have appeared much earlier in amniote evolution than we think, although it could also be a case of convergent evolution caused by intense post-mating sexual selection on males. Detailed histological, embryological, and genetic studies would be required to answer this question, which would probably constitute the dissertation project you'd least want your family to know about. (update: I found out that Casey Gilman. a PhD student at UMass Amherst is working on this for his dissertation as we speak. You can donate to his crowd-funded project here).

ACKNOWLEDGMENTS

Thanks to Robert Jadin and Sjon Hauser for use of their photographs.

REFERENCES

Booth, W. and G. W. Schuett. 2011. Molecular genetic evidence for alternative reproductive strategies in North American pitvipers (Serpentes: Viperidae): long-term sperm storage and facultative parthenogenesis. Biological Journal of the Linnean Society 104:934–942 <link>

Clark, R. W., G. W. Schuett, R. A. Repp, M. Amarello, C. F. Smith, and H.-W. Herrmann. 2014. Mating Systems, Reproductive Success, and Sexual Selection in Secretive Species: A Case Study of the Western Diamond-Backed Rattlesnake, Crotalus atrox. PLoS ONE 9:e90616 <link>

Dubey, S., G. P. Brown, T. Madsen, and R. Shine. 2009. Sexual selection favours large body size in males of a tropical snake (Stegonotus cucullatus, Colubridae). Animal Behaviour 77:177-182 <link>

Greene, H. W. 1997. Snakes: The Evolution of Mystery in Nature. University of California Press, Berkeley <link>

S. D. Johnston, B. Smith, M. Pyne, D. Stenzel, and W. V. Holt. 2007. One‐Sided Ejaculation of Echidna Sperm Bundles. The American Naturalist 170:E162-E164 <link>

Laszlo, J. 1975. Probing as a practical method of sex recognition in snakes. International Zoo Yearbook 15:178-179.

Madsen, T., R. Shine, J. Loman, and T. Håkansson. 1992. Why do female adders copulate so frequently? Nature 355:440-441 <link>

Olsson, M. and T. Madsen. 2001. Promiscuity in Sand Lizards (Lacerta agilis) and Adder Snakes (Vipera berus): Causes and Consequences. Journal of Heredity 92:190-197 <link>

Sever, D. M. and W. C. Hamlett. 2002. Female sperm storage in reptiles. Journal of Experimental Zoology 292:187-199 <link>

Shine, R., M. M. Olsson, M. P. LeMaster, I. T. Moore, and R. T. Mason. 2000. Are snakes right-handed ? Asymmetry in hemipenis size and usage in gartersnakes (Thamnophis sirtalis). Behavioral Ecology 11:411-415 <link>

Tokarz, R. R. and J. B. Slowinski. 1990. Alternation of hemipenis use as a behavioural means of increasing sperm transfer in the lizard Anolis sagrei. Animal Behaviour 40:374-379 <link>

Tokarz, R. R. and S. J. Kirkpatrick. 1991. Copulation frequency and pattern of hemipenis use in males of the lizard Anolis sagrei in a semi-natural enclosure. Animal Behaviour 41:1039-1044 <link>

Zweifel, R. G. 1980. Aspects of the biology of a laboratory population of kingsnakes. Pages 141-152 in J. B. Murphy and J. T. Collins, editors. Reproductive biology and diseases of captive reptiles. Society for the Study of Amphibians and Reptiles, Lawrence, Kansas.

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Global distribution of snakes

Snakes are found in almost all parts of the world, with the exception of New Zealand and Ireland, the polar regions, the Atlantic Ocean, and some very urban areas. Many species are very widespread. Pelagic Sea Snakes (Pelamis platurus) are probably found over the greatest percentage of the Earth's surface, although they are entirely marine. On land, Ring-necked Snakes (Diadophis punctatus) and Racers (Coluber constrictor) are found throughout North America, European Adders (Vipera berus) from Spain to Kamchatka and above the Arctic Circle, Grass Snakes (Natrix natrix) from Great Britian to Mongolia, and Gaboon Vipers (Bitis gabonica) from Africa's Gold Coast to its Great Rift Valley. However, the title of "most widespread snake in the world" goes to the tiny Brahminy Blindsnake (Ramphotyphlops braminus), named after Hinduism's Brahmin caste.

Map of locations of Brahminy Blindsnakes
Modified from DiscoverLife and Kraus's database
Most dots represent introduced localities

Brahminy Blindsnakes are found on nearly every continent and on countless islands, mostly in the tropics. They are so successful at least in part because they are the only unisexual species of snake. There are no male Brahminy Blindsnakes. There never have been and there never will be. Instead, each female lays about 4 rice-grain-sized eggs a year, which hatch into sewing-needle-sized daughters identical to each other and to their mother. If that doesn't sound very fecund, it's because it isn't - it doesn't have to be! In spite of their low reproductive output, Brahminy Blindsnakes have spread over most of the world, because just a single individual is capable of founding a new population. In fact, we don't even really know where the original native range of the Brahminy Blindsnake was. It is most common in southern Asia, where it was first discovered in 1796, so it's likely that it originated somewhere around there, but it's difficult to say for sure. Usually, biologists can exploit differences in the genetics or morphology of a widespread species to figure out where it came from. Attempts to uncover the geographic origin of Brahminy Blindsnakes have been unsuccessful because all Brahminy Blindsnakes are clones of one another, so there is almost no variation to analyze!

How did this species evolve? The leading theory for most unisexual species of reptiles, amphibians, and fishes involves a hybrid origin, where two or more "parent" species contribute genes. In most unisexual amphibians and fishes, sperm from a male (often of one of the parent species, but sometimes any sperm will do) is required to initiate development of the eggs but does not contribute genetic material. This is not the case for lizards or for the Brahminy Blindsnake, which are truly parthenogenetic. Which were the parent species of the Brahminy Blindsnake? We don't know. Of the 400-odd blindsnake species, the Brahminy Blindsnake is probably one of the best known due to its wide distribution and peculiar reproductive habits. Some recent phylogenies have shown that it is closely related to the South Indian Blindsnake (Typhlops pammeces), and others to an undescribed species of Sri Lankan blindsnake, both consistent with the hypothesis that south Asia is the species' center of origin. One very recent analysis suggested reclassifying all three species into a new genus, Indotyphlops. Because up to a quarter of all blindsnake species are still undescribed, it's possible that the parent species are as-yet unknown to science.

Image from O'Shea et al 2013
You guessed it, that's a Brahminy Blindsnake

These days Brahminy Blindsnakes mostly get around through the horticulture trade, although in the past they may have hitchhiked along with Pacific Islanders. Snakes are generally good dispersers, with the ability to go without food for long periods of time and squeeze into tight spaces, which might help explain why they have successfully colonized most of the world. Of all the fantastic voyages Brahminy Blindsnakes must have undergone, one of the most amazing is that documented by herpetologist and TV personality Mark O'Shea in East Timor. He and his team found a live Brahminy Blindsnake coming out of the back end of a toad, demonstrating the snakes' resilience to even the most caustic of environments.

Most of the time, an introduced species has about a 50/50 chance of successfully establishing itself in a new environment. Given how widespread Brahminy Blindsnakes are and their infamy as invaders, you might ask whether an introduced population of Brahminy Blindsnakes has ever failed to become established? A comprehensive database of reptile introductions includes only two such instances, one in southern Arizona and one in New Zealand. In Arizona, a population has subsequently become established despite the arid climate, but New Zealand is probably too cold for blindsnakes, and they take introduced species very seriously there. Nevertheless, the Brahminy Blindsnake will probably continue to spread, at least throughout the tropical regions of the world. The literature is full of first reports of this species, so much so that at least one was reported twice! Amazingly, both specimens were bicycle casualties collected in the same suburb of Cairo, leading the second author to title his article "How many times can a flower-pot snake be run over for the first time?"

Click here to read more about blindsnakes and their unique relationship with certain owls, or here for a refresher on their place in snake taxonomy!

ACKNOWLEDGMENTS

Thanks to Todd Pierson for his photograph and to Phil Rosen, Jeff Servoss, Don Swann, Michael Lau, and Skip Lazell for bringing me up to date on the latest in blindsnake biology.

REFERENCES

Baha el Din, S. M. 2001. On the first report of Ramphotyphlops braminus from Egypt: how many times can a flower-pot snake be run over for the first time? Herpetological Review 32:11.

Hedges, S., A. Marion, K. Lipp, J. Marin, and N. Vidal. 2014. A taxonomic framework for typhlopid snakes from the Caribbean and other regions (Reptilia, Squamata). Caribbean Herpetology 49:1-61 <link>

Kamosawa, M. and H. Ota. 1996. Reproductive biology of the brahminy blind snake (Ramphotyphlops braminus) from the Ryukyu archipelago, Japan. Journal of Herpetology 30:9-14.

Kraus, F. 2009. Alien reptiles and amphibians: a scientific compendium and analysis series. Springer, Dordrecht <link>

Nussbaum, R. A. 1980. The brahminy blind snake (Ramphotyphlops braminus) in the Seychelles Archipelago: distribution, variation, and further evidence for parthenogenesis. Herpetologica 36:215-221 <link>

O'Shea, M., A. Kathriner, S. Mecke, C. Sanchez, and H. Kaiser. 2013. ‘Fantastic Voyage’: a live blindsnake (Ramphotyphlops braminus) journeys through the gastrointestinal system of a toad (Duttaphrynus melanostictus). Herpetology Notes 6:467-470 <link>

Ota, H., T. Hikida, M. Matsui, A. Mori, and A. H. Wynn. 1991. Morphological variation, karyotype and reproduction of the parthenogenetic blind snake, Ramphotyphlops braminus, from the insular region of East Asia and Saipan. Amphibia-Reptilia 12:181-193.

Wynn, A. H., C. J. Cole, and A. L. Gardner. 1987. Apparent triploidy in the unisexual brahminy blind snake, Ramphotyphlops braminus. American Museum Novitates 2868:1-7 <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.

This post will soon be available in Spanish!

Alternate title suggested by Mike Pingleton: Not all who slither are lost

Clarión Nightsnake (Hypsiglena unaocularis)
Photograph from Mulcahy et al. 2014

Just over one year ago, a team of scientists from the Smithsonian and the Red de Interacciones Multitróficas rediscovered a species of nightsnake (genus Hypsiglena) on remote Clarión Island in the eastern Pacific Ocean, over 400 miles southwest of Cabo San Lucas. Called the Clarión Nightsnake (Hypsiglena unaocularus), it was originally discovered by the renowned American naturalist William Beebe in 1936, during a nocturnal sea turtle nesting survey. Because Clarión Island is only accessible via military escort, biologists have not visited the island frequently since Beebe's time, and in 1955 herpetologist Bayard Brattstrom suggested that perhaps Beebe's locality information had been an error, since only a single specimen existed and several other Clarión Island expeditions had not turned up another. However, the type specimen collected by Beebe, resting in the herpetology collection of New York's American Museum of Natural History, was sufficiently distinct from any other Hypsiglena specimen that it prompted herp phylogeographer Dan Mulcahy to reexamine Beebe's book and field notes, which contained a pretty clear description of the circumstances under which Beebe found the snake:

“We walked on, flashing the light all around. Not far from the water on the black lava

I saw a small dark brown snake. It seemed to be unlike the one I had found in daylight,

having lines of black spots on the body, so I picked it up and cached it in my shirt.”

(p. 282 of Zaca Venture)

Location of Clarión Is.
From Mulcahy et al. 2014
Click to enlarge

As their name implies, Nightsnakes mostly come out at night (although I found one in southern Utah at about 9:30 in the morning a few weeks ago), and even then they are normally only active under certain conditions - in particular, they prefer to be active when there is not much moonlight, such as on cloudy nights or when the moon is new. Even if one is specifically searching for Nightsnakes, they can be difficult to find. Combined with their generally secretive nature, this could explain the failure of several Clarión Island expeditions to find the Clarión Nightsnake - until Mulcahy's expedition in May of 2013, which found 11 individuals in 15 days. Using phylogenetics, they determined that the Clarión Nightsnake is most closely related to the Santa Catalina Nightsnake (H. catalinae), which is found on Santa Catalina Island in the Gulf of California (which is not the same as the well-known Santa Catalina Island off of the US state of California). Nightsnakes are found all around the shoreline of the Gulf of California, and they are obviously exceptional over-water dispersers, because they occur on many of the islands in that region as well.

This remarkable story of rediscovery is a testament to the kind of attention to detail that it takes to be a good natural historian, but it's not the only species of snake that has been rediscovered many years after its initial description. Here are a few others:

Angel’s Stream Snake (Paratapinophis praemaxillaris)
Photograph from Murphy et al. 2008

Angel’s Stream Snake (Paratapinophis praemaxillaris) was described from two newborn specimens from northern Laos in 1929. At that time it was placed into a new genus because of an unusual process on its nose, but a few years later it was moved into the cosmopolitan genus Opisthotropis. Two more specimens were collected in the 1980s, but it wasn't until 2008, when five adult specimens were collected from a pool at the base of a waterfall on the Nan River in northern Thailand, that it became clear that the nose structure was actually an egg tooth, a structure normally lost a few days after hatching. At that time, Paratapinophis was placed back into its own genus because of several other formerly-overlooked unique features, including sexually dimorphic color, pattern, and scale ornamentation. Like most other natricines, this species eats fishes.

Chersodromus rubriventris
Photograph from Ramírez-Bautista et al. 2013

Chersodromus rubriventris, the Redbelly Earth Runner, was discovered in a cloud forest in San Luis Potosí, Mexico, just after the end of World War II and described a few years later by American herpetologist and spy Edward H. Taylor, who also used his biology as a cover for work in the Philippines, Russia, and Sri Lanka during both world wars. Two other specimens, one from the late 1960s and the other from the early 1980s, were known, but in 2013, a team of herpetologists from the Universidad Autónoma del Estado de Hidalgo found three individuals in a cloud forest in nearby Hidalgo, doubling the number of specimens and photographing the snake alive for the first time. Stomach contents included beetle larvae and ants, both of which are unusual prey for a dipsadid snake.

Atractus wagleri
Photograph from Passos & Arredondo 2009

The genus Atractus, a group of burrowing snakes found from Panama to Argentina, is the most diverse alethinophidian snake genus, with over 130 species, most of which are only known from a few specimens. Recently Paulo Passos of the Brazilian National Museum matched up several previously mis- or unidentified Atractus specimens in South American museums with their species, constituting rediscoveries of sorts. For example, Wagler's Ground Snake (Atractus wagleri) was described in 1945 from a single specimen from western Colombia, and that specimen was lost in a fire in 1948. In 2009 Passos located three additional specimens of this poorly known snake in museums in Colombia. Another species, the Modest Ground Snake (Atractus modestus), was described in 1894 by the great Belgian zoologist George Boulenger, from a single specimen from western Ecuador. In 2007 Passos located more specimens in Ecuadorian museums, expanding the range of the species across most of the country. Although species of Atractus are seemingly quite rare, occurring at high elevations and having secretive fossorial habitats, a large number of Atractus specimens remain misidentified or unidentified in herpetological collections, so our knowledge of these snakes stands to improve dramatically as these are examined and described.

Argus Snail Sucker (Sibon argus)

The Lichen-coloured or Argus Snail Sucker (Sibon argus) is an extremely slender arboreal dipsadine snake with eye-like ("ocellate") spots. It was originally described from a single specimen from southeastern Costa Rica in 1876, by renowned paleontologist Edward Drinker Cope (who feuded with O.C. Marsh in the "Bone Wars" over who could discover more dinosaurs, the subject of an upcoming film starring Steve Carrell as Cope). The validity of the species was uncertain because of the subsequent description of other gracile snakes with ocellated patterns from the same region. In his classic revision of Neotropical snail- and slug-eating snakes, James Peters suggested that Cope's specimen might be aberrant, or perhaps that it represented one half of a species with strong sexual dimorphism (which is rare in snakes), because the only known S. argus specimen was a male, and another species, Sibon longifrenis, was known at the time from just two specimens, both females. Males and females of the same species had been described as separate species before. Ultimately, Peters decided that the two species were probably different, and he was proven right in 1992, when tropical herpetologist Jay Savage was preparing his opus on Costa Rican herpetofauna. Savage discovered both male and female specimens that best matched Cope's 1876 S. argus in the collections of the University of Kansas and the Universidad de Costa Rica. The snakes had been collected in evergreen forests in Panama and Costa Rica, near the type locality of S. argus. With Roy McDiarmid, Savage redescribed the species, which has become much more well-known since. A recent study by Julie Ray and colleagues documented a more diverse diet for this species than previously expected, including other gooey prey such as oligochaete worms and frog eggs. Unfortunately for Sibon argus, both of these prey types are in decline in the neotropics, the worms due to overcollection of their bromeliad homes for horticulture, and the amphibians due to the devastating effects of the amphibian chytrid fungus Batrachochytrium dendrobatidis.

Brygophis coulangesi
Photograph from Andreone & Raxworthy 1998

Other examples of rediscovered snakes abound. The Uluguru Worm Snake (Letheobia uluguruensis) was described from four specimens collected in 1926 from the Uluguru Mountains of eastern Tanzania, a mountain range with dozens of endemic species, and was not seen again until 2004, when four were dug up by local people employed by a group of herpetologists from the London Natural History Museum and the University of Glasgow to search for caecilians. Another blindsnake, Typhlops tasymicris, was rediscovered on Union Island, St. Vincent and the Grenadines, in 2010. An entire genus of blindsnake, Xenotyphlops, was rediscovered in Madagascar, in 2007, 102 years after it's description. A rare sea snake, Hydrophis parviceps, was originally collected by the Danish research vessel Dana and described in 1935 and was seen again only once in 1960 until three turned up in fisheries bycatch off of Vietnam in 2001. Another species of rare sea snake, H. bituberculatus, was rediscovered off Sri Lanka in the late 1980s, over 100 years after the first one was collected (although the fishermen who collected the specimen were so secretive that they refused to divulge the location). One of the rarest snakes in Madagascar, a slow-moving reddish-orange species called Brygophis coulangesi, was first collected in 1968, when one fell from a tree and vomited up a chameleon, with a second specimen found on a cloudy, rainy night during a rain forest survey in 1998, over 300 miles to the north of the first. A second specimen of another Malagasy lamprophiid, Alluaudina mocquardi, was discovered in a pitch-black cave in northern Madagascar in 1982, 50 years after the first was found in a different cave nearby. I don't think any more have been found since, so this one should be getting ready to be rediscovered again soon (edit: City University of New York snake biologist Frank Burbrink informed me that on his recent trip to Madagascar they turned up an Alluaudina mocquardi in tsingy rock at Ankarana - see photo here)!

March 2010 Herp. Review cover
featuring Crotalus lannomi

A high-profile rediscovery graced the cover of the March 2010 issue of the journal Herpetological Review, which featured a photograph of a long-sought-after species of rattlesnake, the Autlán Long-tailed Rattlesnake (Crotalus lannomi). Discovered in the summer of 1966 by Joseph Lannom, C. lannomi became sort of a “holy grail” of rattlesnakes in the decades that followed, as numerous herpetologists ventured into the mountains of western Jalisco in search of it. They were stymied by heavy fog and dangerous flooding, roads with treacherous curves and highway robberies, and drug-related violence. In 2008, five specimens of C. lannomi were found in the foothills of Colima, roughly 50 km from the type locality in Jalisco, in some of Mexico's most pristine forest habitat.

Although most of this was new to me, I've actually written about a different rediscovered viper before, the Spider-tailed Adder (Pseoducerastes urarachnoides) of Iran, which was discovered in 1968 and was at first thought to have either a tumor, a congenital defect, or a growth caused by a parasite, or maybe a spider clinging to its tail (turns out its tail is modified into a lure to attract spider-eating birds). Also, in one of my first articles, I wrote about the South Florida Rainbow Snake (Farancia erytrogramma seminola), described by Wilfred T. Neill in 1964 from Fisheating Creek in Glades County near Lake Okeechobee, Florida, and presumed extinct, never seen again since. To the best of my knowledge this subspecies has yet to be rediscovered, despite a $500 reward from the Center for Snake Conservation and Center for Biological Diversity. (Edit: a diligent reader reminded me that I also wrote about another snake that hasn't been seen since 1975 in one of my earliest articles, the Round Island Burrowing Boa, Bolyeria multocarinata).

Undoubtedly there are numerous snake species left to be discovered and rediscovered, and in many cases almost nobody's out there looking. The Reptile Database has predicted that the total number of described reptile species will surpass 10,000 in 2014, and that non-avian reptiles will perhaps eclipse birds in diversity soon after that. With snakes currently at 3,466, representing just over one third of reptiles, maybe you will be the next to rediscover a snake thought lost!

ACKNOWLEDGMENTS

Thanks to Dan Mulcahy and Don Filipiak for the use of their photographs.

REFERENCES

Andreone, F. and C. Raxworthy. 1998. The colubrid snake Brygophis coulangesi (Domergue 1988) rediscovered in north-eastern Madagascar. Tropical Zoology 11:249-257 <link>

Beebe, CW. 1938. Zaca Venture. Harcourt, Brace and Co. Inc., New York <link>

Cope, E. D. 1875. On the batrachia and reptilia of Costa Rica : With notes on the herpetology and ichthyology of Nicaragua and Peru. Journal of the Academy of Natural Sciences Philadelphia 2:93-157 <link>

Gower, D. J., S. P. Loader, and M. Wilkinson. 2004. Assessing the conservation status of soil‐dwelling vertebrates: Insights from the rediscovery of Typhlops uluguruensis (Reptilia: Serpentes: Typhlopidae). Systematics and Biodiversity 2:79-82 <link>

Lanza, B. 1990. Rediscovery of the Malagasy colubrid snake Alluaudina mocquardi Angel 1939. Tropical Zoology 3:219-223 <link>

Mulcahy, D. G., J. E. Martínez-Gómez, G. Aguirre-León, J. A. Cervantes-Pasqualli, and G. R. Zug. 2014. Rediscovery of an endemic vertebrate from the remote Islas Revillagigedo in the eastern Pacific Ocean: The Clarión Nightsnake lost and found. PLoS ONE 9:e97682 <link>

Mulcahy, D. G. and J. R. Macey. 2009. Vicariance and dispersal form a ring distribution in nightsnakes around the Gulf of California. Molecular Phylogenetics and Evolution 53:537-546 <link>

Murphy, J. C., T. Chan-Ard, S. Mekchai, M. Cota, and H. K. Voris. 2008. The rediscovery of Angel’s Stream Snake, Paratapinophis praemaxillaris Angel, 1929 (Reptilia: Serpentes: Natricidae). The Natural History Journal of Chulalongkorn University 8:169-183 <link>

Passos, P. and J. C. Arredondo. 2009. Rediscovery and redescription of the Andean earth-snake Atractus wagleri (Reptilia: Serpentes: Colubridae). Zootaxa 1969:59-68 <link>

Passos, P., D. F. Cisneros-Heredia, and D. Salazar-V. 2007. Rediscovery and redescription of the rare Andean snake Atractus modestus. The Herpetological Journal 17:1-6 <link>

Peters, J. A. 1960. The snakes of the subfamily Dipsadinae. Miscellaneous Publications of the Museum of Zoology, University of Michigan 114:1-228 <link>

Ramírez-Bautista, A., C. Berriozabal-Islas, R. Cruz-Elizalde, U. Hernández-Salinas, and L. Badillo-Saldaña. 2013. Rediscovery of the snake Chersodromus rubriventris (Squamata: Colubridae) in cloud forest of the Sierra Madre Oriental, México. Western North American Naturalist 73:392-398 <link>

Rasmussen, A. R. 1992. Rediscovery and redescription of Hydrophis bituberculatus Peters, 1872 (Serpentes: Hydrophidae). Herpetologica 48:85-97 <link>

Rasmussen, A. R., J. Elmberg, K. L. Sanders, and P. Gravlund. 2012. Rediscovery of the rare sea snake Hydrophis parviceps Smith 1935: identification and conservation status. Copeia 2012:276-282 <link>

Ray, J. M., C. E. Montgomery, H. K. Mahon, A. H. Savitzky, and K. R. Lips. 2012. Goo-eaters: Diets of the Neotropical snakes Dipsas and Sibon in central Panama. Copeia 2:197-202 <link>

Reyes-Velasco, J., C. I. Grünwald, J. M. Jones, and G. N. Weatherman. 2010. Rediscovery of the rare Autlán Long-tailed Rattlesnake, Crotalus lannomi. Herpetological Review 41:19-25 <link>

Rodríguez, M. J. R., E. J. Bentz, D. P. Scantlebury, R. R. John, D. P. Quinn, J. S. Parmerlee Jr, R. W. Henderson, and R. Powell. 2011. Rediscovery of the Grenada Bank endemic Typhlops tasymicris (Squamata: Typhlopidae). Journal of Herpetology 45:167-168 <link>

Savage, J. M. and R. W. McDiarmid. 1992. Rediscovery of the Central American colubrid snake, Sibon argus, with comments on related species from the region. Copeia 1992:421-432 <link>

Taylor, E. H. 1949. A preliminary account of the herpetology of the state of San Luis Potosí, Mexico. University of Kansas Science Bulletin 33:169-215 <link>

Wallach, V., V. Mercurio, and F. Andreone. 2007. Rediscovery of the enigmatic blind snake genus Xenotyphlops in northern Madagascar, with description of a new species (Serpentes: Typhlopidae). Zootaxa 1402:59-68 <link>

Weaver, R. E. 2010. Activity Patterns of the Desert Nightsnake (Hypsiglena chlorophaea). The Southwestern Naturalist 55:172-178 <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.

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You've probably seen it before - a snake extends its forked tongue, waves it around rapidly, then retracts it. Creepy, right? What do they do that for anyway? Theories explaining the forked tongues of snakes are many and ancient. Aristotle reasoned that it provided snakes with "a twofold pleasure from savours, their gustatory sensation being as it were doubled". 17th century Italian astronomer Giovanni Hodierna thought snake tongues were for cleaning dirt out of their noses. Several writers in the 1600s claimed to have watched snakes catch flies or other animals between the forks of their tongues, using them like forceps. It is a common myth even today that snakes can sting you with their tongues. Watch this video to convince yourself that none of those hypotheses is likely:

A Southern Pacific Rattlesnake (Crotalus oreganus helleri)
touching its tongue tips to the ground

Actually, Aristotle probably got it the closest, as we'll see. Over the last 20 years, members of the laboratory of Kurt Schwenk, a University of Connecticut ecologist and evolutionary biologist, have published a great deal of interesting research on the function of snake tongues. Most animals with tongues use them for tasting, to clean themselves or others, or to capture or manipulate their prey. A few, including humans, also use them to make sounds. Snakes do not use their tongues for any of these things, although they come closest to tasting. A more accurate description of what a snake uses its tongue for is collecting chemicals from the air or ground so that the snake can smell them. By itself, a snake's tongue can neither smell nor taste. Snake tongues have no taste buds. Instead, the tongue is best thought of as a specially-shaped chemical collector. This is because the actual smelling - the conversion of the chemicals into electrical signals sent to the brain by way of receptors - takes place not on the tongue but in the vomeronasal or Jacobson's Organ, which is in the roof of the mouth (and, incidentally, also the name of a pretty sweet band). For a long time everyone thought that the tongue delivered chemicals directly to the Jacobson's Organ, because both the Jacobson's Organ and the pathways that lead to it are paired just like the tips of the tongue. Even this recent Encyclopedia Britannica figure falls victim this assumption (edit: a few days after this article posted, Britannica Earth & Life Science editor John P. Rafferty tweeted me to let me know that they had updated the article, with a new diagram to follow soon). In fact this is, as Schwenk put it, a red herring.

Instead, x-ray movies have revealed that the tongue does not move inside the closed mouth, but that each side of the tongue deposits the chemicals it has collected onto pads on the floor of the mouth (called the anterior processes of the sublingual plicae, in anatomical jargon) as the mouth is closing. It is most likely these plicae that deliver the sampled molecules to the entrance of the Jacobson's Organ (the vomeronasal fenestrae) when the floor of the mouth is elevated to come into contact with the roof following a tongue flick. Further evidence for this heretical notion is that geckos, skinks, and other lizards lack deeply-forked tongues but deliver chemicals to their vomeronasal organs just fine, and in fact so do turtles and many mammals and amphibians (although in none of these groups is the Jacobson's Organ as well-developed as in squamates).

Cross-sectional structure of one half of the Jacobson's Organ,
including the sensory epithelium, lumen, and mushroom body
From Døving & Trotier 1998

Because it is forked, the tongue of a snake can collect chemical information from two different places at once, albeit places that are fairly close together by human standards. Snakes often spread the tips of their tongues apart when they are extended, sometimes to a distance twice as wide as their head. This is significant because it allows them to detect chemical gradients in the environment, which gives them a sense of direction - in other words, snakes use their forked tongues to help them smell in 3-D. Owls use their asymmetrical ears in this way. Snakes and owls use similar neural circuitry to compare the signal strength delivered from each side of the body and determine the direction that a smell or a sound is coming from. (Humans do this with our hearing too, but we're not as good at it). This ability makes it possible for snakes to follow trails left by their prey or by potential mates. In the 1930s, before guidelines on the ethical use of animals in research were as strict, German biologist Herman Kahmann experimentally removed the forked part of snakes' tongues and found that they could still respond to smells, but that they had lost their ability to follow scent trails.¹ Later experiments used the more humane method of blocking the entrance to the Jacobson's Organ on one side and found that these snakes turned in a circle toward the unblocked side when they tried to follow a trail (although one recent experiment that severed the vomeronasal nerve on one side did not support this hypothesis).

Male (left) and female (right)
Copperhead tongue
Figure from Smith et al. 2008

In the 1980s, snake biologist Neil Ford watched how male garter snakes used their tongues when they were following pheromone trails left behind by females. He found that if both tips of the male snake's tongue fell within the width of the trail, the snake continued slithering straight ahead. However, when one tip or the other fell outside the edge of the trail, the snake turned his head away from that tip and back towards the pheromone trail, and his body followed. Following this simple rule allowed the snakes to perform trail-following behavior that was both accurate and directed. If both tongue tips ever touched the ground outside of the trail, the male would stop and swing his head back and forth, tongue-flicking, until he relocated the trail. Snake ecologist Chuck Smith found evidence that male Copperheads have longer, more deeply-forked tongues than females, which presumably enhances their ability to find mates. Although sexual dimorphism is rare in snakes, differences in tongue size are likely to be present other species as well. Scent-trailing is probably also quite helpful to snakes tracking down prey, including for sit-and-wait predators like vipers, which have evolved smelly but non-toxic venom components, about which I've written before, to help them relocate bitten and envenomated prey items. Many lizards that are active hunters also have deeply forked tongues which they spread apart when tongue-flicking, whereas lizards such as geckos and iguanids are mostly either ambush predators or herbivores and have blob-like tongues. Whether following mate or prey, how snakes and lizards determine that they are following the scent trail in the right direction is unknown.

Different types of tongue flicks
From Daghfous et al. 2012

When following a scent-trail, snakes simply touch their tongue tips down to the ground to pick up the chemical information lying there (top panel, left). But snakes can also use a different type of tongue-flick (bottom two panels) to sample airborne chemicals. Snakes often wave their tongues in the air without putting them in contact with anything. The tongue creates self-reinforcing air vortices. Vortices formed in the water by boats drift away from the boat as they form. Bill Ryerson, another student in the Schwenk lab, found that the vortices created in the air by snake tongues have a special property - they do not drift away but rather stay in the vicinity of the tongue, where they can be sampled repeatedly as the tongue skirts the part of each vortex where the air velocity is the highest. Oscillating tongue-flicks are unique to snakes. They usually last 2-3 times longer and can sample 100 times as much air as the simple downward extension of the tongue. The tongue then transfers these molecules to the Jacobson's Organ via the same route described above. Evidence suggests that male Copperheads can also find females using oscillating tongue-flicks to detect airborne pheromones, although the details of how they determine direction using such dispersed and transient odors are poorly understood. We have much to learn about this incredibly advanced sensory system and the role it has played in the evolutionary success of snakes.

1 : Before you lambaste Kahmann too badly, you should also know that he supported his part-Jewish University of Munich colleague Karl von Frisch, who later went on to share the 1973 Nobel Prize in Physiology or Medicine for his discovery of honeybee communication, against Hitler's regime.^↩

ACKNOWLEDGMENTS

Thanks to Bill Ryerson for giving such an engaging talk at SICB 2014 and for talking with me after, so that I was inspired to research and write this piece, and to JustNature and Zack Podratz for allowing me to use their photographs and videos.

REFERENCES

Berkhoudt, H., P. Wilson, and B. Young. 2001. Taste buds in the palatal mucosa of snakes. African Zoology 36:185-188 <link>

Daghfous, G., M. Smargiassi, P.-A. Libourel, R. Wattiez, and V. Bels. 2012. The function of oscillatory tongue-flicks in snakes: insights from kinematics of tongue-flicking in the Banded Water Snake (Nerodia fasciata). Chemical Senses 37:883-896 <link>

Døving, K. B. and D. Trotier. 1998. Structure and function of the vomeronasal organ. Journal of Experimental Biology 201:2913-2925 <link>

Ford, N. B. 1986. The role of pheromone trails in the sociobiology of snakes. Pages 261-278 in D. Duvall, D. Muller-Schwarze, and R. M. Silverstein, editors. Chemical Signals in Vertebrates, Vol 4. Plenum, New York <link>

Gove, D. 1979. A comparative study of snake and lizard tongue‐flicking, with an evolutionary hypothesis. Zeitschrift für Tierpsychologie 51:58-76 <link>

Halpern, M. and S. Borghjid. 1997. Sublingual plicae (anterior processes) are not necessary for garter snake vomeronasal function. Journal of Comparative Psychology 111:302-306 <link>

Parker, M. R., B. A. Young, and K. V. Kardong. 2008. The forked tongue and edge detection in snakes (Crotalus oreganus): an experimental test. Journal of Comparative Psychology 122:35-40 <link>

Schwenk, K. 1994. Why snakes have forked tongues. Science 263:1573-1577 <link>

Smith, C. F. 2007. Sexual dimorphism, and the spatial and reproductive ecology of the copperhead snake, Agkistrodon contortrix. PhD Dissertation. University of Connecticut <link>

Smith, C., K. Schwenk, R. Earley, and G. Schuett. 2008. Sexual size dimorphism of the tongue in a North American pitviper. Journal of Zoology 274:367-374 <link>

Ryerson, W. G. and K. Schwenk. 2012. A simple, inexpensive system for digital particle image velocimetry (DPIV) in biomechanics. Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 317:127-140 <link>

Young, B. A. 1990. Is there a direct link between the ophidian tongue and Jacobson's organ? Amphibia-Reptilia 11:263-276 <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.

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An adult male Taricha granulosa in breeding condition.
There is enough tetrodotoxin in this newt to kill you
and about 29 other people.

Gartersnakes eat newts. I mentioned this remarkable fact in my article on the Scientific American Guest Blog, but it's interesting enough to warrant a more detailed treatment. In 1990, Edmund D. Brodie III and his father, Edmund D. Brodie Jr, published a paper in the journal Evolution that provided the first evidence of a pair of species in a highly coupled arms race. Previously, the concept of an arms race had been criticized because the potential cost to the prey (loss of life) was perceived as more dire than the potential cost to the predator (merely the loss of dinner). This imbalance, known as the life-dinner principle, led scientists to suggest that tightly co-evolving arms races between predators and prey could not exist, because selection pressure on the predator would always be less than that on the prey. However, reasoned Brodie & son, if the prey's defenses are lethal, then selection might be equally strong on both predator and prey, because only highly resistant predators could survive a predation event. This is the case in the predator-prey dynamic between the Rough-skinned Newt (Taricha granulosa) and the Common Gartersnake (Thamnophis sirtalis), which is centered around a toxin called tetrodotoxin.

Chemical structure of tetrodotoxin

Tetrodotoxin is a very interesting chemical. James Bond was poisoned with it at the end of From Russia with Love (and saved by an antidote, which does not exist in real life). It's responsible for the tingling sensation caused by eating properly prepared fugu (and woe betide those who consume this Japanese pufferfish dish improperly prepared). Named after the pufferfish family, it is found in a wide variety of organisms, from flatworms to the blue-ringed octopus, its biological origins are enigmatic. Many species are thought to sequester it from symbiotic bacteria, although some, including newts, are believed to be capable of synthesizing it themselves. In the lab, tetrodotoxin is created under conditions of extreme heat and pressure, and how this molecule is generated inside of living cells is a mystery. Furthermore, it is an extremely potent poison: tetrodotoxin binds to and occludes the extracellular pore of voltage-gated ion channels embedded in muscle cell membranes, preventing the flow of sodium ions into the cell and interrupting the action potentials necessary for muscle contraction. This is not unlike the effect produced by local anesthetics, which also block sodium channels, but with two important differences: they do so from the inside of the cell and their effects are reversible.

Map of gartersnake resistance to tetrodotoxin
Outside of the range of the Rough-skinned Newt,
gartersnakes have essentially no resistance.
Figure from Brodie Jr. et al 2002

The elder Brodie showed in 1968 that many predators died if they were forced to eat newt, including bobcats, herons, kingfishers, moles, weasels, bass, catfish, and most snakes, including racers, rattlesnakes, gophersnakes, whipsnakes, rubber boas, and sharp-tailed snakes. Notably, Common Gartersnakes survived, although they were temporarily incapacitated. Brodie realized that he could measure snake toxin resistance by timing how long a snake was incapacitated for or how much its crawling speed slowed down when it was given a standardized dose of tetrodotoxin. Using this method for measuring resistance, the Brodies demonstrated that newt toxicity and gartersnake toxin resistance co-vary predictably across most of the Pacific Northwest; for example, on Vancouver Island, newts have very low levels of TTX and gartersnakes have almost no resistance to the toxin, whereas in central Oregon and in California's San Francisco Bay area, newts are tens of thousands of times more toxic and gartersnakes have correspondingly high resistance (for the most part, but read on!).

Three species of TTX-resistant snakes:
top: Amphiesma pryori
middle: Erythrolamprus epinephelus
bottom: Rhabdophis tigrinus

It's now known that a number of different snake species are resistant to tetrodotoxin and are capable of eating newts and other TTX-laden prey with impunity. These include two other species of gartersnake, the Santa Cruz gartersnake (Thamnophis atratus), which also eats Rough-skinned Newts, and the aquatic garter snake (Thamnophis couchii), which preys on California Newts (Taricha torosa). A Japanese newt, Cynops ensicauda, is eaten by Pryer's Keelback (Amphiesma pryeri). Some frogs also have tetrodotoxin, and two species, an Atelopus toad in Central American and a Polypedates treefrog in eastern Asia, are respectively eaten by the dipsadineErythrolamprus [Liophis] epinephelus and the natricine Rhabdophis tigrinus. Not only has tetrodotoxin resistance also arisen in these other species of snakes around the world, but the mechanism, which involves changing the shape of the sodium channel pore so that the toxin binds less tightly, has evolved the exact same way in each lineage of snakes, via functionally identical mutations to the gene sequences. This is remarkable because these snakes are moderately but not very closely related to one another, and even more so because pufferfish also have many of the same mutations. These mutations are not found in humans, rats, most snakes, or other non-resistant vertebrates. All this suggests that there are a limited number of ways that evolution can change a sodium channel to make it more resistant to TTX and still maintain its function. In most cases, these and other natricine and dipsadine snakes are probably resistant to multiple prey toxins, as they are known to regularly consume other toxic amphibians and invertebrates.

Common Gartersnake (Thamnophis sirtalis)
from Oregon's Willamette Valley, where newt toxicity and
snake resistance are both at their peak

Although all newts and some other amphibians possess TTX, T. granulosa is many times more toxic than any other species, and its primary predator is many times more resistant than any other snake. Common Gartersnakes themselves actually retain sufficient quantities of newt-derived TTX in their liver for one to two months after eating newts to severely incapacitate or kill their predators, which was the general subject of my original article. Whether or not any of the other TTX-resistant species sequester the toxin remains unknown, although it seems likely. In a few places, Common Gartersnakes have evolved such high resistance to TTX that they have effectively "won" their arms race with their newts. Because snake TTX resistance apparently evolves in a stepwise fashion, with each new mutation to the snake sodium channel pore structure rapidly making it much tougher for TTX to bind tightly, gartersnakes are capable of making quicker leaps in the arms race than are newts, which presumably must evolve higher toxicity by increasing the amount of TTX they produce. Eventually, some gartersnakes seem to have reached a point where no amount of TTX could incapacitate them, so their newt populations (which were already pretty toxic) stopped being selected to produce more toxin. Since we don't really know how they get their toxin in the first place, they might be limited in their ability to produce or sequester it or its precursors.

There's much left to discover about this system, which is perhaps one of the most interesting in snake biology. Where are newts getting tetrodotoxin from? How many other times has TTX resistance evolved in snakes, and has it happened the same way every time? To what extent are gartersnakes using newt-derived TTX to protect against their own predators? Someday, we will find out.

ACKNOWLEDGMENTS

Thanks to current and former members of the Brodie lab, especially Dr. Edmund D. "Doc" Brodie Jr., for discussing this system with me over the last three years.

REFERENCES

Brodie Jr, E. D. 1968. Investigations on the skin toxin of the adult rough-skinned newt, Taricha granulosa. Copeia 1968:307-313 <link>

Brodie III, E. and E. Brodie Jr. 1999. Costs of exploiting poisonous prey: evolutionary trade-offs in a predator-prey arms race. Evolution 53:626-631 <link>

Brodie III, E., C. Feldman, C. Hanifin, J. Motychak, D. Mulcahy, B. Williams, and E. Brodie Jr. 2005. Parallel arms races between garter snakes and newts involving tetrodotoxin as the phenotypic interface of coevolution. Journal of Chemical Ecology 31:343-356 <link>

Geffeney, S., E. Brodie Jr, P. Ruben, and E. Brodie III. 2002. Mechanisms of adaptation in a predator-prey arms race: TTX-resistant sodium channels. Science 297:1336-1339 <link>

Geffeney, S., E. Fujimoto, E. Brodie, and P. Ruben. 2005. Evolutionary diversification of TTX-resistant sodium channels in a predator–prey interaction. Nature 434:759-763 <link>

Hanifin, C. T. and E. D. Brodie Jr. 2008. Phenotypic mismatches reveal escape from arms-race coevolution. PLoS Biology 6:e60 <link>

Feldman, C. R., E. D. Brodie, and M. E. Pfrender. 2012. Constraint shapes convergence in tetrodotoxin-resistant sodium channels of snakes. Proceedings of the National Academy of Sciences 106:13415-13420 <link>

Stokes, A. N., P. K. Ducey, L. Neuman-Lee, C. T. Hanifin, S. S. French, M. E. Pfrender, E. D. Brodie, III, and E. D. Brodie Jr. 2014. Confirmation and distribution of tetrodotoxin for the first time in terrestrial invertebrates: two terrestrial flatworm species (Bipalium adventitium and Bipalium kewense). PLoS ONE 9:e100718 <link>

Williams, B. L. and R. L. Caldwell. 2009. Intra-organismal distribution of tetrodotoxin in two species of blue-ringed octopuses (Hapalochlaena fasciata and H. lunulata). Toxicon 54:345-353 <link>

Williams, B. L., E. D. Brodie Jr., and E. D. Brodie III. 2004. A resistant predator and its toxic prey: persistence of newt toxin leads to poisonous (not venomous) snakes. Journal of Chemical Ecology 30:1901-1919 <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.

Arafura Filesnake (Acrochordus arafurae)

In the swamps, marshes, streams, and estuaries of northern Australia and southeastern Asia live ancient snakes as thick as your arm, with tongues as thin as a thread, skin as rough as a file, and a disposition as gentle as a lamb. These snakes comprise the family Acrochordidae (from the Greek akrochordon, wart), and are known as filesnakes¹, wartsnakes, or elephant trunksnakes. In Indonesian they are known as karung, which means 'sack'; in Thai, as ngū nguang-cĥāng, 'elephant-trunk snake'. There are three species, all in the genus Acrochordus: Javan (A. janavicus), Arafura (A. arafurae), and Little (A. granulatus). The largest, female Javans, grow up to 8 feet and over 20 pounds. Acrochordids are an old and highly distinct group of snakes, distantly related to colubroids, with which they share a common ancestor between 50 and 70, but possibly as long as 90 million years ago.

Close-up of A. arafurae scales

Filesnakes have strongly-keeled scales with the texture of sandpaper or a coarse file, after which they are named. They have very loose, baggy skin. I held one once and it felt like a human arm inside the sleeve of a very sturdy, very baggy rain poncho made out of chain mail. This loose skin is likely an adaptation that allows filesnakes to withstand the great force of the initial dash for freedom of their fish prey. Their sharp scales are used to help gain purchase on slimy fish skin during constriction. They have sensory, bristle-bearing tubercles on the skin between their scales, as well as sensory organs on the scales themselves, both of which presumably help them sense the underwater movements of nearby prey, analogous to the lateral line systems of fishes and some amphibians. Acrochordids sometimes ambush their prey, but more often they forage by searching slowly along the edges of mangroves, billabongs, and other water bodies at night, looking for sleeping fishes and crustaceans (although they don't tear them apart like some southeast Asian snakes). During the day, filesnakes hide in the shadows of overhanging trees, moving with them to remain concealed from predatory birds. They are nearly incapable of moving on land, and shed in the water using a knotting behavior similar to that of Pelamis platurus, the most completely aquatic sea snake.

Acrochordus arafurae regurgitates
an eel-tailed catfish (Tandanus tandanus)
whose spine has pierced its neck

Filesnakes occupy a unique phylogenetic position, not closely related to anything but somewhere in-between the colubroids ("advanced snakes") and the "henophidians" (boas, pythons, and other stem-group snakes). A few recent papers reanimate an old hypothesis that they might be closely related to dragonsnakes, but historically acrochordids have been considered the sister group to all colubroids, a group of >2,850 species (>80% of all living snakes) that includes dragonsnakes, asymmetrical slug-eaters, vipers, homalopsids, elapids, lamprophiids, and strict colubrids. Colubroidea and the three Acrochordus species together form the Caenophidia ("recent snakes"). Acrochordids share unspecialized head scales and undifferentiated ventral scales with boas and pythons, but they are united with colubroids in that they totally lack vestigial limbs and have spines on their hemipenes, a well-developed vomeronasal system, and several particular characteristics of skull morphology, including a coronoid bone. Other features of the skull and skeleton are unique to acrochordids, including the aforementioned skin sense organs, a passive joint between the frontal and parietal skull bones, the presence of certain holes in the vertebrae, the shape of the head of the ribs, and an ear region that most closely resembles the ears that other snakes have as embryos, but which forms in a different way. Acrochordids also have an unusual lung morphology, with a double row of holes leading from the trachea into individual small lunglets, and a more tangled intestinal tract than other snakes.

Acrochordus granulatus with algae growing on its back

Filesnakes have incredibly low metabolic rates, even for a snake, and cannot sustain rigorous physical activity for very long. In captivity, they "epitomize sluggishness in snakes", although radio telemetry has shown that in the wild they move around wetlands slowly but steadily, covering up to 450 feet per night. They can remain submerged for over an hour (record 2 h 20 min), and surface to take about 5 breaths, about one per minute. The first several of these breaths oxygenate the blood, and the last one fills the multi-chambered lung. In addition, Little Filesnakes have about twice as much blood as other snakes, and this voluminous blood is about twice as thick with red blood cells as even that of other diving snakes. Their hemoglobin has a very high affinity for oxygen, which results in their being able to store between three and fifteen times as much oxygen in their blood as a similarly-sized sea snake, and release it slowly over a long period of time. Many turtles also use this strategy. Also like turtles, filesnakes can both obtain oxygen from and release acidic carbon dioxide into the water through their skin, which helps prolong their dives.² In fact, filesnakes are so well-adapted to sitting still that they are practically incapable of exercise, and get tired out quickly.

This slow theme carries over into filesnake life history. Male filesnakes mature around six years old, females around nine, and 8-10 years may elapse between consecutive births. Studies from northern Australia found that only a small proportion of females are reproductive in any given year, and that only the very largest females reproduce relatively frequently. Large Javan Filesnakes give birth to as many as 52 young at once, although the average is closer to 30. Arafura Filesnakes average about 16 (as few as 9 and as many as 25 have been reported), and Little Filesnakes about 6 (as few as 1 and as many as 12). Female filesnakes are courted by up to eight males at a time in shallow water. Their population dynamics are driven by rainfall in northern Australia. One captive filesnake gave birth to a single young after seven years of isolation, suggesting that filesnakes are either capable of parthenogenesis or of very prolonged sperm storage.

The Little Filesnake (Acrochordus granulatus) has
a banded pattern like a sea krait (Laticauda colubrina)

At first glance the three extant Acrochordus species seem quite similar, but in fact they exhibit striking differences in both anatomy and ecology. The Little Filesnake (Acrochordus granulatus) was described in 1799 and used to be classified in a separate, monotypic genus (Chersydrus). As its name suggests, it is the smallest acrochordid (~ 3 feet in total length) and the most widely distributed. It is found along the coast from northwestern India throughout southeast Asia and Indonesia, reaching east to the Solomon Islands. Its diverse habitats include freshwater lakes, rivers, mangroves, mudflats, reefs, and the open ocean, up to 6 miles offshore and over 60 feet deep. It is the most marine of the filesnakes, the most brightly patterned, and has a shorter, more laterally-compressed tail, more granular scales, more dorsally-oriented nostrils, and a salt excretion gland beneath its tongue.³

Acrochordus javanicus

The Javan Filesnake (Acrochordus javanicus) was the first to be described, in 1787, and is the largest and heaviest filesnake, sometimes reaching 8 feet and over 20 pounds. It is found in fresh and brackish water on the Malay Peninsula and on the islands of Sumatra, Java, and Borneo (and was introduced to Florida in the 1980s, although it does not appear to have established there). It is harvested for meat and for its skin, out of which is made fine leather; up to 2 million are exported from Indonesia annually. Unlike other filesnakes, the posterior-most teeth in its lower jaw have sharp edges. The Arafura Filesnake (Acrochordus arafurae) was thought to be the same species as the Javan until 1979. It grows as long but at the same size is only about half as heavy-bodied. It is found only in freshwater habitats in northern Australia and southern New Guinea. Surprisingly, A. arafurae is more closely related to A. granulatus than either is to A. javanicus, a relationship that is supported by genetics as well as morphology.

The long, thin tongue of Acrochordus javanicus
From Greene (1997)

Fossil Acrochordus have been found in Pakistan and Nepal, as well as within the extant range. These extinct filesnakes date from 5-20 million years ago during the Miocene, only a few million years after the Indian plate crashed into Asia to form the Himalayas. They grew larger than modern filesnakes, reaching at least 9 feet, and are the most well-represented snakes in the southern Asian fossil record, possibly because their habitat lends itself well to fossilization. The extinct species Acrochordus dehmi is represented by over 1000 fossils from over 100 different locations, and probably went extinct about 6 million years ago. Because it is so well-known, we can say with confidence that it is more closely related to A. javanicus than to the other two living species of Acrochordus. Molecular clock methods suggest that the three modern species of Acrochordus and A. dehmi diverged from one another 16-20 million years ago, a timescale that usually justifies separation into family-level or higher categories. Despite their superficial similarities, the ecological and morphological differences among the three living Acrochordus species have been considered equivalent to differences among genera in other groups of snakes. Because no fossil acrochordids have been found in Australia, it is assumed that they evolved in Asia and spread to Australia in the last 5 million years. It is also likely that the ancestors of the Little Filesnake entered the ocean before sea snakes (~7 mya) and kraits (~13 mya) and just after marine homalopsids (~18 mya).

Acrochordus in contemporary aboriginal artwork by Chris Liddy (Moonggun),
showing the embryos inside the snake in the northern Australian style

One of the most interesting things about filesnakes is that Aboriginal Australians collect and eat them in some areas. Mostly this is done at the end of the Australian dry season, in November, when water levels are lowest and the snakes are easiest to find and capture. Although the snakes themselves don't generally put up much resistance, the old women who hunt them do so by wading into murky waters filled with crocodiles and feel under overhanging banks, weed beds, and logs, sometimes collecting over 30 snakes per person-hour. Often the snakes are killed immediately by biting their necks. The pregnant females are highly prized for their embryos, which are cooked on hot ashes, eaten like popcorn, and called 'cookies' by Aboriginal children.

1 Not to be confused with African Filesnakes (genus Mehelya), which are so-named not for their texture but for their cross-sectional shape, which resembles a triangular file. ^↩

2 Although the warm, shallow, slow-moving waters in which they live are fairly oxygen-poor and oxygen is difficult to extract out of salty water, so augmenting their ability to hold their breath using their massive blood oxygen reservoir is almost certainly of greater importance. ^↩

3 Little Filesnakes can excrete salt but gradually get dehydrated, so they must have a source of fresh water. They drink rain that falls on the ocean or migrate to areas where rivers flow into estuaries. This is because, like other marine reptiles, filesnakes "pee like a fish": they excrete nitrogen as ammonia, rather than as uric acid like other snakes or as urea like mammals. This is much more wasteful of water than the uric acid method, and it's not clear why they do this.^↩

ACKNOWLEDGMENTS

Thanks to Chris Liddy, Matt Summerville, Darryl Houston, M. & P. Fogden, Jordan de Jong, Stephen Zozaya, Jason Isley, and Dick Bartlett for their photos, and to Rick Shine for information on tracking down Darryl Houston.

REFERENCES

Boulenger, G. A. 1893. Catalogue of the snakes in the British Museum (Natural History). Trustees of the British Museum, London <link>

Feder, M. E. 1980. Blood oxygen stores in the file snake, Acrochordus granulatus, and in other marine snakes. Physiological Zoology 53:394-401 <link>

Heatwole, H. and R. Seymour. 1975. Pulmonary and cutaneous oxygen uptake in sea snakes and a file snake. Comparative Biochemistry and Physiology Part A: Physiology 51:399-405 <link>

Houston, D. and R. Shine. 1994. Movements and activity patterns of Arafura filesnakes (Serpentes: Acrochordidae) in tropical Australia. Herpetologica 50:349-357 <link>

Lillywhite, H. B. and T. M. Ellis. 1994. Ecophysiological aspects of the coastal-estuarine distribution of acrochordid snakes. Estuaries 17:53-61. <link>

Lillywhite, H. B., A. W. Smits, and M. E. Feder. 1988. Body fluid volumes in the aquatic snake, Acrochordus granulatus. Journal of Herpetology 22:434-438 <link>

Madsen, T. and R. Shine. 2000. Rain, fish and snakes: climatically driven population dynamics of Arafura filesnakes in tropical Australia. Oecologia 124:208-215 <link>

Magnusson, W. A. 1979. Production of an embryo by an Acrochordus javanicus isolated for seven years. Copeia 1979:744-745 <link>

McDowell, S. B. 1975. A catalogue of the snakes of New Guinea and the Solomons, with special reference to those in the Bernice P. Bishop Museum. Part II. Anilioidea and Pythoninae. Journal of Herpetology 9:1-79 <link>

McDowell, S. B. 1979. A catalogue of the snakes of New Guinea and the Solomons, with special reference to those in the Bernice P. Bishop Museum. Part III. Boinae and Acrochordoidea (Reptilia, Serpentes). Journal of Herpetology 13:1-92 <link>

Intertubercular papilla of Acrochordus granulatus
From Povel & Van Der Kooij 1996

Povel, D. and J. Van Der Kooij. 1996. Scale sensillae of the file snake (Serpentes: Acrochordidae) and some other aquatic and burrowing snakes. Netherlands Journal of Zoology 47:443-456 <link>

Pyron RA, Burbrink F, Wiens JJ, 2013. A phylogeny and revised classification of Squamata, including 4161 species of lizards and snakes. BMC Biology 13 <link>

Rasmussen, A. R., J. C. Murphy, M. Ompi, J. W. Gibbons, and P. Uetz. 2011. Marine Reptiles. PLoS ONE 6:e27373 <link>

Rieppel, O. and H. Zaher. 2001. The development of the skull in Acrochordus granulatus (Schneider)(Reptilia: Serpentes), with special consideration of the otico‐occipital complex. Journal of Morphology 249:252-266 <link>

Sanders KL, Mumpuni, Hamidy A, Jead J, Gower D, 2010. Phylogeny and divergence times of filesnakes (Acrochordus): inferences from morphology, fossils and three molecular loci. Molecular Phylogenetics and Evolution 56:857-867 <link>

Seymour, R., G. Dobson, and J. Baldwin. 1981. Respiratory and cardiovascular physiology of the aquatic snake, Acrochordus arafurae. Journal of Comparative Physiology 144:215-227 <link>

Shine R, 1995. Australian Snakes: A Natural History Ithaca, New York: Cornell University Press <link>

Shine, R. 1986. Sexual differences in morphology and niche utilization in an aquatic snake, Acrochordus arafurae. Oecologia 69:260-267 <link>

Shine, R. 1986. Ecology of a low-energy specialist: food habits and reproductive biology of the arafura filesnake (Acrochordidae). Copeia 10:424-437 <link>

Shine, R. 1986. Predation upon filesnakes (Acrochordus arafurae) by aboriginal hunters: selectivity with respect to body size, sex and reproductive condition. Copeia 10:238-239 <link>

Shine, R. and D. Houston. 1993. Acrochordidae. in C. Glasby, G. Ross, and P. Beesley, editors. Fauna of Australia. AGPS, Canberra <link>

Shine, R., P. Harlow, J. S. Keogh, and Boeadi. 1995. Biology and commercial utilization of acrochordid snakes, with special reference to karung (Acrochordus javanicus). Journal of Herpetology 29:352-360 <link>

Voris, H. K. and G. S. Glodek. 1980. Habitat, diet, and reproduction of the file snake, Acrochordus granulatus, in the straits of Malacca. Journal of Herpetology 14:108-111 <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.

Click here to read this post in Spanish
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Alternate title suggested by David Steen: Why snakes might benefit from holding it

Most people probably spend as little time as possible thinking about poop, especially snake poop. Some animals produce enormous amounts of poop, like dairy cows. Others make lots of little poops - up to 50 a day in small birds. In contrast, snakes don't poop much at all. In fact, because they eat so infrequently, snakes probably poop the least often of almost any animal. Anyone who has kept a snake as a pet can tell you that a few days after they're fed, most snakes tend to poop once (often in their water bowls, for some annoying reason), and they might poop again within a few more days. Like bird poop, snake poop is made up of two parts - the brown stuff (the fecal fragment, aka the actual poop) and the white stuff (the uric acid fragment, aka the pee, in a solid form). Also like birds, most reptiles use uric acid rather than urea to excrete their excess nitrogen, which helps them conserve water.

A young Racer (Coluber constrictor) that has eaten a
Ring-necked Snake (Diadophis punctatus) nearly 92% its length

You wouldn't think there would be much that's interesting about snake poop, but to a snake biologist everything about snakes is interesting. In 2002, Harvey Lillywhite, Pierre de Delva, and Brice Noonan published a chapter in the book Biology of the Vipers that detailed their studies on snake poop. Their most amazing finding was that some snakes can go for a really, really long time without pooping. As in, over a year. It's not because they're constipated though - these long fecal retention periods have actually evolved for a purpose in snakes. Here's what happens: most snakes eat very large meals, and they eat them all in one piece. That means that when a snake eats a meal, its body mass can more than double all at once, and it can only digest that meal from the outside in, because it hasn't chewed or cut it up into small pieces to increase its surface area. Even for the insane digestive tract of a snake, this is an incredible feat.

And the python's small heart grew two sizes that day
Figure from Riquelme et al. 2011

A well-publicized series of studies by Steve Secor and Jared Diamond on snake digestion is more than fascinating enough to warrant some digression. They revealed that some snakes actually let their digestive tracts atrophy between meals, and rebuild them (and many of their other organs, including their hearts, which double in size) each time they eat. If that sounds strange, remember that some snakes only eat a few times a year, unlike we mammals who must eat every day. In one paper on the subject, the authors used an analogy with driving a car in normal traffic vs. stopping at a railroad crossing. It's fine to keep the engine running during a brief stop, but turning the engine off saves fuel while waiting for a train to pass. By shrinking their organs, snakes are saving energy during the long fasts between meals. The flexibility of their body temperature and fundamental differences in their mitochondria are two of the ways in which snakes are able to endure these extreme fluctuations in their metabolic rate. As their gut size and metabolic rate change, so does their ability to uptake nutrients, which brings us back to the production of poop.

Uromacer oxyrhynchus just can't hold it's poop

Poop is what's left behind after your gut has extracted all the nutrients it can from a meal. The ability of a snake's gut to extract nutrients from its prey can change a lot as the gut itself is rebuilt following a meal. Specifically, it is highest following feeding and tapers off as physiology and morphology return to their pre-feeding states. Normally, once food has been reduced to poop, it doesn't hang around for long. This is true in mammals and birds and in some snakes, including ratsnakes, which normally take about two days between eating and pooping. Even that's relatively long compared with we humans, who are clinically constipated after three days. Other relatively slender or arboreal snakes such as bush and tree vipers (3-7 days) and tree pythons (~6 days) poop fairly regularly, and fecal retention time is at a bird-like minimum of 23 hours in the slender Hispaniolan Pointed-nosed Snake (Uromacer oxyrhynchus). But in other snakes, particularly in heavy-bodied species of henophidians and especially in terrestrial vipers, poop stays in the hindgut for months, even when they are fed often. The maximum values recorded by Lillywhite for boas and pythons fed mice are impressive: 76 days in an Emerald Tree Boa (Corallus caninus), 174 days in a Burmese Python (Python molurus), and 386 days in a Blood Python (P. curtus). For vipers, the figures are just as astounding: 116 days for a Puff Adder (Bitis arietans) and 286 for a Rhinoceros Viper (B. nasicornis) are among the longest, although nothing holds a candle to the heavyweight champion: one Gaboon Viper (B. gabonica) in Lillywhite's dataset that didn't poop for 420 days!

A Burmese Python intestine before (top), two days
after (middle), and 10 days after (bottom) eating.
From Secor 2008

The intestine of a snake can hold a lot of poop. Lillywhite & colleagues measured this by pumping (dead) snake intestines full of saline and found that an average viper hindgut can hold about twice as much total volume as that of a ratsnake. The cumulative mass of the poop stored by the vipers in their study totaled between 5 and 20% of the total body mass of the snakes. In humans, this kind of thing would cause an awful, awful death (some say that's what happened to Elvis). Why did these snakes do this? Lillywhite and colleagues put forth what they called the adaptive ballast hypothesis to explain their observations. When I first heard about the adaptive ballast hypothesis, I actually thought it would be that snakes held onto their poop so that they could use it defensively, in case they needed it to spray onto their would-be assailants during some future predation attempt or capture by a herpetologist. But in fact, it goes something like this:

Poop from this African Rock Python's last meal might help anchor it
as it laboriously swallows this wildebeest

Clearly, being heavy is not advantageous for arboreal snakes, so they poop on a regular basis shortly after eating. In terrestrial snakes, however, a little extra weight can give a snake a distinct advantage in capturing and handling large, potentially dangerous prey. Stored feces contribute an easily-altered component to the body's mass, an inert ballast that, unlike muscle, requires no energy to maintain (so long as the animal is sitting still and doesn't have to drag it around, a perfect fit for the sedentary lifestyle of pythons and vipers - no word yet on fecal retention in the sluggish elephant trunksnakes). This extra mass is concentrated in the posterior of the body, where it presumably increases both the inertia of that region and its friction with the ground. Essentially, the humongous mass of poop could anchor the back end of the snake during a strike or while constricting. Although no one has explicitly tested this idea, it's compelling, because the same evolutionary pressures that caused pythons and vipers to have heavy bodies in the first place could be selecting for these long retention times if they help the snakes more easily obtain food. What's more, the snakes could jettison their ballast quickly if it became a liability, such as following a new meal, before undertaking a long-distance movement, upon becoming pregnant, or prior to hibernation, thereby reducing their body mass by as much as 20% at one go.

In addition to providing ballast, the long time the fecal material spends inside the intestine could potentially increase the absorption of nutrients and water, although it probably doesn't take many months before the snake has got all it can out of its old meals. Uric acid and feces are normally mixed in snakes with short passage times, but in heavy-bodied viperids, boids, and pythons, feces are usually more compact and are more separate from the uric acid.

Few people have looked very deeply into these patterns of defecation (perhaps few would want to), so a lot of questions remain: does more frequent activity induce premature defecation? Do drinking or skin shedding influence defecation patterns? Do these patterns hold up in the field? What other functions might snake poop have? One study showed that captive snakes pooped more quickly after their cages were cleaned, whereas control animals whose cages were merely rearranged did not, which suggests that snakes might be using their feces for marking...something (we really don't know what since they aren't generally thought of as territorial, although they are a whole lot more social than most give them credit for). The mysteries are many.

ACKNOWLEDGMENTS

Thanks to Pedro Rodriguez for allowing the use of his photograph.

REFERENCES

Castoe, T. A., Z. J. Jiang, W. Gu, Z. O. Wang, and D. D. Pollock. 2008. Adaptive evolution and functional redesign of core metabolic proteins in snakes. PLoS ONE 3:e2201 <link>

Chiszar, D., S. Wellborn, M. A. Wand, K. M. Scudder, and H. M. Smith. 1980. Investigatory behavior in snakes, II: Cage cleaning and the induction of defecation in snakes. Animal Learning & Behavior 8:505-510 <link>

Cundall, D. 2002. Envenomation strategies, head form, and feeding ecology in vipers. Pages 149-162 in G. W. Schuett, M. Höggren, M. E. Douglas, and H. W. Greene, editors. Biology of the Vipers. Eagle Mountain Publishers, Eagle Mountain, UT <link>

Lillywhite, H. B., P. de Delva, and B. P. Noonan. 2002. Patterns of gut passage time and the chronic retention of fecal mass in viperid snakes. Pages 497-506 in G. W. Schuett, M. Höggren, M. E. Douglas, and H. W. Greene, editors. Biology of the Vipers. Eagle Mountain Publishers, Eagle Mountain, UT <link>

Riquelme, C. A., J. A. Magida, B. C. Harrison, C. E. Wall, T. G. Marr, S. M. Secor, and L. A. Leinwand. 2011. Fatty acids identified in the Burmese Python promote beneficial cardiac growth. Science 334:528-531 <link>

Secor, S. M. and J. Diamond. 1998. A vertebrate model of extreme physiological regulation. Nature 395:659-662 <link>

Secor, S. M. and J. M. Diamond. 2000. Evolution of regulatory responses to feeding in snakes. Physiological and Biochemical Zoology 73:123-141 <link>

Secor, S. M. 2008. Digestive physiology of the Burmese Python: broad regulation of integrated performance. Journal of Experimental Biology 211:3767-3774 <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.

This article will soon become available in Spanish

The world is full of obscure snakes. According to Darren Naish at Tetrapod Zoology, the more you know about them, the better a person you are. Writing this blog, and in my research, I am often confronted with the challenging task of finding out something - anything at all - about a species of snake that I've never heard of before. This post is a walk-through of the process that I usually use to track down even the most basic information about obscure snakes, although it could be used as an example of how to find trustworthy information about any species of plant or animal. I'll use as an example the species Liophidium mayottensis (Peters's Bright Snake) - a lamprophiid colubroid found on the island of Mayotte. If you're like me then you're filled with questions right away: Who was Peters? What is so bright about this snake? Where's Mayotte?

Wikipedia page for Liophidium mayottensis
as of October 2014

I needed to know about this snake as part of a project I'm doing where we compare endangered species of reptiles with those that aren't to try and figure out if there are traits or features that the endangered species have in common (and the same for invasive species and other special groups). This kind of thing has been done for birds and fish, but not really for reptiles. It's a much larger effort than just me, and my part in it is small, usually tracking down basic information about the reptiles so that we can build a database of reptile life history traits. I'm talking about things like size, sexual dimorphism, whether they lay eggs or give birth to live young, how many eggs or young they have at a time and how often, where and in what kind of habitats they live, what they eat, that kind of thing. Sounds simple, right? We'll just go to Wikipedia...well, as of 2014 that wasn't very helpful.

When faced with a species about which I know almost nothing - in this case a species I had never even heard of before - there are a couple of resources that I generally go to first in order to figure out how I should proceed. The first is always The Reptile Database. This wealth of information is curated by Peter Uetz, Jakob Hallermann, and Jiri Hosek, three individuals to whom the whole of the herpetological world is indebted. Using the advanced search feature, you can look up any species of living reptile using its common or scientific name, including by an old scientific name (a "synonym") that is no longer used. This is important because scientific names change all the time, and sometimes the same species has gone by 10 or 20 different names over the course of its taxonomic lifetime. It is particularly important to know about these names because the species may have gone by them for a long time in older literature, which is sometimes the most important literature there is.

Liophidium mayottensis

Before searching TRD, I sometimes try to use the scientific name itself to figure out a little bit about what I'm looking for. It helps to know some Latin and Greek, and a handy reference that I use a lot is Borror's Dictionary of Word Roots and Combining Forms. In this case, the genus name Liophidium told me that this was a snake with smooth scales (the Greek prefix lio- meaning smooth + the Greek root ophid meaning snake + the Latin suffix -iumnormally used to form abstract nouns). The specific epithet mayottensis means "from Mayotte" (the -ensis suffix is a common way to form an adjective indicating spatial or geographic origin in Latin, similar to the English suffix -ese, as in Maltese, Chinese, or Portuguese). Although the Latin and Greek origins of the scientific name can be helpful, they can also be misleading (for example, the North American Racer is called Coluber constrictor even though it is not a constrictor) or unhelpful (another familiar North American snake, Storeria dekayi, is named after two 19th century herpetologists, David H. Storer and James E. DeKay), so don't rely too much on these.

The Madagascan Biogeographic Realm
Mayotte is the southeasternmost island in the
Comoros chain, although politically it is part of France.
Many interesting snakes inhabit this realm, including bolyeriids

When searching TRD, I always put the full binomial I'm looking for into the 'Synonym' field of TRD's Advanced Search, because the 'Genus' and 'Species epithet' fields only search the current names, and who knows what name it goes by now. Barring any misspellings, at least one record usually turns up, sometimes more if the name I've used has been split into multiple species. In this case, it's just one, and it matches the name I used. From this record, I can find out the currently accepted higher taxonomy of my species. In addition to being a snake (which I already knew), I can see that it's in the recently-erected family Lamprophiidae, a group of snakes found mostly in Africa. Furthermore, I can see that Liophidium mayottensis is in the subfamily Pseudoxyrhophiinae, a group of snakes found almost exclusively in Madagascar. Because Mayotte is an island in the Comoro Island chain, lying just northwest of Madagascar, this subfamilial designation makes sense - we think that lamprophiids colonized Madagascar, Socotra, and the Comoros from Africa about 30 million years ago, one of several radiations of snakes onto these islands. However, in this case knowing the subfamily doesn't help us much in our search for natural history information. Unlike certain instantly-recognizable groups of snakes such as pareatids or xenodermatids, pseudoxyrhophiines are diverse, including almost 90 species with a wide variety of lifestyles. I've written about the genus Langaha, which belongs to this group, before.

The BHL is also a great source of artwork
in the form of old plates, like this mudsnake
from Duméril's Erpétologie Générale,
which adorns the logo of this blog

In order to go further we need look at the rest of the TRD record. Since we're looking for a description of the species, one of the most helpful pieces of information is the location of the original description in the scientific literature. You'll find the name of the person who originally described the species and the year they did it in the TRD record, right next to the scientific name. This is called the authority, and it's presented in parentheses if the name that person used has subsequently been changed. For instance, 11 of the 139 reptile species described by Linnaeus, the father of modern taxonomy, still retain the original names he gave them. You can tell because these are the ones without parentheses. If you look to the bottom of the record, you'll find a citation for the book or article in which that first description resides, along with other literature pertinent to the species. This literature is usually focused on taxonomic changes, although sometimes more general ecology or natural history literature is included as well. Following up on this literature is easier in some cases than others. One thing TRD has done to make it simple is provide links to the full-text if it's available for free online somewhere. A lot of older literature is becoming available through the Biodiversity Heritage Library, a partnership of libraries that have digitized what they call the "legacy literature" of biodiversity.

Wilhlem C.H. Peters

Our species was originally described in 1874 by Wilhelm Carl Hartwig Peters, a German naturalist and explorer, which explains the first part of the common name Peters's Bright Snake (which was probably not applied until much later, since it's considered presumptuous to name a species for oneself). Peters called it Ablabes (Enicognathus) rhodogaster var. mayottensis, a confusing mess if there ever was one. His description was published in the journal Monatsberichte der Königlichen Preussische Akademie des Wissenschaften zu Berlin (which is obfuscatingly abbreviated Monatsber. Königl. Akad. Wiss. Berlin.), which roughly translates to 'Monthly Reports of the Royal Prussian Academy of Sciences in Berlin'. Not exactly the most widely read journal, even if it has existed in one form or another since 1700 and is still around today. Anyway, it's in German, so it'll prove difficult for us to read Peters's original description even if we can find it (which thanks to the BHL, we can). There's also the little problem of whether the issue it's in was published in 1873 or 1874, because the citation in TRD lists both, but fortunately we can check both quickly since the page numbers are also given (it's '73). The article starts on this page and the description is on this one. These days descriptions of new species usually get their own stand-alone articles, but back then it was common practice to shoehorn them into checklists, expedition reports, and other types of articles. There's a description of a new chameleon in the same article. In a way, it's one explanation for the prolific output of Peters, who described 122 new genera and 649 new species of amphibians and reptiles in his lifetime, 281 of which are still recognized today (only four people, all his contemporaries, have described more). The high attrition is partly because many species were inadvertently described more than once. The guys at TRD have done a fabulous job keeping track of all this confusing literature, and I cannot commend them highly enough for their efforts.

Another difference between the 1800s and now is that species descriptions today are generally much more complete. You might be surprised to learn that the International Commission on Zoological Nomenclature, which advises, arbitrates, and recommends rules for the zoological community on describing new species of animals, stipulates only that in order for a species description to count as official, it must include at a bare minimum just "a description or definition that states in words characters that are purported to differentiate the taxon", and even this 'strict' definition applies only to names published after 1930. Peters's description of Liophidium mayottensis (translated) reads:

17.Ablabes (Enicognathus) rhodogaster Schlegel var. mayottensis:

Two young specimens from Mayotte seem to me to belong to the above species, although they do not have red coloration on the belly. Frontal a little longer than high; 8 supralabials, of which the 4th and 5th touch the eye; temporals 1+2+2; infralabials 9, the first pair of which is in contact behind the tapered mental; two pairs of chin shields. Body scales smooth, without apical pits, in 19 longitudinal rows. Ventrals 190, divided anal, subcaudals 99 pairs. Above olive-brown, a little darker along the middle and fourth-to-last row of scales. From the snout through the eye and the frenal region there is a black napkin which is indistinct on the side of the neck and disappears in the penultimate row of scales on the side of the body. Under this there is a bright yellow band, which goes to the mouth. There are three black spots on the rostral and upper lip. The chin and infralabials are spotted or marbled with black and yellow. On the neck are fine yellowish transverse lines. Ventral scales with 4-6 black dots; posterior ventral scales and subcaudals yellowish-white.

Liophidium rhodogaster
Gold-collared Snake

So we've got counts of the scales and descriptions of their position relative to one another, which is considerably more than it took back in the 1870s to name a new species. No drawings, no information on size, habitat, reproduction, nothing. It's forgivable when you know that Peters, by then a museum curator, was merely reporting on a collection of amphibians and reptiles he had been sent from Madagascar and nearby islands by two guys named Pollen and van Dam. Peters thought the snakes they had collected on Mayotte were a variant of a species that had already been described, the Gold-collared Snake of Madagascar, known then as Enicognathus rhodogaster and today as Liophidium rhodogaster (rhodogaster meaning 'red belly'). We learn from TRD that twenty years later Belgian-British zoologist George Boulenger (writing, mercifully, in English) elevated it to its own species and changed the genus so that it was known as Polyodontophis mayottensis. Boulenger is even lighter on details than Peters, saying only that it is very similar to rhodogaster but differs in that it has one more pair of dorsal scale rows, about 11 more ventrals, and about 15 more subcaudals, and that its neck pattern includes the same yellow lines mentioned by Peters. Since he's not trying to describe a new species, it's OK, but it's frustrating since we're looking for more detail about the animal's ecology and natural history.

It's likely that neither Peters nor Boulenger ever saw Liophidium mayottensis, or many of the other species they described, alive, so we can forgive them for not mentioning its habitat or patterns of activity (although they could have at least measured the specimen). Sometimes museum specimens yield information about diet (via stomach contents) or reproduction (via eggs or embryos in utero), but this does not seem to be the case for Peters's Bright Snake. To learn about these things, we'll have to sleuth out some other papers. The other two listed at TRD don't look too promising - one is a biography of Peters that's only available in print, and the other focuses on a different genus, Sibynophis, that's superficially similar to Liophidium but distantly related.

We can do a little better by checking some other common sources of information on the web. We already know that Wikipedia's useless (although the links at the bottom of some pages can be quite useful), but a general Google search for the scientific name typically turns up links to the pages for a species on several authoritative sites that aggregate biodiversity information online. In no particular order, I often check the University of Michigan Museum of Zoology's Animal Diversity Web. This is a great student-authored resource but it's still incomplete, and it doesn't even have a page for our genus yet (but check out their detailed pages on all three Acrochordusspecies). Other similar sites include the Encyclopedia of Life (species page incomplete for L. mayottensis, but check out Laticauda colubrina for a fairly good page), DiscoverLife (which is mostly links with little original content, and is unhelpful for our species, although they host a cool ID guide for North American snakes), and Map of Life (which has lots of cool mapping capabilities but not for our species). Citizen science projects can be a rich source of information on distribution, but such projects are in their infancy for herps. Two of the best are iNaturalist and HerpMapper, neither of which has any data on our species. Remember that none of these sources are peer-reviewed, so they may propagate misinformation (although I have found this to be rare).

One of Pagale Bacha's Flickr photos of L. mayottensis

ARKive is a film and image archive that generally has pictures of rare species when most other websites fail, and that is the case here, but as of 2014 it contained no additional information (contrast with their excellent accounts for snakes like Natrix natrix and Macroprotodon cucullatus). Flickr can be a good source of images too, in this case providing us with four additional images, all taken by the same person of the same individual snake. I have noticed that a culture of accurate species identification exists on Flickr that isn't found elsewhere on the Internet. For instance, don't ever trust Google Images when searching for rare species - in this case, only one of the hundreds of images returned is actually of our snake. Earlier I mentioned the Biodiversity Heritage Library, one of the most consistently useful resources on the web, and their search feature leads us to one new resource: a mention in a paper by John Cadle from 1999, focusing on morphological taxonomy of Malagasy snakes (which states that Liophidium are diurnal and led me to a paper describing the smooth, hinged, spatula-shaped teeth of Liophidium and other snakes, an adaptation for grasping and swallowing hard-bodied prey, such as skinks — their teeth fold backwards when forces are applied to their leading surface, but lock into an erect position if forces come from behind).

Some L. mayottensis DNA. It looks just like the DNA
of any other species, although there's a lot it can tell us.

Two other online databases are more authoritative than those previously mentioned, in that they are reviewed by experts. One is GenBank, the NIH genetic sequence database. A GenBank search reveals that five genes have been sequenced from L. mayottensis, which is more than for most reptiles. These include four mitochondrial genes (ND4, CO1, and cyt-b, which are essential to the electron transport chain of cellular respiration, and 16S, part of the protein synthesis machinery of ribosomes) and one nuclear gene (c-mos, which plays a role in mitosis). These genes were chosen for their conserved functions and relatively slow rates of evolution, which makes them useful for phylogenetic purposes (except for CO1, which evolves at just the right rate for DNA barcoding, a technique which is used, among other things, to monitor trade of reptiles without specialized expert knowledge). A phylogenetic analysis was done to determine the relationship of Liophidium pattoni, a new species discovered in Madagascar in 2009, to the other species in the genus. The results placed L. pattoni as sister to L. rhodogaster, and L. mayottensis as sister to two other Malagasy species, L. torquatum and L. chabaudi. This may seem like a dry, mundane detail, but it actually tells us something very interesting about our species: it probably colonized Mayotte from Madagascar after the ancestors of Liophidium had already radiated there. It also says that Peters, who thought that L. mayottensis was a subspecies of L. rhodogaster, was way off - it's actually more closely related to almost any other member of the genus (although to be fair to Peters, none of those other members had been described yet when he named L. mayottensis — and morphology might lead you to believe that L. mayottensis was the most basal member of the group, since it has 19 dorsal scale rows whereas every other species has 17).

Liophidium pattoni and its relationship to some of its closest relatives, including L. mayottensis
From Vieites et al. 2010

IUCN categories

The other more authoritative online database is the IUCN Red List. The Red List assesses the conservation status of species and often includes a distribution map (although not in this case), some ecological information, and a short bibliography focused on ecology and conservation rather than on taxonomy. The IUCN page contains several useful nuggets, most of which come to us by way of expert knowledge and may or may not be published elsewhere. For instance, we learn that our species is classified as Endangered under the IUCN categories, which are based on quite rigorous and quantitative criteria. Peters's Bright Snake qualifies as Endangered despite very limited data because all known records are from a forested area of about 65 km² in the center of Mayotte, which is subject to a continuing decline in quality (criterion B2b(iii)) and within which the actual occurrence records of the snake suggest that its populations are severely fragmented (criterion B2a). Even if the area of occupancy is underestimated, the entire terrestrial area of Mayotte is only 365 km², which is still less than the minimum of 500 km² that a species must exceed unless both it and its habitat are known to be contiguous and stable.

Hinged teeth of Liophidium rhodogaster
From Savitzky 1981

The IUCN record also lists several other pieces of information. It tells that the known records are all between 144 and 653 meters above sea level. It states that "this snake is diurnal, ground-dwelling and very secretive", "observed in natural forests and plantations", and is egg-laying. This last tidbit is pretty helpful, and it's no surprise that we haven't encountered it before - it's from a field guide written in French by Danny Meirte, covering the terrestrial fauna of the Comoros, published in 1999 and updated in 2004. As for conservation, it says that our species is not used by humans for any known purpose, but that an introduced civet may be a threat. All native reptile species on Mayotte are protected by law, and several nature reserves may benefit L. mayottensis, but no data is available on the snake's occurrence at these sites.

Finally, the IUCN record notes that "the extreme scarcity of observations may be attributed to the cryptic habits of this snake, but also suggests that L. mayottensis is not common". No shock there. The short bibliography includes both the old and new editions of the field guide and a paper by Oliver Hawlitschek in the journal ZooKeys that used field surveys and remotely sensed data to assess the conservation status of Comoran reptiles, upon which most of the conservation assessment is based. The profile also cites another work in preparation by Hawlitschek, who was also an expert reviewer for the species and took the Arkive photograph. I visited his website and was able to learn that he is a German PhD student studying herp conservation & phylogeography in the Comoros.

Phylogenetic tree of Malagasy reptiles based on CO1 DNA barcodes
Liophidium is near the top right
From Nagy et al. 2012

Now we're getting somewhere, although we're still looking for body size and clutch size, two of the most basic species attributes. Usually, after checking all off the above sources, I repeat the whole process on Google Scholar and track down any promising articles. Often , I'll add a search term for the particular attribute I'm looking for (e.g.,"clutch size", "svl") to see if that helps. In this case, even Google Scholar didn't turn up much specific to our species. I was about to give up when I decided to contact Oliver Hawlitschek. When I went to look up his email address, I noticed that he recently published a paper in the journal PLoS ONE, which of all places is known for its free and open accessibility to all. The paper, titled "Island Evolution and Systematic Revision of Comoran Snakes: Why and When Subspecies Still Make Sense", includes supplementary material that finally gives us the answer to our seemingly simple question of "how long is Liophidium mayottensis"? The average adult total length is about 80 cm for both sexes, maximum 1 meter (3 feet), with the tail making up about 30% of the body. When I contacted Oliver he confirmed this, and he also told me that as far as he knew no information on clutch size was available (although he expected it would be small, like that of most other island snakes). From reading his paper, I also learned that this is by far the largest species of Liophidium (the next is L. therezieni at 72.6 cm) and the only one with 19 dorsal scale rows instead of 17. Oliver's paper suggested that Comoran Liophidium (and the snake Lycodryas and lizard Oplurus) are larger than their Malagasy congeners because they are released from competition with larger species that do not occur in the Comoros.

Liophidium mayottensis skull (with tooth closeup, inset)
Image by Cynthia Wang

Oliver also put me in touch with Cynthia Wang, another graduate student who is using high-resolution X-ray computed tomography to make 3-D scans of the skulls of snakes. Turns out she recently scanned a L. mayottensis skull. You can see the spatula-shaped, hinged teeth characteristic of the genus, although the connective tissue is missing. He also told me that he will be returning to the Comoros this November, and that L. mayottensis will be his #1 target while he's there. All in all, a pretty satisfying conclusion.

This was a long article; congratulations if you made it to the end! I justified the length partly in celebration of my birthday this month and partly in celebration of this blog reaching 250,000 views! I hesitated writing this article because I base a lot of my articles around obscure snakes and I was afraid that writing a how-to would amount to writing myself out of a lot of subject matter. On the other hand, I suppose I enjoy the chase, and I think this overly-long article's length goes to show just how much actually is out there, even for really obscure species, if you're willing to look (and there are certainly resources I've missed! Let me know about them in the comments.). I also think that this process is easily generalizable to non-reptiles - there are some great resources out there for amphibians, birds, algae, echinoderms, insects, and much else. Whatever you're interested in, happy researching!

ACKNOWLEDGMENTS

Thanks to Oliver Hawlitschek, Cynthia Wang, Henry Cook, and Pagale Bacha for the use of their images.

REFERENCES

Bauer, A. M., R. Günther, and M. Klipfel. 1995. The Herpetological Contributions of Wilhem CH Peters (1815-1883). SSAR Facsimile Reprints in Herpetology:114.

Boulenger, G. A. 1893. Catalogue of the snakes in the British Museum (Natural History). Trustees of the British Museum, London <link>

Cadle, J. E. 1999. The Dentition, Systematics and Phylogeny of Pseudoxyrhopus and Related Genera from Madagascar (Serpentes: Colubridae) with Descriptions of a New Species and a New Genus. Bulletin of the Museum of Comparative Zoology at Harvard College 155:381-443 <link>

Hawlitschek, O., B. Brückmann, J. Berger, K. Green, and F. Glaw. 2011. Integrating field surveys and remote sensing data to study distribution, habitat use and conservation status of the herpetofauna of the Comoro Islands. ZooKeys 144:21–78 <link>

Hawlitschek, O., Nagy, Z., & Glaw, F. 2012. Island evolution and systematic revision of Comoran snakes: why and when subspecies still make sense. PLoS ONE 7:e42970 <link>

Hedges, S. B. 2013. Revision shock in taxonomy. Zootaxa 3681:297-298 <link>

Meirte, D. 2004. Reptiles. Pages 201-224 in M. Louette, D. Meirte, and R. Jocqué, editors. La faune terrestre de l'archipel des Comores. MRAC, Tervuren.

Nagy, Z. T., U. Joger, M. Wink, F. Glaw, and M. Vences. 2003. Multiple colonization of Madagascar and Socotra by colubrid snakes: evidence from nuclear and mitochondrial gene phylogenies. Proceedings of the Royal Society of London. Series B: Biological Sciences 270:2613-2621 <link>

Peters, W. C. H. 1873. Über eine von Hrn. F. Pollen und van Dam auf Madagascar und anderen ostafrikanischen Inseln gemachte Sammlung von Amphibien. Monatsberichte der Königlichen Preussische Akademie des Wissenschaften zu Berlin 1873:792-795 <link>

Savitzky, A. H. 1981. Hinged teeth in snakes: an adaptation for swallowing hard-bodied prey. Science 212:346-349 <link>

Uetz, P. 2010. The original descriptions of reptiles. Zootaxa 2334:59-68 <link>

Vieites, D. R., F. M. Ratsoavina, R.-D. Randrianiaina, Z. T. Nagy, F. Glaw, and M. Vences. 2010. A rhapsody of colours from Madagascar: discovery of a remarkable new snake of the genus Liophidium and its phylogenetic relationships. Salamandra 46:1-10 <link>

Zaher, H., F. G. Grazziotin, R. Graboski, R. G. Fuentes, P. Sánchez-Martinez, G. G. Montingelli, Y. P. Zhang, and R. W. Murphy. 2012. Phylogenetic relationships of the genus Sibynophis (Serpentes: Colubroidea). Papeis Avulsos de Zoologia (Sao Paulo) 52:141-149 <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.

This post will soon become available in Spanish

Number of new snake species by decade, with highlights
Data from The Reptile Database

Linnaeus's 1758 Systema Naturae, the starting point of zoological nomenclature, described 118 species of reptiles, including 74 snakes (not counting the limbless lizards and amphibians he included in the same group). It took over 100 years for the number of described species of snakes to reach 1000, an event that probably passed without much notice amid the American Civil War. Since that time, new snake species descriptions have been added at the rate of about 15 a year, although molecular taxonomy has increased this pace over the last few decades. The trends for snakes and for reptiles as a whole have been similar, and on July 9th, 2014, a team of American, German, Lao, and Vietnamese scientists described a new species of gecko from Laos, which the journal Herpetological Review reported as the 10,000th reptile species. Needless to say, I was excited, but I was also extremely disappointed because I had been so hoping that it would be a snake! Rather than admit defeat and scrap this planned post, I emailed Peter Uetz at The Reptile Database, an incredible resource that I've praised before, to confirm that this gecko was indeed #10,000. As usual for taxonomy and as I should have suspected, the reality was a bit more complicated.

Although Cyrtodactylus vilaphongi was the 10,000th reptile species for a while, the order and position of entries in The Reptile Database is constantly changing. Although new species get added to the end of the list, it's common for two or more existing species to get synonymized or merged, which moves the position of all subsequent species up. Furthermore, sometimes species that were described long ago and subsequently synonymized are revalidated, leading to 'new' species that aren't really new in the sense that they have existed before. Finally, often existing species get split up, leading to additions that aren't as dramatic as legitimate new discoveries. This last complication is on the rise now that molecular systematics has enabled us to describe the cryptic diversity of some lineages, which are not all that morphologically distinct but may contain considerable genetic diversity.

At the time of my email to Peter last month, C. vilaphongi was the 9988th species, and (happily), a new snake, Siphlophis ayauma, was #10,000. Although this has probably changed again by now, I'm going to operate under the assumption that, since we can't really say with certainty that any particular species was #10,000, if it was a snake, it was probably one of the 11 brand new snake species that have been described so far this year. You can read about many of these on the blog 'Species New to Science', but I'm going to highlight them in a little more detail here.

Rhabdophis guangdongensis
From Zhu et al. 2014

The first new snake described this year, Rhabdophis guangdongensis, was collected by a team of Chinese herpetologists in Guangdong Province in 2008. The reason it wasn't described until the February 20th issue of the journal Zootaxais because, as is often the case, it takes a couple of years to compare both the anatomy and the DNA of a suspected new species to reference specimens of known similar species and establish that the species really is new. In the past, particularly prior to the internet, the difficulty of doing this was a huge problem, resulting in close to half of all 'new' species later being invalidated as duplicates. The genus Rhabdophis is distributed in southern and eastern Asia, and this is the 21st species. It's an extremely interesting genus from a chemical ecology perspective, because at least one species sequesters defensive chemicals from its prey and provisions them to its young (which I wrote about for Scientific American shortly after I started this blog). A recent paper by Yosuke Kojima and Akira Mori on the Japanese species R. tigrinus showed that females periodically leave wetlands for forest streams where they forage on toads, likely to obtain the necessary toxins for provisioning their offspring. The new species also has specialized structures, known as nuchal glands, on the back of its neck, so presumably it stores bufotoxins there as well, although this has yet to be verified.

Opisthotropis durandi
From Teynié et al. 2014

On March 3rd, a team of French, German, and Vietnamese scientists published a description of Opisthotropis durandi, a highly aquatic snake collected from the base of a waterfall in northern Laos. This is the seventh species of Opisthotropis described in the past 20 years, and the first from Laos (although other species are likely to occur there based on their occurrence in surrounding countries). Like the new Rhabdophis, it is also the 21st species in its genus. It is important to realize that, like most species new to science, this snake was already known by local people. It is called Ngou Koung or Ngou Kung, meaning “shrimp snake”, suggesting that it may eat shrimp. The pools at the base of the waterfall where the first specimen was found contained many small shrimp.

Eutrachelophis bassleri and its weird penis
From Myers & McDowell 2014

Harvey Bassler, a petroleum geologist, explored many of the Amazon's upper tributaries for his work during the 1920s and 30s, during which time he collected over 4,200 snakes on the side. Bassler deposited his magnificent collection in the American Museum of Natural History in 1934, and on March 6th this year Charles Myers and Samuel McDowell published a monograph in the Bulletin of the American Museum of Natural History describing a species of snake collected by Bassler in 1927, for which they erected a new genus, Eutrachelophis (‘beautiful-necked snakes’’). They also placed in this genus a species originally described by Boulenger in 1905, Rhadinaea steinbachi, which they renamed Eutrachelophis steinbachi. Although the two species (and a third, yet undescribed) have very similar skeletons, muscles, glands, viscera, and markings, they probably would have been placed in separate genera had they been described in the 19th or early 20th century because their hemipenes are so different. E. steinbachi has long but relatively normal-looking hemipenes, whereas E. bassleri has extremely unusual heimpenes tipped with a dome-like structure so strange (at least within the world of snake hemipenes) that the authors wrote "we have seen nothing quite like [it]." Hemipenes were traditionally considered one of the most taxonomically-important structures in snakes¹ because they were considered to be evolutionarily neutral (that is, unlikely to change in response to selection), but a growing awareness that evolution by both natural and especially sexual selection can influence the morphology of male genitalia led these authors to recognize that these two snakes were in fact close relatives. Although we await molecular confirmation, the authors propose a mechanism by which differential expression of Hox genes²could cause such a rapid divergence in hemipenal morphology between two sister species.

Siphlophis ayauma
From Sheehy et al. 2014

On January 12th, 2008, a group of American and Ecuadorian herpetologists stopped for lunch at a grilled-chicken restaurant in Paute, Azuay province, Ecuador. They noticed a peculiar sun-faded snake on display in a jar of alcohol that they couldn't quite put a name to. Following negotiation with the restaurant owner, the specimen was acquired and determined to belong to the genus Siphlophis, but could not be identified to any known species. A few months later, another specimen was found alive about 100 miles to the north, and two more were discovered in 2011 about the same distance to the south. A fifth individual is now recognized to have been hiding out unnoticed in the collection of the Museo de Zoología, Pontificia Universidad Católica del Ecuador. Because of its red-banded head and its occurrence in the mountains near cold (achachay) streams, the new species was named Siphlophis ayauma after the Kichwa spirit Aya Uma, a good spirit devil who derives strength from nature, particularly from cold mountain pacchas (cascades) and is represented in Kichwa folklore as having a colorful red-banded head. This is the seventh species in the genus, the third species known from Ecuador, and the first new species of Siphlophis since 1940. The results are published in the April 1st issue of the South American Journal of Herpetology.

Philodryas amaru
From Zaher et al. 2014

In a montane grassland high in the Andes Mountains of southern Ecuador, another genus gained its 21st species this year: Philodryas amaru. Known to the Ecuadorian and Brazilian authors since 2005, a small population of these striped racers was formally described in Zootaxa on April 4th this year. The new species resembles Philodryas simonsii in color pattern, but differs noticeably in its hemipenis morphology. "Amaru" means "snake" in Kichwa, and is also the name of a snake deity who influences water and the economy. This diurnal snake lays clutches of 9-13 eggs underground in galleries and under decaying logs, and probably eats frogs and lizards. It is a close relative of the Galapagos racers that I've written about before.

Causus rasmusseni
From Broadley 2014; photo by Paul L. Lloyd

Night adders (genus Causus) are a small and unusual group of vipers found in sub-Saharan Africa. They were once thought to be the most primitive vipers and were placed in their own subfamily, but they are now grouped with the viperines even though they have a plethora of unusual features: platelike head scales, round pupils, a different hinge mechanism for their erectile fangs, incomplete fang canal closure, and elongate venom glands in most species. On April 25th of this year, Don Broadley³ described the first new species of Causus since 1905. He named it Causus rasmusseni after the late Jens Rasmussen, a Dutch expert on African snakes who died in 2005. This species is found only in the watershed between the Congo and Zambezi basins, where it co-occurs with three other species of Causus. Broadley first became aware that there might be a new species of night adder in this region in 1991, when he noticed pale gray C. rhombetaus from northwestern Zambia with black markings and low ventral scale counts. In 2013, someone sent him a picture of one eating a toad (another unusual adaptation that night adders share with several other snakes), which prompted him to look again at the unusual specimens and describe them as a new species. Few molecular data are available for Causus, so this diagnosis is based on morphology alone.

Micrurus potyguaraFrom Pires et al. 2014

Brazil is graced with nearly 400 species of snakes, including 30 of the world's ~80 species of coralsnakes. The morphology of coralsnakes is highly variable, and there are many misidentified specimens in museum collections, so it is often difficult to recognize new species. A group of Brazilian herpetologists working on the tri-colored coralsnakes from the endangered northeastern coastal forests discovered a new species, which they described in the June 5th issue of Zootaxa (if any of these dates are your birthday, then you share a birthday with that of a new species of snake!).

Top: Jaw of Lycodon aulicus
From Jackson & Fritts 2004
Middle: Lycodon zoosvictoriae
From Neang et al. 2014
Bottom: Lycodon cavernicolus
From Grismer et al. 2014

Wolfsnakes (genus Lycodon) are named for their fearsome-looking fang-like anterior maxillary teeth. Unlike the true fangs of vipers, elapids, and atractaspidids, wolfsnake teeth are not grooved or hollow and they have no venom. Instead, their strongly arched upper jaw helps them feed on skinks, whose hard, cylindrical bodies fit snugly into their diastema, or the gap between their anterior and posterior teeth. The wolf-like anterior teeth keep the skink from being squeezed out of the mouth, while the posterior teeth slice through the skink's cycloid scales. At least 16 of the nearly 60 species of Lycodon have been described since the 1990s, including two this June: Lycodon zoosvictoriae from the Cardamom Mountains of southwestern Cambodia, and L. cavernicolus from a limestone cave in peninsular Malaysia. The latter is a cave-adapted species, both specimens of which were found climbing several feet above the cave floor, in total darkness. It's likely that they eat a cave-adapted gecko. Many of the caves in this region are in immediate danger of being quarried for cement before their endemic fauna and flora can be fully documented. Both of these species were also described in Zootaxa, which is a relatively new journal dedicated almost exclusively to rapid publication of new species descriptions, with the stated goal of aiding conservation efforts by circumventing the lengthy delays normally associated with publication of new science. Since its inception in 2001, Zootaxa has become a daily journal that has published nearly one quarter of all new animal taxa and nomenclatural acts in the last five years, including over 400 new species of reptiles and the 7000th species of amphibian.

"Cloudogram" of Crotalus triseriatus species group
showing the new nine-species arrangement
From Bryson et al. 2014

Just three days before the new gecko, a team of scientists from Mexico, the USA, and Canada published a genetic analysis of the Crotalus triseriatus species group, which contains small montane rattlesnakes found in Mexico and the southwestern USA. Although five species were historically recognized within the group, an analysis of seven nuclear genes revealed that there are at least nine species, including two that were previously recognized as subspecies and two more that have not heretofore been formally recognized. The paper described the two new species: Crotalus tlaloci, named for Tláloc, the Aztec god of rain, and Crotalus campbelli, named for herpetologist Jonathan Campbell. The authors of this paper suggest that these rattlesnakes speciated rapidly from a single common ancestor during the uplifting of the Trans-Mexican Volcanic Belt near the end of the Neogene period 2.6 million years ago, which makes sense because they are not very mobile and populations of their common ancestor likely would have become isolated from one another on various "Sky Islands" of suitable habitat during the genesis of this new mountain range. Many species are endemic to the high-altitude pine-oak forests and grasslands of this region, which has become famous as the overwintering grounds of the Monarch Butterfly.

Chironius diamantina
From Fernandes & Hamdan 2014

Surprise! Just when you thought we were through, at press time the description of four more new species of snake had just been published, all from relatively recent issues of Zootaxa. One is a Brazilian species of Chironius, one of my favorite genera. Chironius diamantina is the 16th species in the genus, which is unusual is having a very low, even number of dorsal scale rows (10 or 12), the central pair of which are strongly keeled, giving the snake a distinctly flat-backed appearance. This species is found in riparian forests along rocky streams in coastal Brazil, not too far south of the new coralsnake (above). Chironius are diurnal and generally eat birds and mammals. Another is a new Asian keelback, Herpetoreas burbrinki, from near the border of China, India, and Burma. which is relatively closely related to the Rhabdophis above. Finally, two new species from the large ground-dwelling Latin American genus Atractus, both small and described from single specimens collected decades ago in Colombia (perhaps they will one day be rediscovered). More new species from both of these groups will likely follow, given the taxonomic untidiness of their genera. [Update: shortly after publication David Salazar-Valenzuela alerted me to the fact that I had missed his description, with colleagues, of a third new Atractus from the cloud forests of northern Ecuador earlier this year, in the journal Herpetologica. They mention that some of the specimens were collected from under logs alongside an undescribed species of slender blindsnake of the genus Trilepida, soit seems we are at 3,500 this year without a doubt!] [[Update II: It seems I missed more than I thought - a new species of Trimeresurus from Sumatra was described in September from specimens collected in 1899, and a new Ninia from Trinidad was described in August from a 1988 specimen.]]

In addition to these 15 species, there are a couple of species of snake which were described long ago but that were revalidated recently, including several scolecophidians (Typhlops silus, first described in 1959; Afrotyphlops angeli, first described in 1952; and Letheobia acutirostrata, first described in 1916) and a rattlesnake (Crotalus armstrongi, originally described as a subspecies in 1979 and elevated by the same group that described C. tlaloci and C. campbelli). These are typically announced with less fanfare than the truly new descriptions that I've highlighted above.

Although it's actually been the slowest year for new snakes since 1997⁴, we have 15 new snakes this year, bringing snakes to a total of 3,499 (and 2014 isn't over yet!). We could make it to 3,500 snakes in the same year that we hit 10,000 reptiles. I think these milestones in taxonomy emphasize the importance of reptiles and how much we have left to learn about them. I doubt that the pace of new species descriptions will slow down anytime soon, as experts estimate that less than 15% of the species on Earth have yet been described. Increasingly, reptiles, and snakes in particular, are becoming poster-children for biodiversity and conservation, a welcome change from their history of being overlooked and maligned. Soon, we will have high-quality global range maps for all species of reptiles, an achievement reached some time ago by amphibians, mammals, and birds, which will enable their incorporation into global assessments of vertebrate diversity and conservation planning. It's an exciting time.

ACKNOWLEDGMENTS

Thanks to Peter Uetz at The Reptile Database for sharing with me some inside information, and to the authors of these papers for their photos.

REFERENCES

Newspaper clipping from 10 January 1960
showing Broadley with his amputated finger.
You can see more at the finger's Facebook page
or listen to Broadley describe the experience here.

Angarita-Sierra, T. 2014. Hemipenial Morphology in the Semifossorial Snakes of the Genus Ninia and a New Species from Trinidad, West Indies (Serpentes: Dipsadidae). South American Journal of Herpetology 9:114-130 <link>

Broadley, D. G. 2014. A new species of Causus Lichtenstein from the Congo/Zambezi watershed in north-western Zambia (Reptilia: Squamata: Viperidae). Arnoldia Zimbabwe 10:341-350 <link>

Bryson, R. J., C. W. Linkem, M. E. Dorcas, A. Lathrop, J. M. Jones, J. Alvarado-Diaz, C. I. Grunwald, and R. W. Murphy. 2014. Multilocus species delimitation in the Crotalus triseriatus species group (Serpentes: Viperidae: Crotalinae), with the description of two new species. Zootaxa 3826:475-496 <link>

Cope, E. D. 1895. The classification of the Ophidia. Transactions of the American Philosophical Society 18:186-219 <link>

Dowling, H. G. 1967. Hemipenes and other characters in colubrid classification. Herpetologica 23:138–142 <link>

Grismer, L. L., E. S. H. Quah, S. Anuar, M. A. Muin, P. L. Wood Jr, and S. A. M. Nor. 2014. A diminutive new species of cave-dwelling Wolf Snake (Colubridae: Lycodon Boie, 1826) from Peninsular Malaysia. Zootaxa 3815:51-67 <link>

Guo, P., Q. Liu, L. Zhang, J. X. Li, Y. Huang, and R. A. Pyron. 2014. A taxonomic revision of the Asian keelback snakes, genus Amphiesma (Serpentes: Colubridae: Natricinae), with description of a new species. Zootaxa 3873:425-440 <link>

Fernandes, D. and B. Hamdan. 2014. A new species of Chironius Fitzinger, 1826 from the state of Bahia, Northeastern Brazil (Serpentes: Colubridae). Zootaxa 3881:563-575 <link>

Trimeresurus gunaleni
From Vogel et al 2014

Jackson, K. and T. H. Fritts. 2004. Dentitional specialisations for durophagy in the Common Wolf snake, Lycodon aulicus capucinus. Amphibia-Reptilia 25:247-254 <link>

Köhler, G. and M. Kieckbusch. 2014. Two new species of Atractus from Colombia (Reptilia, Squamata, Dipsadidae). Zootaxa 3872:291-300 <link>

Linnaeus, C. 1758. Systema naturæ per regna tria naturæ, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima, reformata. [10th ed.]. Laurentii Salvii, Holmiae, Stockholm, Sweden <link>

Myers, C. W. and S. B. McDowell. 2014. New Taxa and Cryptic Species of Neotropical Snakes (Xenodontinae), with Commentary on Hemipenes as Generic and Specific Characters. Bulletin of the American Museum of Natural History 385:1-112 <link>

Neang, T., T. Hartmann, S. Hun, N. J. Souter, and N. M. Furey. 2014. A new species of wolf snake (Colubridae: Lycodon Fitzinger, 1826) from Phnom Samkos Wildlife Sanctuary, Cardamom Mountains, southwest Cambodia. Zootaxa 3814:68-80 <link>

Pires, M. G., N. J. da Silva Jr., D. T. Feitosa, A. L. d. C. Prudente, G. A. P. Filho, and H. Zaher. 2014. A new species of triadal coral snake of the genus Micrurus Wagler, 1824 (Serpentes: Elapidae) from northeastern Brazil. Zootaxa 3811:569-585 <link>

Atractus savagei
From Salazar-Valenzuela et al. 2014

Salazar-Valenzuela, D., O. Torres-Carvajal, and P. Passos. 2014. A New Species of Atractus (Serpentes: Dipsadidae) from the Andes of Ecuador. Herpetologica 70:350-363 <link>

Schneider, N., T. Q. Nguyen, M. D. Le, L. Nophaseud, M. Bonkowski, and T. Ziegler. 2014. A new species of Cyrtodactylus (Squamata: Gekkonidae) from the karst forest of northern Laos. Zootaxa 3835:80-97 <link>

Sheehy, C. M., M. H. Yánez-Muñoz, J. H. Valencia, and E. N. Smith. 2014. A new species of Siphlophis (Serpentes: Dipsadidae: Xenodontinae) from the eastern Andean slopes of Ecuador. South American Journal of Herpetology 9:30-45 <link>

Teynié, A., A. Lottier, P. David, T. Q. Nguyen, and G. Vogel. 2014. A new species of the genus Opisthotropis Günther, 1872 from northern Laos (Squamata: Natricidae). Zootaxa 3774:165-183 <link>

Uetz, P. 2010. The original descriptions of reptiles. Zootaxa 2334:59-68 <link>

Vogel, G., P. David, and I. Sidik. 2014. On Trimeresurus sumatranus (Raffles, 1822), with the designation of a neotype and the description of a new species of pitviper from Sumatra (Squamata: Viperidae: Crotalinae). Amphibian and Reptile Conservation 8:1–29 <link>

Zaher, H., J. C. Arredondo, J. H. Valencia, E. Arbeláez, M. T. Rodrigues, and M. Altamirano-Benavides. 2014. A new Andean species of Philodryas (Dipsadidae, Xenodontinae) from Ecuador. Zootaxa 3785:469–480 <link>

Zhu, G.-X., Y.-Y. Wang, H. Takeuchi, and E.-M. Zhao. 2014. A new species of the genus Rhabdophis Fitzinger, 1843 (Squamata: Colubridae) from Guangdong Province, southern China. Zootaxa 3765:469-481 <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.

This post will soon become available in Spanish

King Cobra (Ophiophagus hannah; top) and
Burmese Python (Python bivittatus; bottom),
the two snake species whose genomes
were fully sequenced in 2013

One year ago today, the first snake genomes ever sequenced hit the newsstands. OK, so two papers in Proceedings of the National Academy of Sciences isn't exactly the cover of Time magazine to most people, but it was big enough news that it was covered by The Huffington Post and the two most prominent interdisciplinary scientific journals, Science and Nature, the former devoting a special section to the event. One year later, dear reader, welcome to the Life is Short, but Snakes are Long coverage of the snake genome project. So just what is the big deal about these snake genomes anyway, and what's changed in snake biology in the year that they've been available?

In one way, sequencing a snake genome means that snakes finally join the illustrious ranks of lab animals like the mouse, rat, guinea pig, fruit fly, and amoeba, all of whom have already had their genomes sequenced. By now the genomes of several hundred species have been sequenced, starting with a virus in the 1970s, and the first archaeon, bacterium, and eukaryote within one year of one another in 1995-96. The first animal genome sequenced was that of the model nematode Caenorhabditis elegans in 1998, and the first vertebrate was a pufferfish, so chosen because its genome is so small, in 2002 (although an incomplete first draft of the human genome preceded that by a year). As of 2014, we're now up to just over 100 vertebrate species, about 60 of which have been annotated and formally published, as well as numerous other animals, plants, fungi, protists, and prokaryotes. Last week, Science highlighted drafts of 38 new bird and 3 new crocodilian genomes, the largest single release of vertebrate genomes to date. But we are still a long way from sequencing the genomes of all known species. Why have we chosen the species we have? What does it mean to sequence a genome, exactly, and why do we do it?

Breakdown of what the human genome
consists of. Exons are coding DNA.
From Reece et al. (2013)

We use the word genome to refer to all the DNA within a single organism. Confusingly, this is not quite the same thing as saying all the genes in an organism, because we usually only call sections of DNA "genes" if we know what they do. You've probably heard that 98% of the human genome is "junk", or non-coding, DNA, which is just another way of saying that we haven't figured out what it does yet. Actually, we now know lots of things that non-coding DNA is good for, but we still usually don't call most of that DNA "genes" because we use that word specifically to mean sections of DNA that are read out via RNA and translated (usually) into proteins, which then have obvious effects on cells and the body. Non-coding DNA can also have effects on the body, often by regulating other genes, but it works in a more complicated way that we don't yet fully understand, so we tend make over-generalizations about it or dismiss it as unimportant.

Avian tree of life based on whole-genome
sequences. We're still several years away from
a tree like this for squamate reptiles.
From Jarvis et al. 2014

When we say we have sequenced the genome of an organism, we mean that we have read the sequences of all of its DNA, every one of its genes and all of its non-coding DNA, even if we don't know what it all does. The -ome suffix is added to the word 'gene' to signify "all". Yogis will be familiar with the Sanskrit word Om, which means "the whole thing", something that encompasses the entire universe in its unlimitnedness. Other fields in biology that consider all constituents of something collectively have picked up on this neologism, so we have proteomics (the study of all the proteins in a particular organism), transcriptomics (the study of all the RNA), and so on. Genomes are huge¹, and we've strategically chosen species to sequence that are scattered across the diversity of life so that we can construct a skeletal tree of life based on genomic data. We have high confidence in such a tree² because whole genomes contain so much data that trees built from them are more likely to reflect true evolutionary relationships than trees built from just one or a few genes. So we've selected exemplars from each major group of organisms to start out with (e.g., one sea urchin, one sea squirt, one lamprey), and eventually we'll go back and fill in the gaps. By sequencing the King Cobra (Ophiophagus hannah) and Burmese Python (Python bivittatus) genomes first, we're setting these species up to become model organisms, exemplars, and in some ways stand-ins for all of snake diversity in many future studies.

Understanding the genes controlling variation among individuals
of the same species, like the color morphs of these Groundsnakes
(Sonora semiannulata), must await population genomics
and a better understanding of gene expression regulation

When we sequence a genome we read all the DNA from a single individual³. This is different from knowing all the possible variants (often called alleles) of those genes. It's often said that a person has "the genes for" something, when in reality all people have the same genes, with different alleles. For example, if the person whose genome was sequenced in the Human Genome Project had brown eyes, we'll just have the gene sequences for brown eyes, not for blue or green. In order to get an idea of all the possible variants of all the genes in a species, we'll need to sequence the genomes of many individuals. Some genes, such as those involved in the immune system, have over 1,500 alleles (the "gene pool"), no more than two of which occur within the genome of a single individual (one from the mother and one from the father). So understanding the entire gene pool of a species is a very daunting task, given that we only have whole genomes for a few hundred species (one individual each), with multiple individuals of a few species, including humans.⁴ Population genomics is an emerging field, yet to be applied to snakes in any form, although apparently a few projects are in the works.

So what have we learned from these snake genomes? Here are the basics:

Snake genomes are about half the size of the human genome (although an organism's complexity is not directly proportional to its genome size; for example, some salamander genomes are more than 60 times larger than the human genome).
The proportion of repetitive elements ("junk DNA") in snake genomes is about the same as that in humans (~60%).
Snakes have a faster baseline rate of evolution than other reptiles, birds, or mammals, as
Red represents fast rates of neutral substitution
From supplement to Castoe et al. 2013
evidenced by their larger accumulation of neutral substitutions. and colubroid snakes have rates even faster than that of snakes at large.
Adaptive evolution (as evidenced by functional, non-neutral, changes to genes) in snakes has happened to over 500 genes, especially those involved in the development of the limbs, spine, skull, and eye, and those regulating the function of the cardiovascular system, lipid and protein metabolism, and cell birth and death. We already knew that all of these systems in snakes were highly modified relative to other vertebrates, and now we know that the genes that underlie them are too.
Some groups of genes have grown or shrank in snakes - for example, snakes have a lot more genes coding for vomeronasal receptors, and a lot fewer genes coding for opsins, which are light-sensitive proteins in the eye. This makes sense given what we know about snake sensory systems.
Changes to gene expression that happen after a snake feeds involve thousands of genes that control rapid changes in organ size - but genes that control cell division change in the kidney, liver, and spleen, organs that grow by cell division, but not in the heart, which grows when individual existing cells get larger.
Snake genomes contain endogenous viral elements from three families of viruses that have recurrently infiltrated their DNA over the past 50 million years. This is actually not rare, although it is bizarre and awesome that the 'fossils' of these ancient viral genomes can be identified in their host genomes even after tens of millions of years, and it can help us better understand both the biology of viruses and that of their snake hosts, including how viruses have contributed functions to the genetic repertoires of their hosts.

From the cobra genome in particular, we've learned or confirmed a great deal about the evolution of snake venoms. In particular, we now know that, unlike the venom of the platypus, the only other venomous vertebrate with a sequenced genome, snake venom has evolved primarily through gene duplication and restriction. Many venom proteins probably evolved like this:

A snake has a gene that makes a protein somewhere in its body, including possibly in its salivary or venom gland⁵
The gene for that protein is duplicated by accident during routine DNA replication or repair, resulting in a new, spare copy of the gene
The effects of selection are relaxed on the duplicate gene, which gives it opportunities to mutate
Mutations to transcription-factor binding sites change the signal for where the duplicate gene should be expressed, causing the new protein to be made only in the venom gland
If the new protein helps the snake catch more prey, it improves fitness and causes natural selection
Because the old protein is still being made, the new gene and protein are free to evolve to become more toxic or to take on some new function
The new copy of the gene may become duplicated again, and subsequent new copies may mutate further, leading to diversification within a gene/toxin family⁶

The King Cobra venom gland, with
expression profiles of the venom (left) and
accessory gland (right). From Vonk et al. 2013

It's not yet clear to what extent the evolution of these novel toxic venom proteins corresponded with a shift to higher levels of their expression in the venom gland and lower levels of expression elsewhere. Although it seems obvious that their expression in non-venom-gland tissues would be harmful, their non-toxic orthologs are expressed in tissues as diverse as the kidney and brain in pythons, and no one has yet measured their expression outside of the venom gland in venomous snakes. Alternatively, gene duplication might have taken place after the change in function, if the genes in question were alternatively spliced to produce both toxic and non-toxic proteins from the same gene. Evolution of siRNA and other regulatory elements (which is hard to detect because there's still a lot we don't understand about how it works) could then restrict expression of a particular splice variant to the venom gland, which could explain why we're seeing evidence that the venom protein genes themselves are often still expressed in other tissues even though they are capable of coding for highly toxic proteins that must be maintained in the venom gland in a competent but inactive state.

The cobra genome by itself does not answer these questions, even with help from that of the python. In order to fully understand the evolution of snake venoms (with major implications for public health, particularly in developing countries, not to mention the potential of venoms to be used as drugs), we'll need genomic, transcriptomic, and proteomic data from numerous snake species.

Characterization of genomic biodiversity has the potential to change our understanding of evolution in fundamental ways. From explaining how snakes are capable of physiological feats to helping us understand how new genes appear, what "junk DNA" does, and what the tree of life looks like, genome sequencing is one of the most exciting current frontiers in biology. As in many things, snakes are (one of) the last groups of vertebrates to the party (although it's worth noting that there aren't any fully annotated salamander or caecilian genomes yet). A snake genome doesn't add a whole lot to the picture of the vertebrate tree of life, because the Green Anole genome, sequenced in 2011, represents squamates on the tree, and no one is arguing that snakes aren't squamates. But, within squamates there are a number of puzzling unresolved relationships, including such fundamental questions as the origin of snakes and the placement of iguanians. In the interest of helping to shed light on these, and on the aforementioned complexity of snake venom evolution, another 10 or so snake genomes are likely to come out within the next couple of years, including those of the:

Texas Blindsnake (Rena dulcis)
Reticulate Wormsnake (Amerotyphlops reticulatus)
Red Pipesnake (Anilius scytale)
Mexican Burrowing Python (Loxocemus bicolor)
Round Island Splitjaw Snake (or "boa"; Casarea dussumieri)
Boa Constrictor (Boa constrictor)
Western Diamond-backed Rattlesnake (Crotalus atrox)
Speckled Rattlesnake (Crotalus mitchelli)
Copperhead (Agkistrodon contortrix)
Eastern Coralsnake (Micrurus fulvius)
Cloudy Snail-eating Snake (Sibon nebulatus)
Common Gartersnake (Thamnophis sirtalis)

As you can probably see if you know your snake taxonomy, these species represent a scattering of well-known snakes from each of the major branches of the snake tree. They have been strategically chosen to enable snake biologists to use them to put together a well-supported skeleton of the snake tree of life. However, several branches (such as the dwarf pipesnakes, acrochordids, and lamprophiids) are still missing.⁷ In particular, an atractaspidid genome would be useful in building a better understanding of the role of convergence in snake venom evolution - resolving the debate between proponents of a single ancient origin for venom and those of several more recent, independent origins. Genomes of scolecophidian blindsnakes and toxicoferan lizards such as Gila monsters will also help resolve this question. Hopefully, these genomes and others will continue to illuminate evolutionary biology for us in ways Darwin could have scarcely imagined.

1 Because genome sequences contain so much data, they are stored electronically and require a large amount of computing power and storage capacity. The computing power is actually more limiting than the biochemistry right now. A human genome contains about 6 billion base pairs (one for each person on Earth in 1999), which take up a couple of gigabytes. If that doesn't sound that impressive, imagine all that information stored in every one of your cells, then compare the size of a cell with that of a microchip here.^↩

2 This is not to say that (as has been presumed by many) molecular data are inherently superior to morphological data, especially in the case of extinct fossil taxa, from which we cannot garner much molecular information (although that generalization too has been challenged).^↩

3 How are the individuals whose genomes are sequenced chosen? The unsatisfying answer is that the scientists involved typically use whatever individuals are convenient. Specifically, the cobra and python genomes seem to have been taken from animals from the pet trade. We may not know the true geographic origin of these individuals, or even whether they might be the offspring of animals from two or more different parts of the species' range. Why is this important? If we sequence the genome of a cobra from Indonesia, but cobras in India have evolved different venom genes because of different evolutionary pressures, then we won't know that until we get some cobras from India. Taxonomic conclusions drawn from Boa constrictor gene sequences on GenBank are dubious because of the ambiguous origins of many of these specimens. The primary reasons to sequence a whole genome are subtly different from the reasons to sequence individual genes, and scientists doing these tasks have different questions. But, we should be cautious about inferring too much from the genome sequence of a single individual of any species.^↩

4 Right now if you're a human you can actually get your whole genome sequenced for less than $5000, even though the first human genome cost over $3 billion, because we've optimized the process.^↩

5 It's unclear how many venom proteins were originally made in the venom gland before they became toxic, and how many were recruited to this tissue following duplication. The original cobra genome paper by Vonk et al. implies that the latter is most common, whereas subsequent work by Hargreaves et al. uses gene expression data from Leopard Gecko salivary glands to suggest the former. Reyes-Velasco et al. used the python genome and transcriptome to suggest that venom genes are recruited preferentially from genes that are expressed at low levels in most tissues but at more variable levels than average across tissues.^↩

6 Of the approximately 24 gene families that code for snake venom proteins, those that produce toxins that are known to be important in prey capture (e.g., the three-finger neurotoxins) have undergone repeated duplication and selection, whereas venom components that perform ancillary functions, such as helping the snake to relocate its bitten prey, do not show high rates of duplication or selection. These rates are probably further influenced by the need to target diverse receptors in different types of prey (in snakes with broad diets), and by predator-prey co-evolutionary arms races (in snakes with narrow diets).^↩

7 A recent effort by a different research group generated a tree for Caenophidia using 333 loci totaling 225,140 base pairs for each of 31 snake species, almost 80,000 of which were informative. This is a drastic improvement on the 10 loci and maximum of 5,814 base pairs of the most comprehensive previous studies, but it is still a long way from the entire genome. Incredibly, they were still unable to resolve certain difficult parts of the snake family tree.^↩

ACKNOWLEDGMENTS

Thanks to JD Willson, Baloch Imrankhan, and Alison Davis Rabosky for the use of their photographs, and to Alison Davis Rabosky and Todd Castoe for providing me with information regarding genomics.

REFERENCES

Alföldi et al. 2011. The genome of the green anole lizard and a comparative analysis with birds and mammals. Nature 477:587-591 <link>

Armengaud, J., J. Trapp, O. Pible, O. Geffard, A. Chaumot, and E. M. Hartmann. 2014. Non-model organisms, a species endangered by proteogenomics. Journal of Proteomics 105:5-18 <link>

Castoe et al. 2013. The Burmese python genome reveals the molecular basis for extreme adaptation in snakes. Proceedings of the National Academy of Sciences 110:20645–20650 <link>

Cox, C. L. and A. R. D. Rabosky. 2013. Spatial and Temporal Drivers of Phenotypic Diversity in Polymorphic Snakes. The American Naturalist DOI: 10.1086/670988 <link>

Gauthier, J. A., M. Kearney, J. A. Maisano, O. Rieppel, and A. D. B. Behlke. 2012. Assembling the squamate Tree of Life: perspectives from the phenotype and the fossil record. Bulletin of the Peabody Museum of Natural History 53:3-308 <link>

Hargreaves, A. D., M. T. Swain, M. J. Hegarty, D. W. Logan, and J. F. Mulley. 2014. Restriction and recruitment-gene duplication and the origin and evolution of snake venom toxins. Genome Biology & Evolution 6:2088-2095 <link>

Hargreaves, A. D., M. T. Swain, D. W. Logan, and J. F. Mulley. 2014. Testing the Toxicofera: Comparative transcriptomics casts doubt on the single, early evolution of the reptile venom system. Toxicon. DOI:10.1016/j.toxicon.2014.10.004 <link>

Jarvis et al. 2014. Whole-genome analyses resolve early branches in the tree of life of modern birds. Science 346:1320-1331 <link>

Losos, J., D. M. Hillis, and H. W. Greene. 2012. Who speaks with a forked tongue? Science 338:1428-1429 <link>

Mackessy, S. P. and L. M. Baxter. 2006. Bioweapons synthesis and storage: The venom gland of front-fanged snakes. Zoologischer Anzeiger 245:147-159 <link>

Pyron, R. A., C. R. Hendry, V. M. Chou, E. M. Lemmon, A. R. Lemmon, and F. T. Burbrink. 2014. Effectiveness of phylogenomic data and coalescent species-tree methods for resolving difficult nodes in the phylogeny of advanced snakes (Serpentes: Caenophidia). Mol. Phylogenet. Evol. 81:221-231 <link>

Reyes-Velasco, J., D. C. Card, A. Andrew, K. J. Shaney, R. H. Adams, D. R. Schield, N. R. Casewell, S. P. Mackessy, and T. A. Castoe. 2014. Expression of venom gene homologs in diverse python tissues suggests a new model for the evolution of snake venom. Molecular Biology and Evolution <link>

Schweitzer, M. H. 2011. Soft tissue preservation in terrestrial Mesozoic vertebrates. Annual Review of Earth and Planetary Sciences 39:187-216 <link>

Vonk et al. 2013. The king cobra genome reveals dynamic gene evolution and adaptation in the snake venom system. Proceedings of the National Academy of Sciences 110:20651–20656 <link>

Yadav, S. P. 2007. The wholeness in suffix -omics, -omes, and the Word Om. Journal of Biomolecular Techniques 18:277 <link>

Zelanis, A. and A. Keiji Tashima. 2014. Unraveling snake venom complexity with ‘omics’ approaches: challenges and perspectives. Toxicon <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.

This post will soon become available in Spanish!
Este post pronto estará disponible en español!

Ambergris Cay Dwarf Boa (Tropidophis g. greenwayi)

Now that the USA and Cuba are finally warming up to one another after a chilly fifty years, we might be poised to learn a lot more about a really interesting group of snakes that reach their highest diversity on Cuba. These are the tropidophiids, or "dwarf boas". Their name is a little misleading—like the splitjaw snakes, they were once thought to be related to the true boas, and the name sticks even now that we now know better. At least the dwarf part is accurate: most tropidophiids are only 1–2 feet long. But this unassuming group of drab, nocturnal, live-bearing snakes holds more surprises and lessons about snake evolution that one would expect at first glance, with no shortage of interesting natural history to boot.

Top: Tropidophis melanurus constricts an anole
From Torres et al. 2014
Bottom: Madagascar Ground Boa
(Acrantophis madagascarensis)
constricts an oplurid lizard

Tropidophiids eat mostly frogs and lizards, and they constrict their prey in the same way as true boas: by winding the anterior part of their body neatly around their prey like a rope around a windlass, usually with an initial twist in the first loop, so that the snake's belly faces its head. This behavior, along with their relatively large gape size, seemed to suggest that they were related to the true boas (family Boidae, sensu stricto), including well-known tree boas, boa constrictors, and anacondas. All true boas are neotropical and there are quite a few in the West Indies, so unlike many of the other boid "hangers-on" (such as the Malagasy Sanzinia & Acrantophis, African Calabaria, North American rosy and rubber boas, Pacific Candoia, and Old World sand boas), a close relationship between tropidophiids and boids was easy to accept in terms of the biogeography of the living species. A comparative analysis of constriction behavior in extant alethinophidian snakes done by Harry Greene and Gordon Burghardt showed that this pattern of constriction is shared by essentially all "henophidian" snakes, including booids, pythonoids, and some uropeltoids, notwithstanding a few fossorial species that have apparently secondarily lost constriction behavior alltogether, because it doesn't work in tight spaces.¹

Top: Panamanian Dwarf Boa (Ungaliophis panamensis),
a member of the group to which tropidophiids were
once thought to be most closely related.
Bottom: Red Pipesnakes (Anilius scytale)
don't resemble tropidophiids very closely,
but we now think that they are each others'
closest living relatives.

In particular, what we now call tropidophiids were thought to be particularly closely related to two other small genera of neotropical boids, Exiliboa and Ungaliophis, which they superficially resemble both morphologically² and ecologially. These still share their common name of "dwarf boa", but about 15 years ago a new picture began to emerge. While DNA from Exiliboa and Ungaliophissuggested that they were indeed related to true boas, evidence from both mitochondrial and nuclear DNA and immunological proteins of Tropidophis and Trachyboa, along with details of their muscular, circulatory, and reproductive anatomy, suggested that they were most closely related to the monotypic family Aniliidae, which contains a single South American species known as the Red Pipesnake (Anilius scytale). As far as we know, Anilius doesn't normally constrict its prey³, because it mostly forages underground on elongate vertebrates such as eels, caecilians, amphisbaenians, and other snakes, similar to various Asian pipesnakes to which it was once thought to be closely related. But, we are now fairly certain that these Asian pipesnakes are convergent with Anilius, that tropidophiids and aniliids are each others' closest relatives, and that the similarity between the gape size and constriction behavior of tropidophiids and that of boas and pythons probably still represents the shared retention of a paired morphology/action pattern used by their common ancestor, it's just a common ancestor that is much older than we originally thought. Estimates suggest that tropidophiids and aniliids diverged from one another 60-110 mya in South America⁴, after their common ancestors were isolated from those of all other modern alethinophidian snakes, which radiated in Africa following the mid-Cretaceous split-up of west Gondwana 70-120 mya. This was the split that formed South America and Africa, and we are now getting used to diving the alethinophidians into two major lineages, Amerophidia (tropidophiids and aniliids) and Afrophidia (everybody else), instead of into a monophyletic "crown-group" Macrostomata containing boas, pythons, and caenophidians, and a basal group of non-macrostomatan pipesnakes more similar in ecology to scolecophidians. My snake taxonomy article from 2013 is actually out-of-date with respect to this major shift in snake taxonomy, because at the time it was still unclear to me (and there are still some strong arguments from paleontologists that the molecular data may be misleading).

The Greater Antilles, Bahamas, and Turks & Caicos

The "new" family Tropidophiidae consists of two species of "eyelash dwarf boas" in the mainland genus Trachyboa (there we go with the boa thing again), and the diverse genus Tropidophis, which contains 32 species in total: 5 from mainland South America, and a West Indian radiation consisting of 17 Cuban species (one of which is shared with Jamaica and one with both Jamaica and Hispaniola), 1 on Hispaniola (shared with Cuba), 5 on Jamaica (two shared with Cuba), 2 in the Bahamas, one from the Turks & Caicos Islands, one each on the three Cayman Islands (Grand Cayman, Little Cayman, and Cayman Brac), and one endemic to Navassa Island, a small, uninhabited, disputed island in the Caribbean Sea between Cuba, Jamaica, and Hispaniola (which is known from four specimens and has not been seen in over 100 years). The West Indian species, particularly the Cuban ones, represent a radiation which rivals and parallels that of Darwin's finches. Morphological and molecular data suggest that the 17 species on Cuba are descended from a single colonization event, and that the island species appear to be more distantly related to the mainland ones than they are to Trachyboa, although four-fifths of the species of Tropidophis have no published sequence data yet so both of those conclusions could change.

Tropidophis xanthogaster bleeding from the mouth,
with blood behind the spectacle making the eyes appear red.
From Torres et al. 2013

As early explorers and biologists collected these snakes from bromeliads, within stone walls, and underneath rocks, they noted that species of Tropidophis made no effort to escape their collection, but rather coiled up into tight balls when captured. Another peculiar defensive behavior was soon noted—autohemorrhage of the nose and mouth. In other words, these snakes spontaneously bleed from these orifices and smear the blood all over themselves when handled. Creepily, the space between their spectacle and their eyes fills with blood momentarily beforehand, so that their eyes appear to flash red. Blood collected from their mouths doesn't clot for over half an hour, whereas blood collected simultaneously from their tails has clotted after 10 minutes, and the mouth blood is more acidic and has fewer red blood cells, presumably because it is mixed with saliva. However, it is not harmful to frogs or lizards, so it is not a substitute for venom. The exact function is unclear, but it appears to be to freak out would-be predators. Like many snakes, Tropidophis habituates to captivity and eventually does not exhibit this behavior.

Tropidophis melanurus, the largest species of Tropidophis
and the first described, from Cocteau & Bibron's 1843
volume on reptiles in de la Sagra's Histoire physique, politique,
et naturelle de l’Ile de Cuba

Just when you thought things couldn't get any more interesting, brace yourself, because most Tropidophis can change color! They are light silver-white at night, when they are active, and dark grayish-brown during the day, when they are not. It takes a Tropidophis 1-2 hours to go from completely light to completely dark, which they accomplish via mobilization of melanosomes (organelles containing the light-absorbing pigment melanin) from the core of a melanophore cell deep within their skin into finger-like extensions of the melanophore that are closer to the surface of the skin, partially blocking stationary xanthophores and iridiophores, which contain yellow, blue, or green pigments. Both adults and juveniles undergo diel color change, and it does not seem to be affected by age, sex, pregnancy, or feeding, although prior to shedding snakes remain dark and inactive for several days. The change is probably predominantly triggered by photoperiod, but exposure to cool temperatures (<63°F) can elicit a partial change from dark to light even in the middle of the day. When captive snakes were transported from Cuba to Czechoslovakia, they became jet-lagged—it took them several days to synchronize their rhythm to the new photoperiod, and keeping them in complete darkness for several days desynchronized their rhythm from that of the sun. The proposed function of this color change is to help nocturnally-active snakes retain their body heat, as light-colored objects lose heat more slowly than dark-colored ones. This is probably similar to the reason that Round Island Splitjaw Snakes, Pacific Keel-scaled Boas (Candoia carinata), and the Hogg Island race of Boa constrictor also become lighter-colored at night.

Tropidophis pardalis on a Cuban stamp

There's much more to learn about tropidophiids, the Cuban radiation of Tropidophis in particular. To date, little ecological information has been collected on most species, owing in part to their rarity and in part to the difficulty of working in the region. How do five or six sympatric species partition resources and coexist in various parts of Cuba? What was the order of speciation and colonization of the islands, and when did it happen? Hopefully tropidophiids will be around long enough for us to find out. They are faced with numerous threats. As in many places, local people not especially fond of them, despite the fact that no Greater Antillean snakes are dangerous to people. Collection for the pet trade may also be a concern, particularly since one former government official in the Turks & Caicos Islands apparently granted a permit to reptile dealers to remove thousands of Tropidophis greenwayi from North Caicos for the pet trade, allegedly implying that it would be preferred if they removed all of the snakes! Throughout the West Indies, most native ecosystems have been absent for centuries, and increasingly rapid development, especially due to tourism, threatens what little remains. And introduction of non-native predators, particularly the Small Indian Mongoose (Herpestes javanicus), may be their biggest threat. As early as 1919, herpetologist Thomas Barbour wrote "In Jamaica [Tropidophis maculatus] is almost extinct owing to the appetite of the introduced mongoose". Ironically, Operation Mongoose was the codename for the Kennedy administration's attempt to create Cuban diplomatic, political, and economic isolation in hopes of weakening Castro’s regime. Cats, dogs, rats, goats, pigs, cane toads, and even other introduced snakes also threaten not just tropidophiids, but all 120+ snake species endemic to the West Indies as well as the rest of the native fauna. Improved PR and conservation programs have benefited several lizard species, and could help snakes too.

Tropidophis haetianus

I'm going to go ahead and wager that we'll discover a few new species of Tropidophis in the not-too-distant future, and that possibly the mainland species will get moved into a new genus. I also think that we need a more creative common name for them than "dwarf boa", preferably one that doesn't include the word "boa" at all. One existing option is "wood snakes", which is mediocre at best. They are also called "rock pythons" in the Caicos Islands, an equally misleading name as "dwarf boa", "culebras bobas" (dumb snakes) in Cuba, and "shame snakes" on Andros Island in the Bahamas, both of which may refer to their head-hiding defensive behavior. However, my favorite is the name they are known by in many parts of the West Indies: "thunder-snakes", because they are more frequently seen after severe rainstorms. Caribbean Thunder-snakes has a nice ring to it, and it could help improve their image.

1 1: Constriction behavior has become a lot more variable within the Colubroidea, where it has also been lost in several venomous lineages. Venom and constriction can be thought of as two different solutions to the same problem—how to kill large prey without exposing yourself to undue risk. Also, the contention that constriction and large gape size were lost in fossorial henophidians (aka "regressed" macrostomatans, including uropeltids, anomochilids, and aniliids) is seemingly contradicted by the complex multipinnate morphology of their jaw adductor muscles, which is sufficiently similar to that of their lizard ancestors that it is unlikely to have re-evolved in the exact same way multiple times. This problem might also be an issue for scolecophidians, given that they have similar jaw muscle morphology to pipesnakes but appear to be more closely related to other living snakes than they are to some basal fossil macrostomate snakes with limbs (symoliophiids). Stay tuned for more on the unresolved relationships at the base of the snake family tree, including a look at what fossil snakes can tell us.^↩

2 2: All four genera (Exiliboa, Ungaliophis, Tropidophis, and Trachyboa) either completely lack a left lung or have a greatly reduced one, a characteristic they share with anomochilids and some caenophidians, but not with most other henophidians, which have a somewhat reduced but functional left lung. In addition, all four genera also have a "lung" on the dorsal wall of the trachea: the tracheal cartilages do not form closed rings but remain open on the top, where a greatly expanded ligament forms the tracheal lung. It has alveoli just like a regular lung, which are especially deep near the head, and is contiguous with the true lung in the vicinity of the heart. But, although this might seem like very strong evidence that these four genera are closely related, tracheal lungs of diverse structure are widespread among snakes, being found in certain scolecophidians, xenophidiids, acrochordids, vipers, atractaspidids, sea snakes, and many colubroid snakes.^↩

3 3: A tantalizing bit of evidence emerged in 2008—biologists in Brazil videotaped the prey subjugation behavior of a captive Anilius scytale, which essentially constricted an amphisbaenian that they tried to feed it. In general its constriction behavior agreed with that of other henophidia, although it was more variable in the particulars, which could have been due to the difficulty of holding onto the elongate, "vigorous and constantly twisting prey". But, data from a single observation do not a generalization make, and more studies are needed.^↩

4 4: Fossils of ten extinct species in five genera from the Paleocene, Eocene, and Oligocene of Europe, Africa, & North and South America have been assigned to the Tropidophiidae, although all of them are probably actually either ungaliophiines or stem afrophidians. Two genera, Falseryx and Rottophis, both from the Oligocene of western Europe, have some similarities with living tropidophiids as well as with ungaliophiines, but for the most part their skulls are poorly preserved, leaving paleontologists to work on just their vertebrae. Paleogene erycines dominated the snake fauna of North America prior to the Miocene explosion of colubroids, but as far as we know all of these species were much more closely related to modern rosy and rubber boas than they were to tropidophiids. The only unequivocal tropidophiid fossils are from the Pleistocene of Florida and the Bahamas.^↩

ACKNOWLEDGMENTS

Thanks to Kenny Wray, Nick Garbutt, Alex Figueroa, Patrick Campbell, Pedro Bernardo, and Carlos De Soto Molinari for the use of their photographs.

REFERENCES

Battersby, J. 1938. LXIV.—Some snakes of the genus Tropidophis. The Annals and Magazine of Natural History 1:557-560 <link>

Brongersma, L. 1951. Some notes upon the anatomy of Tropidophis and Trachyboa (Serpentes). Zoologische Mededelingen 31:107-124 <link>

Cocteau, J. and G. Bibron. 1843. Reptiles. in M. R. de la Sagra, editor. Histoire physique, politique, et naturelle de l’Ile de Cuba. Vol. 4. Arthus Bertrand, Paris <link>

Tropidophis paucisquamis from Brazil

Curcio, F. F., P. M. Sales Nunes, A. J. S. Argolo, G. Skuk, and M. T. Rodrigues. 2012. Taxonomy of the South American Dwarf Boas of the Genus Tropidophis Bibron, 1840, With the Description of Two New Species from the Atlantic Forest (Serpentes: Tropidophiidae). Herpetological Monographs 26:80-121 <link>

Cocteau, J. and G. Bibron. 1843. Reptiles. In: M. R. de la Sagra. Histoire physique, politique, et naturelle de l’Ile de Cuba. Vol. 4. Arthus Bertrand, Paris <link>

Dessauer, H. C., J. E. Cadle, and R. Lawson. 1987. Patterns of snake evolution suggested by their proteins. Fieldiana Zoology New Series 34:1–34 <link>

Echternacht, A. C., F. J. Burton, and J. M. Blumenthal. 2011. The amphibians and reptiles of the Cayman Islands: conservation issues in the face of invasions. Pages 129-147 in A. Hailey, B. Wilson, and J. Horrocks, editors. Conservation of Caribbean Island Herpetofaunas Volume 2: Regional Accounts of the West Indies. Brill, Leiden, Netherlands <link>

Fong, A. 2005. Variation in and natural history notes on Tropidophis fuscus (Serpentes: Tropidophiidae) from Cuba. Herpetological Review 36:118-119.

Greene, H. W. and G. M. Burghardt. 1978. Behavior and phylogeny: constriction in ancient and modern snakes. Science 200:74-77 <link>

Hecht, M. K., V. Walters, and G. Ramm. 1955. Observations on the natural history of the Bahaman pigmy boa, Tropidophis pardalis, with notes on autohemorrhage. Copeia 1955:249-251 <link>

Hedges, S. B. 2002. Morphological variation and the definition of species in the snake genus Tropidophis (Serpentes, Tropidophiidae). Bulletin of The Natural History Museum. Zoology Series 68:83-90 <link>

Hedges, S. B., A. Estrada, and L. Diaz. 1999. New snake (Tropidophis) from western Cuba. Copeia 1999:376-381 <link>

Hedges, S. B. and O. H. Garrido. 1992. A new species of Tropidophis from Cuba (Serpentes: Tropidophiidae). Copeia 1992:820-825 <link>

Hedges, S. B. and O. H. Garrido. 1999. A new snake of the genus Tropidophis (Tropidophiidae) from central Cuba. Journal of Herpetology 33:436-441 <link>

Hedges, S. B. and O. H. Garrido. 2002. A new snake of the genus Tropidophis (Tropidophiidae) from eastern Cuba. Journal of Herpetology 36:157–161 <link>

Hedges, S. B., O. H. Garrido, and L. M. Diaz. 2001. A new banded snake of the genus Tropidophis (Tropidophiidae) from north-central Cuba. Journal of Herpetology 35:615-617 <link>

Hedges, S. B., C. Hass, and T. Maugel. 1989. Physiological color change in snakes. Journal of Herpetology 23:450-455 <link>

Iturriaga, M. 2014. Autohemorrhaging behavior in the Cuban Dwarf Boa Tropidophis melanurus Schlegel, 1837 (Serpentes: Tropidophiidae). Herpetology Notes 7:339-341 <link>

Iverson, J. B. 1986. Notes on the natural history of the Caicos Islands dwarf boa, Tropidophis greenwayi. Caribbean Journal of Science 22:191-198.

Marques, O. A. V. and I. Sazima. 2008. Winding to and fro: constriction in the snake Anilius scytale. Herpetological Bulletin 103:29-31 <link>

Meylan, P. A. 1996. Pleistocene amphibians and reptiles from the Leisey Shell Pit, Hillsborough County, Florida. Bulletin of the Florida Museum of Natural History 37:273-297 <link>

Olson, S. L., ed. 1982. Fossil Vertebrates from the Bahamas. Smithsonian Institution Press, Washington, DC, USA <link>

Rehák, I. 1987. Color change in the snake Tropidophis feicki (Reptilia: Squamata: Tropidophidae). Vestnk Ceskoslovenske Spolecnosti Zoologicke 51:300-303.

Reynolds, R. G. 2011. Status, conservation, and introduction of amphibians and reptiles in the Turks and Caicos Islands, British West Indies. Pages 377-406 in A. Hailey, B. Wilson, and J. Horrocks, editors. Conservation of Caribbean Island Herpetofaunas. Volume 2: Regional Accounts of the West Indies. Brill, Leiden, The Netherlands <link>

Reynolds, R. G., M. L. Niemiller, and L. J. Revell. 2014. Toward a Tree-of-Life for the boas and pythons: multilocus species-level phylogeny with unprecedented taxon sampling. Molecular Phylogenetics and Evolution 71:201-213 <link>

Rieppel, O. 2012. “Regressed” Macrostomatan Snakes. Fieldiana Life and Earth Sciences 5:99-103 <link>

Rivalta, V., A. González, and L. Rodríguez. 2013. Collection of herpetology of the institute of ecology and systematics, La Habana, Cuba. Family Tropidophiidae, Genus Tropidophis. Revista Colombiana de Ciencia Animal 5:282-300 <link>

Schwartz, A. 1957. A new species of boa (genus Tropidophis) from western Cuba. American Museum Novitates 1839:1-8 <link>

Schwartz, A. 1975. Variation in the Antillean boid snake Tropidophis haetianus Cope. Journal of Herpetology 9:303-311 <link>

Schwartz, A. and R. J. Marsh. 1960. A review of the pardalis-maculatus complex of the boid genus Tropidophis of the West Indies. Bulletin of the Museum of Comparative Zoology at Harvard College 123:49-84 <link>

Siegel, D. S., A. Miralles, and R. D. Aldridge. 2011. Controversial snake relationships supported by reproductive anatomy. Journal of Anatomy 218:342-348 <link>

Stull, O. G. 1928. A revision of the genus Tropidophis. Occasional Papers of the Museum of Zoology University of Michigan 195:1-49 <link>

Szyndlar, Z. and W. Böhme. 1996. Redescription of Tropidonotus atavus von Meyer, 1855 from the Upper Oligocene of Rott (Germany) and its allocation to Rottophis gen. nov. (Serpentes, Boidae). Palaeontographica Abteilung A 240:145-161 <link>

Szyndlar, Z., R. Smith, and J.-C. Rage. 2008. A new dwarf boa (Serpentes, Booidea,‘Tropidophiidae’) from the Early Oligocene of Belgium: a case of the isolation of Western European snake faunas. Zoological Journal of the Linnean Society 152:393-406 <link>

Thomas, R. 1963. Cayman Islands Tropidophis (Reptilia, Serpentes). Breviora 195:1-8 <link>

Tolson, P. J. and R. W. Henderson. 2006. An overview of snake conservation in the West Indies. Applied Herpetology 3:345-356 <link>

Torres, J., C. Pérez-Penichet, and O. Torres. 2014. Predation attempt by Tropidophis melanurus (Serpentes, Tropidophiidae) on Anolis porcus (Sauria, Dactyloidae). Herpetology Notes 7:527-529 <link>

Torres, J., O. J. Torres, and R. Marrero. 2013. Autohemorrage in Tropidophis xanthogaster (Serpentes:Tropidophiidae) from Guanahacabibes, Cuba. Herpetology Notes 6:579-581 <link>

Vidal, N., A. S. Delmas, and S. B. Hedges. 2007. The higher-level relationships of alethinophidian snakes inferred from seven nuclear and mitochondrial genes. Pages 27-33 in R. W. Henderson and R. Powell, editors. Biology of the Boas and Pythons. Eagle Mountain Publishing, Eagle Mountain, Utah, USA <link>

Wilcox, T. P., D. J. Zwickl, T. A. Heath, and D. M. Hillis. 2002. Phylogenetic relationships of the dwarf boas and a comparison of Bayesian and bootstrap measures of phylogenetic support. Molecular Phylogenetics and Evolution 25:361-371 <link>

Zaher, H. 1994. Les Tropidopheoidea (Serpentes: Alethinophidea) sont-ils reellement monophyletiques? Arugments en faveur de leur polyphyletisme. Comptes Rendus de l'Académie des Sciences Paris 317:471–478 <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.

This post will soon be available in Spanish

Anilius scytale, the only living member of the family Aniliidae,
one of only two snake families containing just a single species

Deep in the Amazon rain forest there lives a fairly small, fairly obscure, red and black snake called Anilius scytale. It is banded, like many red and black snakes, but it has no venom, so it may be a coralsnake mimic. It spends most of its time under ground or in the water. Morphologically, it has a mixture of characteristics that place it somewhere in the no-man's-land we call "henophidia"—it has pelvic vestiges like many boas and pythons, but it has a small gape and is not capable of eating large bulky prey. It mostly feeds on elongate vertebrates, including other snakes, amphisbaenians, caecilians, and eels, and like other snake-eating snakes individuals can eat prey approaching their own total length. Its ventral scales are only barely wider than its dorsal scales, and it has just a few enlarged head scales, including one large hexagonal scale covering the eye and the surrounding skin. Males are smaller than females, which are viviparous, capable of giving birth to as many as 24 live young at a time. In 1946, the great naturalist William Beebe wrote "This is a strange snake", meaning that it's not quite like any other snakes. It is alone in its family, Aniliidae.

Head of Anilius showing the large scale covering both
the eye and the surrounding skin, like blindsnakes but
unlike most heno- and caenophidians

Snake biologists have used the term "pipesnake" to refer to any of three different lineages of snakes: the cylindrophiids (10 species of "Asian pipesnakes"), anomochilids (3 species of "dwarf pipesnakes"), and aniliids (1 species of "red pipesnake"; i.e., Anilius scytale). I'd like to propose that we begin to think of Anilius as "the pipesnake that wasn't", because (as I alluded to last month), it is now thought to be most closely related to tropidophiids (aka "the boas that weren't), superficially boa-like snakes found mostly in the Caribbean. Molecular data and some morphological data, especially that of the soft anatomy of the lungs and reproductive system, suggests that these two groups are each others' closest relatives, and they are now placed together in the Amerophidia (aka Anilioidea), the basal-most lineage of alethinophidia, which was apparently isolated in South America during the split-up of west Gondwana. Details of the skull anatomy cast some doubt on this classification, suggesting a closer relationship between aniliids and other non-macrostomatan pipesnakes, although even if this is true there are undoubtedly deep splits between Anilius and any other living snakes. Like the tuatara and the coelacanth, Anilius has not had close living relatives for tens of millions of years. Only it knows if it's lonely out there on such a long branch of the snake family tree.

Top: The plate of Anilius and a caiman as it appeared in
the 1719 printing of Merian's Metamorphosis
Insectorum Surinamensium
Bottom: A later version of the plate,
recolored and with the eggs removed

If Anilius is lonely, it can take some solace from having been noticed and beautifully illustrated by one of the first ecologists, Maria Sibylla Merian. Merian was a remarkable artist and scientist who lived from 1647 to 1717. She was one of the first trained artists to conduct detailed, long-term studies of living organisms, and the first published female naturalist. Most of her drawings, which she sketched from life on vellum and later engraved herself on copper plates, depict the life cycles of insects and their plant hosts, which she raised in captivity. She was the first to document that caterpillars turned into butterflies, and she described the life cycles of hundreds of insects, amassing evidence that contradicted the then-widespread notion that insects were "born of mud" by spontaneous generation (although others were credited with this discovery for a long time because her work was largely ignored, because it was written in Dutch rather than Latin). In 1699, Merian and her fifteen year-old daughter traveled to Surinam, where they spent the next two years studying and drawing the indigenous animals and plants, including several snakes. Her most famous work, Metamorphosis Insectorum Surinamensium, contains plates of many of these snakes, including one of an Anilius eating the egg of a caiman and being simultaneously attacked by the adult crocodilian. Like most of her drawings, it shows aspects of the natural history and ecology of the organisms in it, and helped establish a style of scientific illustration that later inspired naturalists from Catesby to Audubon. She depicted most of her insects life-sized, from various angles, in all stages of their life cycles, and most importantly, interacting with their host plants and predators. Her observations of animal behavior and plant-animal interactions are so detailed that many consider her the first ecologist. Considering that she died when Linnaeus was only 10 years old, it is all the more remarkable that her writings and drawings emphasize where organisms live and what they do rather than how they should be classified. Her works became very popular among Europe's upper class, and Czar Peter the Great in particular purchased many of her original watercolors and recruited her daughter as an art advisor and teacher at the newly-founded Academy of Arts in St. Petersburg. The Argentine Black and White Tegu, Tupinambis merianae, is named after her. Merian's text has not been translated into English, but I have taken a stab at translating her paragraph about snakes here:

Like crocodiles, some snakes hatch from eggs. They lay many small ones. The head and the tail of this snake, the Amphisbona, are the same shape and size, but you can tell which is the head because it has a mouth and small eyes, whereas the tail does not. Of all snakes, this one is the cleanest in color, being black, red, and yellow; others are grayish white, yellow, and brown with bodies that are more flattened.

ACKNOWLEDGMENTS

Thanks to Patrick Campbell and Andrew Snyder for allowing me to use their images.

REFERENCES

Anilius from d'Orbigny's 1849 Dictionnaire
Universel d'Histoire Naturelle

Beebe, W. 1946. Field notes on the snakes of Karatabo, British Guiana, and Caripito, Venezuela. Zoologica 31:11-52.

Duellman, W.E. 1978. The biology of an equatorial herpetofauna in Amazonian Ecuador. Miscellaneous Publications, Museum of Natural History, University of Kansas 65:1-352 <link>

Etheridge, K. 2011. Maria Sibylla Merian: The First Ecologist. in V. Molinari and D. Andreolle, editors. Women and Science: Figures and Representations – 17th century to present. Cambridge Scholars Publishing, Newcastle upon Tyne <link>

Marques, O. A. V. and I. Sazima. 2008. Winding to and fro: constriction in the snake Anilius scytale. Herpetological Bulletin 103:29-31 <link>

Martins, M. and E. M. Oliveira. 1998. Natural history of snakes in forests of the Manaus region, Central Amazonia, Brazil. Herpetological Natural History 6:78-150 <link>

Maschio, G. F., A. L. da Costa Prudente, A. C. de Lima, and D. T. Feitosa. 2007. Reproductive biology of Anilius scytale (Linnaeus, 1758) (Serpentes, Aniliidae) from eastern Amazonia, Brazil. South American Journal of Herpetology 2:179-183 <link>

Maschio, G. F., A. L. C. Prudente, F. S. Rodrigues, and M. S. Hoogmoed. 2010. Food habits of Anilius scytale (Serpentes: Aniliidae) in the Brazilian Amazonia. Zoologia (Curitiba, Impresso) 27:184-190 <link>

Merian, M.S. 1719. Metamorphosis Insectorum Surinamensium. Joannes Oosterwyk, Amsterdam <link>

Pieters, F. F. J. M. and D. Winthagen. 1999. Maria Sibylla Merian, naturalist and artist (1647-1717): a commemoration on the occasion of the 350th anniversary of her birth Archives of Natural History 26:1-18 <link>

Sawaya, R. J. 2010. The defensive tail display of Anilius scytale (Serpentes: Aniliidae). Herpetology Notes 3:249-250 <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.

This post will soon become available in Spanish

Eastern Diamondback Rattlesnake (Crotalus adamanteus),
the world's largest species of rattlesnake (maximum 8'3")

Rattlesnakes are one of North America's most iconic symbols. I think of them as herpetological Bald Eagles, only more diverse. Our continent boasts all 41 species, from huge diamondbacks to tiny pygmies, all of which diversified from a common ancestor 10-20 million years ago. Both American Indians and America's founding fathers viewed rattlesnakes as symbols of independence and strength, and new research is revealing that they are among the most social and behaviorally complex of snakes, caring for their young and displaying signs of spatial awareness and self-identity. Large species may take as long as ten years to become sexually mature, reproduce only once every three years in the northern part of their range, and live up to 30 years. Although many people fear rattlesnakes, comparatively speaking you are more likely to be bitten by a dog, struck by lightning, killed by office supplies, by your pajamas, or by just about anything other than a venomous snake in the USA. However, numerous communities in Alabama, Georgia, Kansas, New Mexico, Oklahoma, and Texas [Edit: Melissa Amarello of Advocates for Snake Preservation tells me that the Kansas & New Mexico roundups have been discontinued since 2007 for economic reasons.] carry out annual rattlesnake roundups, events with the purpose of exterminating wild rattlesnakes from the landscape.

Western Diamondback Rattlesnake (Crotalus atrox),
the species targeted by most roundups these days

Wholesale slaughter of rattlesnakes and other venomous snakes is nothing new. Already in 1750 the Swedish naturalist Pehr Kalm observed that "Formerly there were large numbers of these snakes in New Sweden as well as in other parts of North America now occupied by Europeans; however, they have nearly been exterminated." The first recorded bounties were paid to rattlesnake hunters in the 1680s in Masssachusetts. At first, communities and informal groups organized roundups in an attempt to improve public safety—although whether rounding up and killing rattlesnakes actually accomplishes this goal is debatable. Financial gain was not the purpose of early roundups, because the rattlesnakes themselves were considered worthless. In the 1950s, civic organizations such as fire departments, Jaycees, Kiwanis, and the Lions Club took on the role of organizing roundups, which became larger and began to gain more commercial potential; people would pay to attend and would support vendors by buying rattlesnake products. Modern roundup organizers are primarily motivated by raising money for their local community or for charity, and rattlesnake roundups are now more similar in nature to other public events, such as county fairs or rodeos. Most include other events, including occasional educational programs and/or daredevil shows, as well as music, dances, beauty pageants, and carnival rides (some to the point where the rattlesnakes are more of a sideshow, such as the case of the roundup in Freer, Texas). The population of the small communities where these events occur can increase tenfold during roundups, and millions of dollars can enter the local economy, only a small percentage of which come directly from the sale of the rattlesnakes. As a result of geography, competition among one another for visitors, and declining demand and prices for dead rattlesnakes, 36 of the 47 rattlesnake roundups in Texas closed their doors between 1991 and 2006. Texas state laws have also increased the requirements for hunting rattlesnakes, requiring a costly non-game permit and prohibiting collecting snake on roads, and high gas prices have made the costs of hunting snakes over wide areas prohibitive, as many herpers know.

Western Rattlesnake (Crotalus oreganus), the species
by which most Americans are bitten—about 1,500 a year¹

In the past, rattlesnakes gathered for roundups were shot, stomped, buried, or otherwise wasted. Now, at the Texas roundups that remain, all parts of the rattlesnake are used: the venom is ostensibly sold for antivenom production and medical research², the meat cooked and eaten, often right there at the roundup, the rattles, heads, and skins made into curios and souveniers, the gall bladders are sold to a growing Asian-American market, and the remaining guts are used for fish bait. It's likely that the incentive to amass live, healthy rattlesnakes of commercial value has reduced the amount of cruel and inhumane treatment that the snakes suffer, although snakes subjected to the exploitative and sensational daredevil contests or otherwise manhandled for the amusement of the public are certainly not treated ethically, and I doubt such behavior would be tolerated if its target were any other kind of animal.

Dead snakes, mostly homalopsids, for sale at a market in
Indonesia. One cylindrophiid is visible in the upper right.
Photo by Nurcholis Anhari Lubis, National Geographic.

At a broader scale, the economic incentives associated with rattlesnake roundups might also provide incentives for communities to "manage" their local rattlesnake populations and prevent their extinction. Is it possible that rattlesnakes might one day be regulated as a game species and managed, as we manage deer, turkey, quail, and so many other species? Probably not, unfortunately—it is extremely difficult to know how many snakes are in an area, because mark-recapture techniques used for other wildlife are hampered by the low detection probably of individual snakes. As a result, state DWRs aren't very likely to try to manage snakes as game species, even though western diamondbacks in Texas effectively are one, because are traded and have a market value, at roundups and also outside of them. New techniques for monitoring snakes and programs to enhance management efforts for non-game wildlife, such as State Wildlife Action Plans, could help bring about this change. It's an approach that has worked for crocodilians, which are harvested for their meat and skins, and it might be needed to help regulate the billion-dollar global snake trade for food, skins, and pets, particularly in light of emerging markets in southeast Asia. Even some wildlife biologists are reluctant to view venomous snakes as wildlife rather than as pests, and as a result the responsible management of venomous snakes is lacking. For instance, in Georgia there are essentially no restrictions on the harvest of non-threatened "poisonous" snakes, whereas non-venomous snakes and most other non-game wildlife are protected. It might be beneficial if we started managing more herps as game rather than non-game, if only because more people would care if they disappeared. If state wildlife agencies mandated that rattlesnake hunters mark and release a certain portion of their catch, and those hunters hunted the same areas every year and at the same time of year (which already happens), and the same effort were put forth in control areas where no snakes were removed, then a real monitoring program could be built. A modeling exercise showed that a minimum size limit could protect most females, improve hunter profits, and has the potential to result in a sustainable harvest, particularly in the southern part of Texas where western diamondbacks and their populations likely grow rapidly.

Timber Rattlesnake (Crotalus horridus), the species whose
former range overlaps with the most densely-populated areas
of the USA. Even so, most people will never see one.

Evidence from roundup reports suggests that rattlesnake roundups in Alabama & Georgia are indeed negatively affecting populations of eastern diamondbacks, whereas limited evidence suggests that those in Texas and New Mexico [Edit: The New Mexico roundup is now defunct.] might not be affecting western diamondback populations quite so much—the average number of western diamondbacks brought to the Sweetwater roundup (about 2,900; range 800-9,700) did not decrease between 1959 and 2006 ³. It's likely that Timber Rattlesnake roundups in Pennsylvania were once quite harmful, considering the extent of habitat development throughout the range of this species and its reliance on a limited number of communal dens, but a Pennsylvania state law has prohibited the killing of native venomous snakes since the 1970s⁴. Certainly different species of rattlesnakes respond differently to harvest; some are more fecund than others, and differences in lifespan, age at maturity, and biological interactions also play a role. A survey showed that many roundup organizers and rattlesnake hunters believe that roundups do not harm rattlesnake populations, but they also paradoxically think that removing rattlesnakes from land does protect humans, pets, and livestock from rattlesnake bites. In reality, the ecological effects of removing predators are as unknown and controversial as ever. Ecological research has shown that predator control doesnot always accomplish what people think it does. The ecological effects of pumping gasoline fumes into rattlesnake burrows and dens in order to evacuate the residents (which is how the majority of rattlesnakes brought to roundups are collected) are also unclear, although it's hard to imagine that they aren't negative. As for the claim that rattlesnake roundups prevent snakebite, there is little to no data to support or refute this claim, but I find it very hard to conclude that this is true. Snakebite in the USA is already so exceedingly rare compared with that in other countries that any reduction in its incidence would be almost impossible to detect, and fine-scale data to assess the rate of snakebite at a spatial scale relevant to the area hunted for rattlesnake roundups are non-existent. Bill Ransberger, a rattlesnake handler from Sweetwater, says he has been bitten 42 times by rattlesnakes since 1958, a number that represents about one-twentieth of one percent of all the rattlesnake bites in the USA during that time period. There really is no way to evaluate the number of snakebites caused or prevented by rattlesnake roundups.

Active since 1971, in 2012 the Evans County Wildlife Club
decided to discontinue their annual rounding-up of wild
rattlesnakes and now hosts the Claxton Rattlesnake Festival,
which features live captive rattlesnakes which are provided by the
Georgia DNR and displayed but not killed. I took this photo
along Interstate 16 in Georgia in 2009.

All told, habitat destruction and fragmentation are probably worse for rattlesnakes than roundups, although actual estimates of the effects of either on rattlesnake populations are scarce and fraught with uncertainty. The destruction of rattlesnakes at roundups or by other means has probably never benefited livestock or grazing lands or human safety or "the balance of nature". The educational messages at roundups, if they exist, are mostly ones of "bad environmental science and senseless risk-taking". However, it's hard to deny that the roundups, particularly Sweetwater, have become symbols of community identity, publicity extravaganzas, and boons to struggling local economies. Today, between 17 and 25 roundups exist in towns in seven [Edit: four: Texas (10), Oklahoma (5), Georgia (1), and Alabama (1); five if you count the 8 catch-and-release events in Pennsylvania] states. Whether these events transform into more positive, respectful events, or wither and die, probably has more bearing on the future of those communities than on the future of rattlesnakes. But, in keeping with the theme that wildlife-human interactions ought to be more respectful than they are, foresightful roundup organizers might want to imitate those in Georgia and Pennsylvania by beginning to shift the focus of their events towards conserving and learning more about native wildlife, perhaps by focusing on finding rattlesnakes in order to contribute data about them to citizen science programs. It's time we start treating rattlesnakes with the poise and dignity with which they treat us.

If you'd like to do something to encourage rattlesnake roundups to reform, sign this petition, join Rise Against Rattlesnake Roundups, and attend one of these events:

The second annual Texas Rattlesnake Festival, coming up on April 11th and 12th 2015 at Dell Diamond’s United Heritage Center in Round Rock, Texas
Claxton Rattlesnake Festival in Claxton, Georgia, hosted by the Evans County Wildlife Club on March 14th & 15th, a former rattlesnake roundup
Fitzgerald Wild Chicken Festival on March 20th & 21st in Fitzgerald, Georgia, also a former rattlesnake roundup

If you're aware of other reformed rattlesnake roundups or events that portray venomous snakes in a positive way, please let me know in the comments!

1 It's tough to estimate this number because not all snakebites are reported and the species is not reported or may be incorrectly identified in all reported snakebites. To get 1,500, I used data from southern California suggesting that 80-90% of snakebites in that region are from C. oreganus, and extrapolated to the figures reported in the most recent review that ~4,700 human exposures to native venomous snakes occur each year, about half of which are to rattlesnakes. I assumed that half of the 48% of bites from unidentified venomous snakes were also from rattlesnakes. Although the actual figure might be anywhere from 1,000 to 2,000, I'm fairly confident that C. oreganus is the species of rattlesnake by which most Americans are bitten every year, because it's among the most common and widespread. Probably slightly more people are bitten by Copperheads (Agkistrodon contortrix) each year.^↩

2 Herpetologists and physicians claim that venom collected at roundups is unsuitable for use in the manufacture of antivenin, because it is not sterile. Both venom dealers and antivenom producers are quite guarded about the sources that they use, so it is difficult to evaluate this claim or that made by the organizers of rattlesnake roundups that the venom that they collect is put to some useful purpose.^↩

Data from Adams & Thomas 2008 (p.69)

3 Interviews conducted by the same authors found that claims that area hunted has increased or that roundups are importing snakes from far away to sustain themselves are apparently unfounded (except, see the Pennsylvania comment below). At least, snake hunters at Sweetwater and other Texas roundups reported hunting the same dens year after year, and the lower prices paid per pound of snake (see graph) suggest that importing snakes or hunting them over a wider range is not a viable economic strategy. In 1991, 83 of 111 Texas counties within the range of the western diamondback were hunted for roundups, with much of the effort clumped around the communities holding the roundups and at dens adjacent to roads, because the equipment used for pumping gasoline fumes into dens is heavy. It's likely that much less of this land is hunted today, given the number of roundups that have shut down, new TX state laws prohibiting the collection of any snakes from roads, the increased price of gas, the decreasing price of rattlesnake meat & skins, and liability concerns of landowners.^↩

4 It seems that most Pennsylvania roundups have converted to catch-and-release events as per Pennsylvania state law, while a minority import (and kill, and eat) a limited number western diamondbacks from the southwest each year. The state legislature is reluctant to ban the events completely, as they are mainstays of firehouse fund-raisers in almost a dozen rural communities, but they have instituted bag and size limits and a two-day season, restricted collection to male snakes, and mandated that all snakes be marked and released where they were captured (although enforcement is understandably quite challenging). [Edit: Melissa Amarello helped me confirm the truth of this.]^↩

ACKNOWLEDGMENTS

Thanks to Dave Irving, Rich, Augustus Rentfro, and Nurcholis Anhari Lubis for the use of their photographs.

REFERENCES

Adams, C.E. and J.K. Thomas. 2008. Texas Rattlesnake Roundups. Texas A&M University Press, College Station, Texas <link>

Adams, C.E., J.K. Thomas, K.J. Strnadel, and S.L. Jester. 1994. Texas rattlesnake roundups: Implications of unregulated commercial use of wildlife. Wildlife Society Bulletin 22:324-330 <link>

Campbell, J.A., D.R. Formanowicz Jr, and E.D. Brodie Jr. 1989. Potential impact of rattlesnake roundups on natural populations. Texas Journal of Science 41:301-317.

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

Clark, R.W., W.S. Brown, R. Stechert, and H.W. Greene. 2012. Cryptic sociality in rattlesnakes (Crotalus horridus) detected by kinship analysis. Biology Letters 8:523-525 <link>

Douglas, M.E., M.R. Douglas, G.W. Schuett, and L.W. Porras. 2006. Evolution of rattlesnakes (Viperidae; Crotalus) in the warm deserts of western North America shaped by Neogene vicariance and Quaternary climate change. Molecular Ecology 15:3353-3374 <link>

Fitch, H.S. 1998. The Sharon Springs Roundup and prairie rattlesnake demography. Transactions of the Kansas Academy of Science 101:101-113 <link>

Fitzgerald, L.A. and C.W. Painter. 2000. Rattlesnake commercialization: Long-term trends, issues, and implications for conservation. Wildlife Society Bulletin 28:235-253 <link/full-text>

Larsen, E.L. 1957. Pehr Kalm's Account of the North American Rattlesnake and the Medicines Used in the Treatment of its Sting. American Midland Naturalist 57:502-511 <link>

Means, D.B. 2009. Effects of rattlesnake roundups on the Eastern Diamondback Rattlesnake (Crotalus adamanteus). Herpetological Conservation and Biology 4:132-141 <link>

Mushinsky, H.R. and A.H. Savitzky. Position of The American Society of Ichthyologists and Herpetologists Concerning Rattlesnake Conservation and Roundups <link>

Reber, D.L. and A.S. Reber. 1994. Kansas Herpetological Society position paper regarding rattlesnake roundups <link>

Seifert, S.A., L.V. Boyer, B.E. Benson, and J.J. Rogers. 2009. AAPCC database characterization of native U.S. venomous snake exposures, 2001-2005. Clinical Toxicology 47:327-335 <link>

Speake, D.W. and R.H. Mount. 1973. Some possible ecological effects of "rattlesnake roundups" in the southeastern coastal plain. Pp. 267-277 27th Annual Conference of the Southeastern Association of Game and Fish Commissioners <link>

Thomas, J.K. and C.E. Adams. 1993. The social organization of rattlesnake roundups in rural communities. Sociological Spectrum 13:433-449 <link>

Weir, J. 1992. The Sweetwater Rattlesnake Round‐Up: A Case Study in Environmental Ethics. Conservation Biology 6:116-127 <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.

This post will soon be available in Spanish!

Spitting cobras have been known for centuries,
as you can see from this report published in the
Journal of the Bombay Natural History Society in 1900¹

A clever comic from birdandmoon
highlighting the fact that king cobras
are not true cobras

Cobras are some of the most iconic snakes in the world, instantly recognizable by their hoods even to those who have never seen one. They are also among the most dangerous snakes—fast-moving, with potent neurotoxic venom, cobra bites cause injury or death to many people in Asia and Africa. Cobras are elapids, together with coralsnakes, mambas, kraits, seasnakes, and numerous terrestrial Australian snakes both well-known and obscure. What unites these ~350 species of snakes is their short, immovable, and hollow ("proteroglyphous") fangs. Elapids probably evolved in Asia between 25 and 30 million years ago. By 16 million years ago, cobras were found in Europe, where they no longer live, and in Asia and Africa, where they are still found today. The core cobra clade consists of three small genera (Hemachatus, Aspidelaps, and Walterinnesia) and one large one, Naja. Other hooded snakes that are usually called "cobras" include tree cobras (genus Pseudohaje), whose placement remains uncertain, and the king cobra (Ophiophagus hannah), which is probably more closely related to mambas than it is to true cobras. Ironically, most people, if asked for a species of cobra, would almost certainly come up with the king first. But, probably they would think of a spitting cobra second, and with good reason from an evolutionary perspective, as we shall see.

Mozambique Spitting Cobra (Naja mossambica)

Almost all spitting cobras belong to the genus Naja, a large genus that comes from the Sanskrit word for snake, nāga. Literature buffs will recognize the name of the cobras in Kipling's Rikki Tikki Tavi, which led to the name of the snake Nagini in the Harry Potter books. Over the past 50 years, the number of species within the genus Naja has risen from six to 29², and more will probably become recognized in the future. At least 15 of these species can spit their venom through the air. The best of them are capable of aiming at targets the size of a human face with >90% accuracy up to 8 feet away. This adaptation represents the only purely defensive use of venom by any snake. Vipers and other venomous snakes occasionally eject venom from their fangs into the air, particularly when being handled, but these snakes are not aiming at anything, so they are not really using their venom defensively. Spitting in cobras is an adaptation that involves changes to the morphology of the fangs, their head musculature, and the chemistry of their venom.

Fangs of cobras progressively adapted for spitting.

Dotted lines show the venom canal, dark arrows indicate
the flow of water injected into the top of the fang.

From Bogert 1943

Left: "normal" non-spitting cobra fang (Naja kaouthia)

Right: spitting cobra fang (Naja pallida)
The sutures are visible above the exit orifices.
From Young et al. 2004

All snake fangs are modified teeth provisioned with grooves that vary in depth and degree of closure. In vipers and elapids, the grooves are completely closed, forming hollow tubes, along the front edge of which a narrow suture can still be seen where the ridges forming the tube have come together in the developing embryo. In spitting cobras, the inside of this tube contains ridges, which act like rifling in a gun barrel to impart spin on the venom. The discharge orifice, located near but not at the point of the tooth (like a hypodermic needle), is large and elliptical in non-spitting cobras but small and round in spitting cobras, which has the same velocity-increasing effect as putting your thumb most of the way over the end of a garden hose. A sharp 90° bend at the distal end directs the jet of venom forward or slightly upward, instead of downward as in most snakes, and venom stream spins towards the exit orifice, which prevents the flow from slowing down as it goes through the sharp bend at the exit (similar strategies are used in pressure washers). These adaptations of the fang enable a cobra to spit venom in defense but do not prevent venom injection when biting, which is used both defensively and for killing prey. In fact, spitting cobras can meter the duration of their venom pulse, which is normally about five times longer during biting (1/4th of a second) than during spitting (1/20th of a second). This affects the quantity of venom ejected, which varies considerably from bite to bite and may consist of up to 100 times more venom than the fairly consistent 1.9-3.7 milligrams (~1/10th of a milliliter) of venom per spit. Most estimates suggest that a single cobra has enough venom to spit about 40-50 times consecutively. The fluid dynamics of such tiny volumes over relatively long distances are complex, and spitting cobra venom has shear-reducing properties, such as high surface tension and viscosity, which hold the droplets together as they fly through the air. Some species of spitting cobra eject their venom as a spray, whereas others eject two pressurized parallel streams. Reports of the maximum distance achievable by a spitting cobra vary from surely exaggerated distances of 12 feet or more to more believable (though still impressive) distances of five to eight feet.

Venom spray patterns of Red Spitting Cobras (Naja pallida)
From Westhoff et al. 2005

Middle: Examples of head movement patterns of Black-necked

Spitting Cobras (Naja nigricollis). Black dots represent the

positions of the upper and lower jaws, red dots indicate the

period of venom spitting.
From Westhoff et al. 2005

Bottom: Congruence between target (back; blue)
and cobra’s head (red; front plot) motion during spitting.

Data are offset 180 ms to reflect the cobra's reaction time.
From Westhoff et al 2010

Unlike vipers, cobras cannot move their fangs, so in order to accurately hit their targets, they move their heads instead. When a spitting cobra spits, it opens its mouth slightly and contracts the muscles around the venom glands so that a small amount of venom is forced out of the glands and down the venom canal of the fangs. At the same time, the upper lip scales and the fang sheaths are levered up out of the way and the maxilla levered down, removing soft tissue barriers between the venom glands and the fangs as well as between the exit orifices of the fangs and the air around them³. Most often, the spit is accompanied by slight movements of the head in response to change in direction of the target, which disperse the venom over an area about the size of a human face. Measurements indicate that more head rotation corresponds to a larger area covered by the venom stream, allowing cobras to adjust for target size and distance. Splattering of the venom when it hits the target and partial disintegration of the venom stream as it travels through the air increase the chance that at least some of the venom will hit the target's eye. Consequently, cobras only need to aim at the center of the face, rather than precisely at the eyes, in order to hit the eyes 90-100% of the time. They adjust for target movement by using a strategy familiar to any Space Invaders or Galaga player: firing not at where you are but at where you're going to be. Chameleons, archer fish and spitting spiders do the same kind of thing. In some species venom spitting is often accompanied by an audible hiss as the cobra exhales, but in contrast to early reports that spitting cobras propelled their venom with their breath, this is not an essential part of the spitting process. In one experiment, spitting cobras restrained in tubes did not seem to suffer from reduced spitting ability or range. How do they choose their targets? Cobras have good vision and moving human faces are the stimuli that normally elicit spitting, although in lab experiments they will also spit at masks, photos of human faces, and even plain ovals without eyes, as long as they are moving, but not at moving triangles. Adult cobras will not spit at stationary human faces or moving human hands, although newly hatched cobras will spit at nearly anything, even if it is beyond their maximum target distance, including human hands, unhatched eggs, other baby cobras, and even their own reflection. Hatchling cobras also spit more of their venom, proportionally, and rotate their heads in a more pronounced fashion; their spitting performance improves following their first shed. Like many stereotypical snake defensive behaviors, most spitting cobras apparently habituate to humans when in captivity and are disinclined to spit after a while, although some spit without hesitation and willingness to express defensive behavior is very variable from individual to individual.

Sumatran Spitting Cobra (Naja sumatrana)

Although the color and consistency of spat venom does not change noticeably with repeated spitting, the venom chemistry of at least one species, Red Spitting Cobras (Naja pallida), changed over 10 minutes of repeated spitting. The quantity of venom remained the same and the toxin concentration rose over the first 20 spits, but both decreased afterward. The first five spits contained a protein that was not found in later spits, which might be involved in venom storage. Although this protein is non-toxic, most of the other molecules in spitting cobra venom are not. African spitting cobra venom is rich in cytotoxins and PLA₂s, which cause tissue damage; spitting cobra cytotoxins lack certain acidic proteins, which frees them to damage tissues in the eyes. If even a small quantity of venom contacts the eye it causes instant, intense pain and damage to the cornea and mucous membranes. If left untreated, it can lead to blindness. Treating spitting cobra venom in your eyes involves flushing it out with water for 15-20 minutes. Anti-inflammatory eye drops are sometimes prescribed.

Rinkhals (Hemachatus haemachatus)

The 29 living species of Naja fall into four groups: a basal Asian clade of eleven species (subgenusNaja, including six accomplished spitting members, two non-spitters, and three species of intermediate spitting ability), an African spitting group of eight species (subgenus Afronaja), and two African non-spitting groups of six and four species, respectively (subgenus Uraeus, found mostly in open areas, and subgenus Boulengerina, found mostly in forests). This pattern of species relationships suggests that spitting evolved more than once! In Asia, the six spitting cobras (Naja siamensis, N. sumatrana, N. sputatrix, N. mandalayensis, N. samarensis, and N. philippinensis⁴) are probably one another's closest relatives, and their closest cousins are a group of three cobra species (Naja atra, N. kaouthia, and N. sagittifera) with somewhat modified fangs and intermediate spitting ability. They can spit their venom, but they do so rarely and with less accuracy than the "true" spitters. The remaining Asian cobras, Naja naja and Naja oxiana, do not spit their venom but nevertheless are more closely related to Asian spitting cobras than to other cobras. This means that venom spitting arose independently in the common ancestor of the seven species of African spitting cobras (N. pallida, N. nubiae, N. katiensis, N. nigricollis, N. ashei, N. mossambica, and N. nigricincta), which form a monophyletic group sometimes referred to as Afronaja. Their cousins, the other African Naja (i.e., subgenera Uraeus and Boulengerina), do not spit. Finally, a member of one of those small genera, a very interesting cobra known as the rinkhals (Hemachatus haemachatus) also spits its venom, indicating that venom spitting has evolved three times in cobras (or, alternatively, been lost twice, in Naja naja/N. oxiana and in the common ancestor of Uraeus and Boulengerina, with a third partial loss in N. atra & kin). Because the details of spitting behavior and morphology differ slightly among the three groups of spitting cobras, the former hypothesis is more likely.

The largest Giant Spitting Cobras (Naja ashei) can top 9 feet.
This species was described in 2007.
From Wüster & Broadley 2007

Why do some cobras spit their venom? Herpetologist Thomas Barbour, who published one of the first studies on spitting cobras, thought that spitting cobras evolved venom spitting for much the same reason that rattlesnakes were thought to have evolved their rattles—to alert large ungulates to their presence and avoid getting stepped on. He was speculating in the absence of any direct evidence when he wrote in 1922 that "The African veldt is the only other region in the world where snakes abound and where hoofed animals grazed in numbers comparable with those of the western American plains. Snakes probably found the heavy antelopes equally dangerous though unwitting foes and many antelopes probably suffered from snake bite. No rattle was evolved, however but some of the common veldt-ranging snakes secured protection in another way. Several common cobras and cobra-allies learned to expel their poison in a fine spray for very considerable distances, and with a fairly shrewd aim at the eye."

Nearly 100 years after Barbour, we have just as little direct evidence—published field observations of spitting cobras interacting with their non-human predators are non-existent. The main reason we now think that the evolutionary cause of these adaptations isn't so simple is that spitting is too old. Molecular dating methods suggest that African spitting cobras evolved about 15 million years ago, whereas the spread of open grasslands and their characteristic megafauna (elephants, etc.) didn't happen until about 5 million years ago. Asian spitting cobras don't inhabit open grasslands, so this hypothesis seems unlikely to explain their evolution either. African spitting cobras are eaten by birds and other snakes, against which spitting venom would be a relatively ineffective weapon, and in captive experiments cobras do not spit at mounted bird specimens. Given what we know about face targeting, it's possible that spitting may represent a defense that is specifically adapted for use against primates [Edit: Harry Greene hinted at this idea in his recent book,Tracks and Shadows]. Barbour's comment that "...[venom spitting] must antedate man's coming, for contact between man and the snakes can hardly be conceived as sufficiently frequent to account for the modification" may be technically correct, but the evolution of spitting cobras coincides roughly with the evolution of apes in Asia and Africa, which (as we all know) are diurnal primates with forward-facing eyes, some of which are omnivorous and many of which (ourselves included) habitually kill snakes either for food or in defense. Could it be that spitting cobras evolved their venom spitting capacity to deal with threats from our own ancestors? Only further research into the co-evolution of apes and snakes can tell us. Perhaps this is why, although certain toads, salamanders, insects, and scorpions can also eject their toxin defensively, spitting cobras are by far the longest- and best-known organisms to do so. Clearly, much remains to learn about them and their fascinating habits.

1 The cobra in this account was undoubtedly Naja mandalayensis, which was described by Joe Slowinski & Wolfgang Wüster 100 years later. Before 2000, no spitting cobras were known from Burma. Cobra specimens with fangs highly modified for spitting from northeastern India may represent a seventh species of undescribed Asian spitting cobra.^↩

2 This number includes species of cobras formerly placed in the genera Boulengerina and Paranaja, both of which have been synonymized with Naja in the last 15 years. In part, the reason for this change is that, when scientists realized that some species of Naja were more closely related to Boulengerina and Paranaja than they were to other Naja (i.e., that Naja was paraphyletic), they were reluctant to split up the genus Naja because they didn't want to change the name of medically-important snakes and create potential confusion. However, a few sources use Afronaja and other other subgenera as full genera anyway.^↩

3 The fang sheath is soft tissue that completely surrounds the fang at rest, including at the top, which keeps the venom from dribbling out. In other venomous snakes, physical contact with a target is required for displacement of the fang sheath and release of venom, but spitting cobras have co-opted the movements normally used for jaw-walking over a prey item (the ‘pterygoid walk’) to free their fangs for spitting in the absence of any external physical contact. This has been termed the "buccal buckle" (pronounced "buckle buckle") by the research group of Bruce Young, of Kirksville College, which has studied several aspects of the functional morphology of spitting in cobras.^↩

4 Naja philippinensis is the only spitting cobra species with pronounced sexual dimorphism in discharge orifice size—females have longer orifices less well-adapted for spitting, whereas males have small round orifices. The evolutionary causes and consequences of this dimorphism are not understood.^↩

This post is part of a Reptile and Amphibian Blogging Network (RAmBlN) online event called #CrawliesConverge. We are writing about convergent evolution in reptiles and amphibians. Find our event schedule here, or follow on Twitter or Facebook.

ACKNOWLEDGMENTS

Thanks to Dan Rosenberg and Ray Hamilton for allowing me to use their photos.

REFERENCES

Barbour, T. 1922. Rattlesnakes and spitting snakes. Copeia 105:36-38 <link>

Berthé, R., S. de Pury, H. Bleckmann, and G. Westhoff. 2009. Spitting cobras adjust their venom distribution to target distance. Journal of Comparative Physiology A 195:753–757 <link>

Berthé, R.A., G. Westhoff, and H. Bleckmann. 2013. Potential targets aimed at by spitting cobras when deterring predators from attacking. Journal of Comparative Physiology A 199:335-340 <link>

Bogert, C.M. 1943. Dentitional phenomena in cobras and other elapids, with notes on adaptive modifications of fangs. Bulletin of the American Museum of Natural History 81:285-360 <link>

Cascardi, J., B.A. Young, H.D. Husic, and J. Sherma. 1999. Protein variation in the venom spat by the red spitting cobra, Naja pallida (Reptilia: Serpentes). Toxicon 37:1271-1279 <link>

Chu ER, Weinstein SA, White J, Warrell DA (2010) Venom ophthalmia caused by venoms of spitting elapid and other snakes: Report of ten cases with review of epidemiology, clinical features, pathophysiology and management. Toxicon 56:259-272 <link>

Goring Jones, M.D. 1900. Can a cobra eject its poison? Journal of the Bombay Natural History Society 8:376 <link>

Hayes, W., S. Herbert, J. Harrison, and K. Wiley. 2008. Spitting versus biting: differential venom gland contraction regulates venom expenditure in the Black-Necked Spitting Cobra, Naja nigricollis nigricollis. Journal of Herpetology 42:453-460 <link>

Keogh, J.S. 1998. Molecular phylogeny of elapid snakes and a consideration of their biogeographic history. Biological Journal of the Linnean Society 63:177-203 <link>

Petras, D., L. Sanz, Á. Segura, M. Herrera, M. Villalta, D. Solano, M. Vargas, G. León, D.A. Warrell, and R.D.G. Theakston. 2011. Snake venomics of African spitting cobras: toxin composition and assessment of congeneric cross-reactivity of the pan-African EchiTAb-Plus-ICP antivenom by antivenomics and neutralization approaches. Journal of Proteome Research 10:1266-1280 <link>

Rasmussen, S., B. Young, and H. Krimm. 1995. On the ‘spitting’ behaviour in cobras (Serpentes: Elapidae). Journal of Zoology 237:27-35 <link>

Slowinski, J.B. and W. Wüster. 2000. A new cobra (Elapidae: Naja) from Myanmar (Burma). Herpetologica 2000:257-270 <link>

Szyndlar, Z. and J.C. Rage. 1990. West Palearctic cobras of the genus Naja (Serpentes: Elapidae): interrelationships among extinct and extant species. Amphibia-Reptilia 11:385–400 <link>

Triep, M., D. Hess, H. Chaves, C. Brücker, A. Balmert, G. Westhoff, and H. Bleckmann. 2013. 3D Flow in the Venom Channel of a Spitting Cobra: Do the Ridges in the Fangs Act as Fluid Guide Vanes? PLoS ONE 8:e61548 <link>

Wallach, V., W. Wüster, and D.G. Broadley. 2009. In praise of subgenera: taxonomic status of cobras of the genus Naja Laurenti (Serpentes: Elapidae). Zootaxa 2236:26-36 <link>

Westhoff, G., K. Tzschätzsch, and H. Bleckmann. 2005. The spitting behavior of two species of spitting cobras. Journal of Comparative Physiology A 191:873-881 <link>

Westhoff, G., M. Boetig, H. Bleckmann, and B.A. Young. 2010. Target tracking during venom ‘spitting’by cobras. Journal of Experimental Biology 213:1797-1802 <link>

Wüster, W. and D.G. Broadley. 2007. Get an eyeful of this: a new species of giant spitting cobra from eastern and north-eastern Africa (Squamata: Serpentes: Elapidae: Naja). Zootaxa 1532:51-68 <link>

Wüster, W., S. Crookes, I. Ineich, Y. Mané, C.E. Pook, J.F. Trape, and D.G. Broadley. 2007. The phylogeny of cobras inferred from mitochondrial DNA sequences: Evolution of venom spitting and the phylogeography of the African spitting cobras (Serpentes: Elapidae: Naja nigricollis complex). Molecular Phylogenetics and Evolution 45:437-453 <link>

Wüster, W. and R.S. Thorpe. 1992. Dentitional phenomena in cobras revisited: spitting and fang structure in the Asiatic species of Naja (Serpentes: Elapidae). Herpetologica:424-434 <link>

Young, B.A., M. Boetig, and G. Westhoff. 2009. Functional bases of the spatial dispersal of venom during cobra “spitting”. Physiological and Biochemical Zoology 82:80-89 <link>

Young, B.A., M. Boetig, and G. Westhoff. 2009. Spitting behaviour of hatchling red spitting cobras (Naja pallida). The Herpetological Journal 19:185-191 <link>

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

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